Brenda M. Speek1,2,3*
Afnan Khalil Ahmad Suleiman3
Eline Keuning3Valentina Sechi2Cees J. N. Buisman1,2
T. Martijn Bezemer2,4- 1Environmental Technology, Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen, Netherlands
- 2Wetsus, European Centre of Excellence for Sustainable Water Technology, Leeuwarden, Netherlands
- 3Bioclear Earth B.V., Groningen, Netherlands
- 4Aboveground Belowground Interactions Group, Institute of Biology, Leiden University, Leiden, Netherlands
The soil microbiome drives soil nutrient cycling and is intrinsically linked to plant productivity in agriculture. Archaea are members of many soil microbiomes and play important roles in nutrient cycling, particularly in the carbon and nitrogen cycle. Many archaeal groups contribute to both carbon and nitrogen cycles, but their dual roles are often underappreciated. For instance, ammonia-oxidizing archaea couple ammonia oxidation to carbon fixation, contributing to carbon sequestration in soils. Methanogenic archaea use ATP produced through methanogenesis for nitrogen fixation. N-DAMO archaea directly couple carbon and nitrogen cycling through nitrate-dependent anaerobic methane oxidation, while haloarchaea contribute to carbon sequestration and denitrification. Here, we synthesize the latest research regarding the dual roles of archaea in carbon and nitrogen cycling in agricultural soils. We pay special attention to how nutrient input influences these roles. We show that the relevance of the processes is highly context dependent. In addition, we identify several research directions that will help harness the difference roles of archaea in carbon and nitrogen cycling to increase agricultural productivity and sustainability. Finally, we showcase that abundance and activity of archaea in the soil microbiome could be steered through nutrient input or microbiome engineering strategies.
1 Introduction
Nutrient cycling is a central function of agricultural soils, maintaining fertility and supporting crop production (Jiao et al., 2019a). Because soil productivity directly affects food production, agricultural soils are typically closely managed (Tully and Ryals, 2017; Kopittke et al., 2019). Management strategies, such as nutrient input, directly impact biochemical nutrient cycling (Frink et al., 1999; Tully and Ryals, 2017). Understanding which processes drive nutrient cycling and how they increase soil productivity is therefore critical (Nealson and Stahl, 1997).
Key players in biochemical nutrient cycling are microbes (Sahu et al., 2017). These microorganisms contribute to maintain soil functionality and crop growth, by contributing to many different processes in soil nutrient cycling, including nitrification, nitrogen (N) fixation, carbon (C) turnover and phosphorus solubilization (Falkowski et al., 2008; Buée et al., 2009; Hartmann and Six, 2022). Bacteria are generally the most abundant group of microorganisms in soils (Bates et al., 2011; Wang et al., 2020). One bacterial species can perform multiple roles and thereby contribute to different nutrient cycles at the same time (Wang X. et al., 2024). Numerous studies have examined the roles of bacteria in agricultural soils; however, archaea have not received the same attention yet.
While previously considered extremophiles (Mehta and Baross, 2006; Dekas et al., 2009), this view has changed, as archaea have been found in common environments such as soils (Bates et al., 2011). Archaea are important members of the soil microbiome (Chen et al., 2008; Moissl-Eichinger et al., 2018; Naitam et al., 2023) and several archaeal species have been found to interact with plants (Chow et al., 2022). Specifically, archaea can improve plant growth through direct and indirect mechanisms; including contributing to biochemical nutrient cycling, mitigation of stresses in plants, phosphate solubilisation, siderophore production and degradation of pollutants (Odelade and Babalola, 2019; Alori et al., 2020; Singh et al., 2023; Martínez-Espinosa, 2024; Ventura et al., 2025). Particularly haloarchaea, known for their adaptation to saline environments, are frequently mentioned for their plant growth-promoting properties (Naitam et al., 2023), while many other archaeal species are known to play roles in biochemical nutrient cycling (Falkowski et al., 2008; Schleper and Nicol, 2010; Offre et al., 2013; Wright and Lehtovirta-Morley, 2023). The impact of archaea on plant growth and nutrient cycling underlines the importance of archaea in agricultural soils and plant productivity.
Agricultural soils can be divided into drylands, land used for crop growth and grasslands, and wetlands, including paddy fields (Jiao et al., 2019a). Dry- and wetlands typically harbour distinct archaeal communities due to differences in oxygen availability, irrigation and management practices (Jiao et al., 2019b). The most dominant archaeal phyla in soils are often the Thaumarchaeota and Euryarchaeota, recently reclassified as Methanobacteriota (Vaksmaa et al., 2016; Yuan et al., 2018; Clark et al., 2020; Megyes et al., 2021; Liu et al., 2022; Saghaï et al., 2022; Zhang et al., 2023). Both phyla have important roles in C and N turnover (Schleper and Nicol, 2010; Offre et al., 2013; Naitam and Kaushik, 2021).
The C- and N-cycles are essential in agriculture: they provide essential nutrients that support plant growth, but at the same time, can result in the release of several potent greenhouse gases (GHGs) (Shah et al., 2020). N plays an important role in plant development, and its deficiency can decrease plant growth, hinder root development and decrease plant dry mass (Frink et al., 1999). N application, in the form of chemical or organic fertilizer, is therefore essential for plants to obtain sufficient N (Ding et al., 2005; Diaz et al., 2006). Both bacteria and archaea play important roles in the transformation of N into ammonium (NH4+) and NO3− (Cui et al., 2017), the primary sources of N for plants. Members of the Thaumarchaeota, specifically the ammonia-oxidizing archaea (AOA), are highly abundant in grasslands and crop lands, composing up to 95% of the total archaeal community (Clark et al., 2020; Megyes et al., 2021; Liu et al., 2022; Saghaï et al., 2022; Zhang et al., 2023). However, certain bacteria and archaea can transform nitrate (NO3−) into nitrous oxide (N2O), a GHG 273 times more potent than carbon dioxide (CO2), through denitrification (Spiertz, 2010; Hirsch and Mauchline, 2015).
The C-cycle influences key soil functions. Soil organic matter (SOM), which consists of approximately 58% organic C, is crucial for retaining soil structure and the water holding capacity of the soil (Manns et al., 2016). The soil microbiome is essential for the generation of SOM and plays a small role in sequestering atmospheric CO2 (Kallenbach et al., 2016; Jiang et al., 2022). Through microbial respiration, SOM is returned to the atmosphere as CO₂. Under anoxic conditions, methane (CH4), another potent GHG with a global warming potential 37 times greater than CO₂, is produced by methanogenic archaea (Derwent, 2020). However, methanotrophic archaea and bacteria can mitigate CH4 emissions by utilizing CH₄ for energy generation (McGlynn, 2017). Both methanogens and methanotrophs belong to the phylum of Methanobacteriota. Methanobacteriota thrive in anaerobic conditions, comprising more than 50% of the archaeal community in these environments (Vaksmaa et al., 2016; Yuan et al., 2018).
Above, four specific archaeal groups are mentioned: AOA, methanogens, methanotrophs and haloarchaea. These archaeal groups are typically characterized by a single well-known characteristic, i.e., ammonia (NH3) oxidation in AOA, CH4 production in methanogens and CH4 oxidation in methanotrophs, or salt tolerance and plant growth-promoting potential for haloarchaea. Yet, all four of these archaeal groups have the potential to contribute to both C- and N-cycling (Figure 1; Table 1). For example, AOA make contributions to N- and C- cycling through N2O formation and CO2 fixation (Pratscher et al., 2011). Methanogens contribute to N-cycling via N2 fixation (Leigh, 2000; Dekas et al., 2009). A specific subset of the anaerobic methanotrophs, N-DAMO archaea, contribute to NO3− reduction and DNRA (Dissimilatory Nitrate Reduction to Ammonium) (Raghoebarsing et al., 2006; Wang et al., 2025). In contrast, while haloarchaea are not typically found in agricultural soils, they occupy a niche in saline environments, where they contribute to C turnover and denitrification (Torregrosa-Crespo et al., 2020a; Miralles-Robledillo et al., 2024).
Figure 1. A simplified depiction of the carbon and nitrogen cycle in soil. 1) Biological Nitrogen Fixation (BNF), 2) Ammonia oxidation, 3) Nitrite oxidation, 4) Nitrate reduction, 5) Dissimilatory Nitrate Reduction to Ammonia (DNRA), 6) Nitrite reduction, 7) Nitric oxide reduction, 8) Nitrous oxide reduction, 9) Methane oxidation, 10) Methanogenesis, 11) Carbon assimilation, 12) Methanogenesis, 13) Respiration, and 14) Carbon fixation.
Table 1. Overview of the relevant archaeal groups and their roles in C- and N-cycling.
This review aims to increase the understanding of dual roles of AOA, methanogens, N-DAMO archaea, and haloarchaea in C- and N-cycling in agricultural soils. We highlight the potential ecological significance of their dual roles, with particular emphasis on their contributions to GHG emissions. By synthesizing current knowledge on the dual roles of these four archaeal groups in C- and N-cycling, we address the following questions: (1) Under which agricultural conditions are their roles in C- and N-cycling most relevant? (2) How does nutrient addition influence their activity and function? and (3) How can existing knowledge be used to improve current agricultural management practices or which future research is needed before current management practices can be improved? We aim to contribute to identifying research gaps and new research directions which will help in the development of agricultural strategies that utilize the underrecognized functions of archaea in C- and N-cycling to increase agricultural productivity and sustainability. To address these questions, we first provide an overview of the four archaeal groups that participate in both C- and N-cycling, highlighting their ecological niches and contributions to both nutrient cycles.
2 Archaeal groups with dual roles in C- and N-cycling
2.1 Ammonia-oxidizing archaea (AOA)
AOA catalyse the first and rate-limiting step of nitrification by oxidizing NH3 to nitrite (NO2−) (Könneke et al., 2005; Francis et al., 2007). AOA are often compared to ammonia-oxidizing bacteria (AOB), their bacterial counterparts that catalyse the same reaction. AOA and AOB occupy different ecological niches, but AOA can dominate in abundance under certain environmental conditions (Leininger et al., 2006; Sterngren et al., 2015; Mukhtar et al., 2019; Clark et al., 2020). All AOA fall into the class of Nitrososphaeria, within the phylum Thermoproteota (Rinke et al., 2021). Nitrososphaeria are often the most dominant archaeal class in soils, composing over 70% of the total archaeal community (Megyes et al., 2021; Liu et al., 2022; Saghaï et al., 2022; W. Hu et al., 2022). The order Nitrososphaeria has been classified into several lineages with different characteristics based on NH3 affinity, optimum pH and urea usage, which allows the different lineages to occupy specific ecological niches (Lehtovirta-Morley et al., 2024; Zheng et al., 2024).
2.2 Haloarchaea
Haloarchaea thrive in saline and hypersaline environments (Oren, 2002; Baker et al., 2024). All haloarchaea belong to the class of Halobacteria within the phylum Methanobacteriota (Garrity et al., 2001). Halobacteria have been found to compose 46.5–89.5% of the total archaeal community in saline soils (Zhao S. et al., 2024). While typically not dominant in other soil types, they have been detected in drylands, where they can make up 20% of the archaeal community (Hu W. et al., 2022). Due to their reported plant growth–promoting properties, haloarchaea have been proposed as potential inoculants to enhance plant tolerance to different stressors (Yadav et al., 2015; Naitam et al., 2023; Mukhtar et al., 2024).
2.3 Methanogenic archaea
Methanogenic archaea are well-known for their exclusive contribution to CH4 production, as bacteria do not perform this process (Bapteste et al., 2005). While exceptions have been discovered, many methanogens belong to the phylum of Methanobacteriota (Wu et al., 2024). Due to their anoxic nature, methanogens are important contributors to C-cycling in waterlogged soil such as wetlands and paddy fields (Narrowe et al., 2019; Asakawa, 2021). Methanogenic archaea contribute up to 350–420 Tg of CH4 emissions per year (Lyu et al., 2018), with approximately 50% of CH4 emissions originating from wetlands and rice paddy fields (Lyu et al., 2018). Even though methanogens can play a prominent role in CH4 emissions in aerated soils (Angel et al., 2012; Angle et al., 2017), they have a low abundance compared to other archaeal groups in these environments (Angel et al., 2012; Alves et al., 2022).
2.4 N-DAMO archaea
As this review focuses on archaea that impact C- and N-cycling, here the focus will be specifically on archaea that perform nitrate-dependent anaerobic methane oxidation (N-DAMO). N-DAMO archaea belong to the genus of Candidatus (Ca.) Methanoperedens, within the phylum of Methanobacteriota (Raghoebarsing et al., 2006; Zehnle and Schoelmerich, 2025). N-DAMO archaea were first discovered in a consortium with N-DAMO bacteria, who use NO2− for anaerobic oxidation of CH4, producing CO2 and nitrogen gas (N2) (Raghoebarsing et al., 2006). N-DAMO archaea reduce NO3− during anaerobic CH4 oxidation, forming CO2 and NO2− through reverse methanogenesis (Haroon et al., 2013; Wei et al., 2022). N-DAMO archaea are found in wetlands and paddy fields (Ding et al., 2016; Wang et al., 2022). In soils they are often detected in association with NO2−-utilizing bacteria who use the NO2− produced by N-DAMO archaea (Ding et al., 2016). Many ANME (anaerobic methanotrophic archaea) have partnerships with sulphate reducing bacteria for electron shuttling, however, Ca. Methanoperedens does not need this symbiotic reaction (Zehnle and Schoelmerich, 2025).
3 Archaeal contribution to nitrogen cycling
3.1 Nitrification
AOA contribute to N-cycling in two major ways: (1) through NH3 oxidization, and (2) by producing N2O (Santoro et al., 2011). AOA and AOB perform oxidation of NH3 to hydroxylamine (NH2OH) using the enzyme ammonia-monooxygenase (AMO) (Zhalnina et al., 2012). In most AOA species, AMO exhibits a higher substrate affinity compared to AOB (Zhalnina et al., 2012). Under conditions with low N availability, AOA can therefore outcompete AOB (Ouyang et al., 2017). Moreover, AOA are known for their tolerance of acidic conditions (Gubry-Rangin et al., 2010; Yao et al., 2011; Zhalnina et al., 2012) and obligate acidophilic AOA species have been described (Lehtovirta-Morley et al., 2024). Under acidic conditions, NH₃ availability is reduced, leading to conditions that favour AOA (Prosser and Nicol, 2012). AOA are however not limited to acid soils and can grow in a wide pH range from acidic to alkaline (Prosser and Nicol, 2012). By contrast, AOB prefer soils at neutral pH (Robinson et al., 2014; Du et al., 2022). Finally, AOA have a higher affinity for oxygen than AOB, which can give them a growth advantage under oxygen-limited conditions (Du et al., 2022).
AMO has been identified as the enzyme catalysing the oxidation of NH3 to NH2OH (Vajrala et al., 2013). The process of NH2OH conversion to NO2− is less well understood. AOB convert NH2OH to nitric oxide (NO) using hydroxylamine dehydrogenase (HAO), whereas another unidentified enzyme converts NH2OH to NO2− (Caranto and Lancaster, 2017). AOA lack the gene encoding HAO, and this part of the NH3 oxidation process therefore remains unclear (Walker et al., 2010) (Figure 2).
Figure 2. Key enzymes and simplified pathways involved in carbon and nitrogen cycling, specifically focused on the reactions mentioned in this review. The color of the arrow corresponds to the archaeal group involved in the reaction: Green = methanogens, Orange = AOA, purple = N-DAMO archaea, and blue = Halarchaea. Unidentified enzymes are indicated as “?”. NH2OH = hydroxylamine, NH4OH = ammonium hydroxide, 3-HP/4-HB = 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB) cycle, RuBisCO = ribulose-1,5-bisphosphate carboxylase/oxygenase, amoA = ammonia monooxygenase, hao = hydroxylamine oxidoreductase, hcp = hydroxylamine reductase, nxr = nitrite oxidoreductase (has not been identified in archaea), nirS/nirK = nitrite reductase, norB = nitric oxide reductase, nosZ = nitrous oxide reductase, narG/narH = nitrate reductase, mcr = methyl-coenzyme M reductase (involved in methanogenesis and reverse methanogenesis).
Nevertheless, both groups can produce N2O during NH3 oxidation. In AOB, several routes of N2O formation have been proposed, including: 1) N2O formation via the oxidation of NH2OH to NO by HAO, 2) NO2− reduction to NO via nitrite reductase (NIR) and NO reductase (NOR), and 3) oxidation of NH2OH by cytochrome P460 (Ritchie and Nicholas, 1972; Poth and Focht, 1985; Shaw et al., 2006; Caranto et al., 2016). Studies into the N2O production mechanism of marine AOA give several insights into the possible pathways of N2O production in AOA. Using isotope tracing experiments, Wan et al. (2023) found that AOA have several pathways of N2O production, depending on environmental conditions (Figure 2). Both NH2OH and NO were identified as key intermediates in AOA metabolism for N2O formation. Most notably, N2O formation was observed via NH2OH oxidation and reaction of NH2OH with NO. Under low oxygen conditions, nirK (copper-containing nitrite reductase) might be involved in the process of converting NO2− to NO and O2 (Kraft et al., 2022; Hernández-Magaña and Kraft, 2024). O2 produced during the process can subsequently be used during NH3 oxidation. NO was further converted into N2O and N2 through the action of yet to be identified enzymes. nirK in AOA is likely involved in the generation of NO from both NO2− and NH2OH, indicating several pathways for N2O production (Kobayashi et al., 2018). Jung et al. (2014b) studied the N2O production by five soil AOA. N2O production by soil AOA primarily took place via NH2OH oxidation and via nitrifier denitrification from NO2−, indicating that soil AOA also have different pathways for N2O production (Jung et al., 2014b).
In two marine AOA species, N2O production increased with decreasing oxygen concentrations (Qin et al., 2017). It is unclear if this is also the case for soil AOA. When the N2O production of Nitrososphaera viennensis, a soil AOA, Nitrosopumilus maritimus, a marine AOA, and Nitrosospira multiformis, an AOB, were compared, no increase in N2O production was observed at lower oxygen concentrations, while more N2O production was measured for the AOB species (Stieglmeier et al., 2014). Niche differentiation within the AOA can play a role in N2O emission by different AOA species (Jung et al., 2019). Ca. Nitrosotenuis chungbukensis from the order Nitrosopumilales, demonstrated higher yields of N2O than Ca. Nitrosocosmicus oleophilus from the order Nitrososphaerales (Jung et al., 2019). The amount of N2O produced seemed to depend on the environmental pH. At pH 7.5, N2O production originated largely from NH2OH. In acidic environments, Ca. N. oleophilus seems to increase N2O production. Interestingly, an isotope tracing experiment showed that Ca. N. oleophilus produced >50% of N2O from NO2−, which would suggest N2O formation through a nitrifier denitrification pathway (Jung et al., 2019). In addition, upregulation of a putative cythochrome P450 NO reductase was observed under acidic conditions. Cytochrome P450 is an enzyme involved in conversion of NO to N2O (Harris, 2002). This enzyme is also used for NO reduction by other microbial species (Higgins et al., 2018). These results suggest that Ca. N. chungbukensis and Ca. N. oleophilus use different pathways for N2O formation under acidic conditions. These findings exemplify the importance of studying the N2O yields of different AOA lineages.
3.2 Denitrification
Denitrification is the reduction of NO3− to N2, via NO2−, NO and N2O (Bakken et al., 2012; Thomson et al., 2012). Some microorganisms possess all genes for denitrification and can carry out the entire pathway, whereas others lack the capacity to reduce NO3− all the way to N2 and therefore perform partial denitrification (Babbin et al., 2015). Many haloarchaea are predicted to perform (partial) denitrification (Torregrosa-Crespo et al., 2018; Torregrosa-Crespo et al., 2019; Miralles-Robledillo et al., 2021). Haloarchaea likely perform denitrification through a similar pathway as denitrifying bacteria (Torregrosa-Crespo et al., 2020a; Miralles-Robledillo et al., 2024) (Figure 2). Some haloarchaea, such as Haloferax mediterranei, can reduce NO3− all the way to N2, while others are predicted to catalyse partial denitrification potentially contributing to N2O formation (Torregrosa-Crespo et al., 2020b).
Four enzymes are involved in the reduction reactions of the denitrification pathway: membrane-bound nitrate reductase (NAR) or periplasmic nitrate reductase (NAP), NIR, NOR and nitrous oxide reductase (NOS) (Bothe et al., 2000). Many haloarchaea encode the NarG and NarH subunits of NAR (Miralles-Robledillo et al., 2021). The second step, NO2− reduction, is performed by one of two main nitrite reductases: nirS (cytochrome-cd1-dependent nitrite reductases) or nirK (Kandeler et al., 2006). Genome analysis by Miralles-Robledillo et al. (2021) indicates that haloarchaea encode nirK and do not have nirS. In addition, the same study reveals that qNOR (norZ) is the main NOR in haloarchaea. Finally, haloarchaea encode NosZ for N2O reduction.
Considering the high relative abundance of haloarchaea in saline environments and the fact that half of the haloarchaea species are predicted to perform (partial) denitrification, they could significantly contribute to gaseous N-emissions (Shi et al., 2016; Torregrosa-Crespo et al., 2018; Miralles-Robledillo et al., 2021). Based on genome analysis it can be interfered which haloarchaea are complete denitrifiers and which are partial denitrifiers (Miralles-Robledillo et al., 2021). While denitrification by some species has been tested in laboratory environments (Torregrosa-Crespo et al., 2019) and RNA-seq studies are conducted to understand the denitrification process (Miralles-Robledillo et al., 2024), studies regarding their contribution to the release of N gasses in the environment are lacking.
3.3 Biological nitrogen fixation
N is most commonly present in the atmosphere in the form of N2, which is unavailable for most organisms (Erisman et al., 2008). N2 fixation, the reduction of N2 to NH3, is carried out by a select group of bacteria and archaea known as diazotrophs (Boyd and Peters, 2013). Within the bacterial domain, N2 fixation is a more widespread ability, and N2-fixing bacteria can either be free-living, or plant associated (Pi et al., 2022). In the domain of archaea N2 fixation has, to date, only been demonstrated within methanogenic archaea (Leigh, 2000; Dekas et al., 2009). N2-fixing methanogens have been identified across several orders, including Methanobacteriales, Methanosarcinales, Methanocellales and Methanomicrobiales (Leigh, 2000; Koirala and Brözel, 2021). Notably, N2-fixing archaea are exclusively free-living (Pi et al., 2022). It is unclear whether N2 fixation first evolved in archaea and was subsequently transferred to bacteria or vice versa. Both the archaea-first and, more recently, the bacteria-first hypotheses have been proposed (Pi et al., 2022).
N2 fixation in methanogens is coupled to methanogenesis, as fixation requires the input of ATP generated through methanogenesis (Bae et al., 2018). N2 fixation is catalysed by the enzyme nitrogenase, of which three different variants exist (Riyaz and Khan, 2025): Fe-dependent, Vanadium (V)-dependent and molybdenum (Mo)-dependent nitrogenase. Mo-nitrogenase is the common type of nitrogenase, encoded by most, if not all, diazotrophs (Chanderban et al., 2023). In addition, it is the most efficient enzyme requiring the lowest amount of ATP for N2 fixation (Chanderban et al., 2023; Riyaz and Khan, 2025). Identified N2-fixing methanogens encode the Mo-dependent nitrogenase (Leigh, 2000). Some species, including Methanosarcina acetivorans, even encode all three variants (Chanderban et al., 2023). As Mo-nitrogenase is the common type of nitrogenase, N2-fixing microorganisms are often detected using nifH, encoding the Fe protein of Mo-nitrogenase, as a biomarker (Fani et al., 2000).
N2-fixing methanogens have been detected in a variety of different environments, including hydrothermal vents (Mehta and Baross, 2006), soil (Bae et al., 2018) and inside plant roots (Bao et al., 2025). Bae et al. (2018) used nifH to study activity of N2-fixating archaea in the Florida everglades, a freshwater wetland affected by the intensification of agricultural practices. They found that in soils unaffected by agricultural effluent, 49% of the nifH mRNA transcripts belong to methanogens. This indicates that there is a significant contribution of methanogenic archaea to N2 fixation in these wetlands.
Since N is an important element in agriculture, it is unsurprising that many studies have focussed on the effect of agricultural practices on diazotrophs. These studies use nifH as a biomarker for detection of both bacterial and archaeal diazotrophs (Fan et al., 2019; Han et al., 2019; Gao et al., 2021; Li et al., 2023; Zhou et al., 2023). However, the detection of N2-fixing archaea is often not reported in these studies. Because most samples were collected from the topsoil (0–20 cm), this may explain the absence of N₂-fixing archaea. If N2-fixing archaea were present, they are not further discussed, potentially due to their low abundance compared to N2-fixing bacteria (Nepel et al., 2022).
The use of nifH as a biomarker to detect archaeal N2-fixing methanogens has several limitations. Evaluation of different nifH primers revealed that not all primer pairs detect archaeal N2-fixers (Gaby and Buckley, 2012; Angel et al., 2018). Furthermore, many microbial species carry pseudo-nifH, they encode nifH but are unable to perform N2 fixation (Mise et al., 2021). This is the case for some anaerobic microorganisms, such as Clostridia species and some methanogens. Instead, other subunits of nitrogenase have been suggested as more suitable biomarkers, such as nifD, encoding the beta-subunit of nitrogenase (Mise et al., 2021). The occurrence of pseudo-nifD is less likely (Mise et al., 2021). Masuda et al. (2023) used nifD to determine the effect of fertilization on the N2-fixing community in paddy fields. They found a low abundance of total archaeal nifD compared to bacterial nifD, which indicates that bacteria are the major N2-fixers in these paddy fields. At genus level, the archaeal genus Ca. Methanoperendens was found amongst the top 5 of most abundant genera, particularly in unfertilized paddy fields (Masuda et al., 2023). The identification of Ca. Methanoperendens as a N2-fixer is surprising, as this archaeon is a methanotroph and not a methanogen. Since N2 fixation for archaea has only been identified in methanogens, the results of this study require further clarification and could potentially indicate that N2 fixation within archaea is not limited to methanogenic archaea. Evidence of possible N2 fixation by methanotrophic archaea has previously been found in methane seep sediments (Miyazaki et al., 2009).
3.4 Dissimilatory nitrate reduction to ammonium (DNRA)
N-DAMO archaea reduce NO3− to NO2− using electrons produced from CH4 via the reverse methanogenesis pathway (Haroon et al., 2013). This conversion is however not the only contribution N-DAMO archaea make to the N-cycle, as N-DAMO archaea can perform DNRA. In bacteria, DNRA is a two-step process where NO3− is reduced to NO2− and subsequently to NH4+ via NH2OH (Zhao et al., 2025). NO3− is reduced to NO2− by NAR or NAP and NO2− is reduced to NH4+ by pentaheme cytochrome c nitrite reductase (NrfA) (Zhao et al., 2025).
N-DAMO archaea encode both nrfA and narG, indicating a similar pathway for NO3− reduction as bacteria (Haroon et al., 2013; Nie et al., 2021). However, N-DAMO archaea seem to possess several different pathways for DNRA (Wang et al., 2025). Wang et al. (2025) discovered two possible pathways of DNRA in the presence of manganese (Mn): (1) ammonia-forming nitrite reductase (Nrf) pathway and (2) the reverse hydroxylamine:ubiquinone reductase module pathway. In addition to nrfA, hao and the gene encoding hydroxylamine reductase (hcp) were upregulated in the presence of Mn. This suggests that NO2− was reduced to NH2OH by hao and subsequently to NH4+ by hcp (Figure 2).
Furthermore, N-DAMO archaea Ca. Methanoperedens nitroreducens was shown the perform DNRA in the presence of iron and low concentrations of NO3− (Tan et al., 2024). Under the tested conditions, DNRA was coupled to N2O emissions. The gene encoding cytochrome P460 was upregulated, suggesting a role in catalysing the oxidation of NH2OH to N2O. Additionally, the nitric oxide reductase flavorubredoxin (norV) was upregulated, indicating the presence of a second N2O formation pathway, in which NO is produced by NrfA and subsequently reduced to N2O via NorV. The results of these studies suggest that DNRA may take place under specific conditions with different electron acceptors using different pathways.
4 Archaeal contribution to carbon cycling
4.1 Carbon fixation
AOA are generally considered to be obligate autotrophs, relying on atmospheric CO2 as their sole source of carbon through CO2 fixation. Pratscher et al. (2011) showed direct evidence of autotrophic growth in soil AOA using RNA-stable isotope probing. While a marine AOA species has been suggested to exhibit mixotrophic growth (Hallam et al., 2006), genomic analysis indicates that not all soil AOA are capable of mixotrophic growth (Lehtovirta-Morley et al., 2024).
CO2 fixation in AOA is coupled to NH3 oxidation (Pratscher et al., 2011). Without NH3 present, no CO2 fixation will take place. AOA fix CO2 via the 3-hydroxypropionate/4-hydroxybutyrate (3-HP/4-HB) cycle (Pratscher et al., 2011), this pathway is conserved within all AOA lineages (Lehtovirta-Morley et al., 2024). The gene encoding acetyl-CoA carboxylase α-submit (accA) is an essential gene involved in CO2 fixation in AOA (Yakimov et al., 2009). In contrast, AOB perform CO2 fixation via the Calvin-Benson-Bassham (CBB) cycle (Stein et al., 2007). A difference between the 3-HP/4-HB and CBB cycle is the energy required for CO2 fixation; the archaeal 3-HP/4-HP pathway requires less ATP then the CBB cycle (Könneke et al., 2014), making the archaeal pathway more efficient for biomass formation.
Most research regarding CO2 fixation by AOA and its environmental significance has been performed in oceans and deep seas. Due to the oligotrophic conditions in water, AOA make significant contributions to CO2 fixation (Wu et al., 2022). A study involving marine AOA and AOB found that N. maritimus formed 1.3 g dry biomass per mole NH3 oxidized, and the marine AOB N. oceani 0.8 g dry mass per mole (Könneke et al., 2014). This indicates that N. maritimus can form biomass more efficiently than N. oceani.
A study on AOA and AOB in forest soils estimated that AOA oxidize 59.8 μg N in the form of NH3 to fix 1 μg C to their biomass (Norman et al., 2015). For AOB this was 58.2 μg N (Norman et al., 2015). While this study looked at the whole community of AOA and AOB rather than single species, these results indicate that the efficiency of CO2 fixation is similar between both groups. To our knowledge there are currently no studies that performed similar experiments in agricultural soils.
Microcosm experiments with soils from grassland found that 80% of CO2 fixed into the SOC pool originated from AOA and AOB combined (Xia et al., 2022). Particularly in water amended soils without N addition, AOA contributed significantly to CO2 fixation, while AOB made large contributions under urea addition (Xia et al., 2022). This result is in line with the fact that AOA can outcompete AOB when N concentrations are low and may indicate that AOA might significantly contribute to CO2 fixation in N limited soils.
In contrast to AOA, Haloarchaea are considered photoheterotrophs, as they use organic C compounds as their C source and require light to generate energy (Grant, 2001). For example, Haloarcula hispanica was found to grow on acetate as a sole C source (Falb et al., 2008). However, comparative genomics has revealed exceptions: the haloarchaea Natronomonas pharaonis encodes an archaeal-type RuBisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase), indicating that it might be capable of CO2 fixation (Falb et al., 2008). Whether other haloarchaea carry RuBisCO remains to be resolved.
Methanogens can also contribute to C-cycling via CO2 fixation. Specifically, autotrophic hydrogenotrophic methanogens who use CO2 and H2 as their sole source for C and energy generation (Borrel et al., 2016). Although heterotrophic hydrogenotrophic methanogens have been discovered as well (Kouzuma et al., 2017). Hydrogenotrophic methanogenic archaea are commonly detected in paddy fields, and several orders have been detected in grassland soils (Table 2).
Table 2. Methanogen groups capable of hydrogenotrophic methanogenesis and their habitats.
Most CO2 reducing methanogens fixate C via the reductive acetyl-CoA cycle, also known as the Wood-Ljungdahl pathway, but there are exceptions: Methanospirillum hungatei was found to encode RuBisCO and PRK (phosphoribulokinase), which are involved in the reductive hexulose-phosphate pathway for CO2 fixation (Kono et al., 2017; Lemaire et al., 2020). It is not clear if M. hungatei can grow with CO2 as a C source. For autotrophic hydrogenotrophic methanogens, CO2 is an important source for C and energy generation. A study by Chen et al. (2019) reports that Methanobacterium congolense converts four moles of CO2 into CH4 for each mole CO2 that was converted into biomass. This experiment included only one strain of M. congolense and was performed under CO2 limited conditions. Similar experiments could be conducted under ambient CO₂ concentrations and with other methanogen strains to determine whether rates are comparable. In soil environments where methanogens are abundant, CO2 fixation could potentially contribute to carbon sequestration. However, since CH4 has a higher global warming potential than CO2, emissions may outweigh the GHG reduction benefits of CO2 fixation (Danny Harvey, 1993).
4.2 Methanogenesis
Methanogenesis involves the degradation of organic matter into CO2 and CH4 (Conrad, 2020). While methanogenesis was initially thought to be a process solely occurring in anaerobic environments, it can also take place under aerobic conditions (Serrano-Silva et al., 2014; Angle et al., 2017). Methanogens rely on other members of the soil microbiome to obtain their substrates for methanogenesis (Conrad, 2020). Fermenting and hydrogenotrophic microorganisms degrade complex organic matter into CO2, H2 and simple organic compounds, which can in turn be utilized by methanogenic archaea (Conrad, 2020). Methanogens perform methanogenesis primarily through one of three pathways: (1) the methylotrophic pathway, (2) the acetoclastic pathway and (3) the hydrogenotrophic pathway (Liu and Whitman, 2008). Methylotrophic methanogenesis involves the utilization of methylated compounds as substrates (Liu and Whitman, 2008; Serrano-Silva et al., 2014). Acetoclastic methanogens use acetate as a substrate and hydrogenotrophic methanogens produce CH4 from CO2 and H2 (Liu and Whitman, 2008; Serrano-Silva et al., 2014). The hydrogenotrophic and acetoclastic pathways are the most common (Enrich-Prast et al., 2014; Kim and Whitman, 2014; Serrano-Silva et al., 2014). All methanogens encode Methyl-coenzyme M reductase (MCR), which is involved in the final step of methane formation (Enzmann et al., 2018). The mcr gene, particularly mcrA, is commonly employed as a molecular marker to detect methanogens in environmental samples. For a schematic overview of the three different pathways, we refer to Enzmann et al. (2018). For more in-depth information regarding enzymes involved in the methanogenesis process, we refer to the review by Reeve et al. (1997).
4.3 Nitrate-dependent anaerobic methane oxidation (N-DAMO)
CH4 oxidation is the process of oxidizing CH4 to CO2 (Serrano-Silva et al., 2014) (Figure 1). CH4 oxidation has been identified within both bacteria and archaea and can be performed under aerobic and anaerobic conditions (Wei et al., 2022; Zhao Y. et al., 2024). N-DAMO archaea perform CH4 oxidation anaerobically through the reduction of NO3− to NO2− (Raghoebarsing et al., 2006) (Figure 2). Anaerobic methane oxidation in archaea is thought to proceed via reverse methanogenesis, as N-DAMO archaea harbour enzymes used for CH4 formation in methanogens, including mcr (Hallam et al., 2004; Shima and Thauer, 2005; Haroon et al., 2013; Wei et al., 2022).
The N-DAMO process has been shown to contribute to 12–33% of total CH4 oxidation, N-DAMO archaea could therefore be promising for CH4 removal in different environments (Wang et al., 2022). In marsh soil, stable isotope probing was used to determine the contribution of N-DAMO archaea and bacteria to CH4 oxidation. The activity of N-DAMO bacteria was predicted to be 0.1–3.8 nmol 13CO2 g−1 dry soil day−1 and the activity of N-DAMO archaea 0.1 to 4.1 nmol 13CO2 g−1 dry soil day−1 (Zheng et al., 2020). Interestingly, a recent study showed that anaerobic CH4 oxidation can be an important source of SOM formation (Zhang et al., 2021). While this study did not distinguish between the different anaerobic CH4 oxidation pathways, approximately 60% of CH4 was turned into SOM instead of being respired as CO2.
5 The impact of nutrient input
Nutrient addition through fertilization is a common management strategy in agriculture, widely used to improve crop yield and quality by supplying essential nutrients, such as N, to soils (Bindraban et al., 2015; Ishfaq et al., 2023). Therefore, it is likely that the functions of the discussed archaeal groups in C- and N-cycling will be impacted by nutrient addition. Not only does nutrient input provide plants with nutrients for growth, the addition of nutrients can also increase emission of several GHGs.
Soil nitrification rates significantly increase with increasing N content in the soil (Li et al., 2020). It is therefore not surprising that fertilization will affect the activity of AOA in nutrient cycling. In particular, the type of fertilizer that is applied seems to be relevant, as growth and activity of AOA is increased under manure addition compared to synthetic fertilizer (Zeng et al., 2024; Wu et al., 2025). This is in line with the preference of AOA for lower levels of NH3, as manure releases NH3 slowly over time (Zhang et al., 2012; Prosser et al., 2020). Furthermore, long-term inorganic fertilizer application can reduce the pH of the soil, which can also lead to an increase in AOA (Ding et al., 2020). In addition, the N in fertilizer has the potential to increase the abundance of specific AOA lineages. In fields receiving manure with >900 kg/ha N, Nitrosopumilus was the predominant AOA lineage (Wang Z. et al., 2023). Application of manure with <600 kg/ha N led to higher abundance of Nitrososphaera. Even within the same AOA lineage, taxa can react differently to fertilizer input. For example, in acidic soil under different long-term organic and chemical fertilization regimes, Nitrososphaerales were the predominant AOA (Zhao et al., 2022). These regimes also led to differences in the abundance of Nitrososphaerales clades, likely driven by fertilizer-induced changes in soil pH. In paddy fields fertilized with manure, Nitrosotalea devanaterra-like AOA, from the Ca. Nitrosotaleales lineage, were the predominant AOA (Liu et al., 2018). The Ca. Nitrosotaleales lineage is known for its adaptation to acidic soils (Table 3), therefore its abundance was likely linked to the acidic pH in three out of the four studied soils.
Table 3. Characteristics of AOA lineages detected in soil environments based on cultured representatives.
As nitrification rates increase, N2O emissions from AOA are also expected to increase. Several field studies have examined the contribution of AOA and AOB to N2O emission and the effects of nutrient input on the emission rates (Di et al., 2013; Hink et al., 2017; Hei et al., 2023; Zeng et al., 2024). In general, higher availability of NH3 and a neutral to alkalic pH are linked to increased contribution of AOB to nitrification (Rütting et al., 2021) and N2O emissions (Di et al., 2013; Hu L. et al., 2022; Zeng et al., 2024). Under N limiting conditions, AOA can exhibit a higher contribution to N2O emissions than AOB (Guo et al., 2025), likely because AOA are able to outcompete AOB at low substrate concentrations.
In line with this, the type of fertilizer applied to the soil might affect whether AOB or AOA produce more N2O. Hei et al. (2023) studied the effect of switching chemical fertilization to fertilization with manure in field plots. The N in the chemical fertilizer was applied in the form of urea and contained the same amount of N as the applied manure. Full substitution of urea with manure reduced N2O emissions from the plots (Hei et al., 2023). The reduction in N2O emissions correlated with a reduction in the abundance of AOB and an increase in the abundance of AOA. As the field plots received the same N concentrations, this reduction in AOB was most likely a result of the form of N used as fertilizer. It has been reported that AOB have higher affinity for urea than AOA (Qin et al., 2024), while manure releases N more gradually, favouring AOA (Zhang et al., 2012). It should be mentioned that the authors noted a 16–210% reduction of cumulative N2O emissions, and that cumulative emissions cannot be reduced more than 100%. Their observations are however supported by Hink et al. (2017), who found that AOA produce ∼0.5 × 10−3 N2O-N per NO3−-N produced and AOB ∼ 0.95 × 10−3 N2O-N per NO3−-N, suggesting that AOA produce less N2O during NH3 oxidation.
Likewise, CO2 fixation by AOA seems to be influenced by nutrient addition. Studies in soil often focus on the detection of CO2− fixating microorganisms using qPCR and correlate gene abundance and CO2 fixation rates. accA has been used as an indicator gene for the 3-HP/4-HB pathway of AOA (Mao et al., 2024). In two different studies, one in a Mollisol with wheat-soybean-maize rotation and one in paddy soil, a positive correlation was found between accA abundance, autotrophic archaeal community composition and the CO2 fixation rate (Liao et al., 2020; Wang Q. et al., 2024). Specifically, in Mollisol, no fertilizer and manure treatment had higher accA copy numbers compared to NPK (nitrogen, phosphorus, and potassium) fertilizer and NPK fertilizer with manure (Liao et al., 2020).
In rice fields, conventional fertilization, consisting of NPK application, decreased the accA copy number, while it increased under conventional treatment combined with manure application (Wang Q. et al., 2024). The effect of manure combined with chemical fertilizer is therefore not in line with the results of Liao et al. (2020). This might indicate that fertilizer application is not the only regulator of the accA copy number. It is important, however, to mention that the gene abundance of the bacterial CO2 fixation pathway was much higher. Nevertheless, these findings indicate contribution of AOA to CO2 fixation in these soils.
Similar to AOA, it has been observed that methanogens react to fertilizer application and that different fertilizer treatments affect methanogen groups differently. Chemical and organic N application have been observed to increase CH4 fluxes (Kong et al., 2019). For example, acetoclastic methanogens increased in relative abundance during organic fertilization, while hydrogenotrophic methanogens decreased (Yuan et al., 2018). Acetoclastic methanogens require acetate as their substrate for methanogenesis, which is provided during fertilization with manure, but not during chemical fertilization. This observation was confirmed by Kong et al. (2019), who observed acetoclastic methanogens only under manure treatment.
The effect of management practices on CO2 and N2 fixation by methanogens is still an underexplored subject. The link between CO2 fixation and biomass formation has only been demonstrated in batch experiments for Methanobacterium congolense so far (Chen et al., 2019). In addition, the low abundance of N2-fixing methanogens in agriculture soils suggests that they do not play a major role in N2 fixation.
N-DAMO archaea require NO3− for the oxidation of CH4. Hence, it is not surprising that they are affected by fertilizer input (Wang et al., 2022). The activity and abundance of N-DAMO archaea increases with fertilizer addition, and in turn, their increase in abundance leads to higher contributions to NO3− and CH4 removal in paddy fields (Wang et al., 2022). In addition, the activity of N-DAMO archaea can potentially be optimized through supplementation of nutrients. Wang S. et al. (2024) demonstrated that through optimization of molybdenum, tungsten and selenium concentrations in growth media, the abundance of mcrA could be upregulated. Therefore, increasing the concentrations of these nutrients through fertilization might increase the CH4 oxidation rate of N-DAMO archaea.
Nutrient availability was observed to impact community composition of haloarchaea in saltwater samples (Hua et al., 2021). To our knowledge, no studies have been performed to determine the effect of nutrient input on this archaeal group. As haloarchaea are involved in denitrification, it can be speculated that the input of additional N can increase the emission of N gasses. With the potential application of haloarchaea as biofertilizers (Naitam et al., 2023), it will be essential to understand the contribution of haloarchaea to C- and N-cycling in the soil.
6 Detection of archaea in agricultural soils
The main challenge in archaeal research and uncovering their role in nutrient cycling, is the fact that many archaea have not been cultured in a laboratory setting (Sun et al., 2020; Rafiq et al., 2023). Several factors limit their culturability such as, lack of ability to mimic correct environmental conditions, and substrate concentrations and the slow growth rates that are typical for archaea. In addition, several archaeal species rely on other members of the soil microbiome for nutrient acquisition, which makes it extremely challenging to obtain pure cultures of these archaea and uncover their full contribution to nutrient cycling (Rafiq et al., 2023).
Despite the challenges in cultivating archaea, they can be studied in realistic environments such as agricultural soils. This is often done using several primers designed to target specific archaeal groups or functional genes (Table 4). For example, amoA primers are widely used for the detection of AOA and specific primers have been designed for the detection of mcrA from M. nitroreducens. Several accA primers have been used to target accA in AOA. nifH and nifD primers can be used for detecting N2-fixing methanogens, but these primers have not been specifically designed for the detection of N2-fixing methanogens.
Table 4. Collection of primers used for detection of archaea in literature cited in this review.
Specific primers for haloarchaea exist. For example, Oxley et al. (2010) designed primers for the detection of haloarchaea in human intestinal tracts. However, such primers have not been tested on soil samples as far as we are aware. While ample primers have been designed for the detection of bacteria involved in denitrification, these primers are not always efficient in detecting archaeal targets due to high sequence divergence (Ma et al., 2019). Specific primers have been designed to detect archaeal denitrification genes (Rusch, 2013), however to our knowledge these primers have not been tested using soil samples.
7 Concluding remarks and perspectives
With the involvement of archaea in both C- and N-cycling, archaea can make a significant contribution to the soil nutrient pool. Most archaeal groups are known to perform a specific role, but current literature suggests that the groups discussed here have a broader relevance in agricultural soils, although evidence in some cases is still limited. Based on available studies on the lesser-known functions of AOA, methanogens, N-DAMO and haloarchaea in C- and N-cycling, it seems that these archaeal groups and their functions mainly occur under specific conditions.
The contribution of AOA to N2O emissions and CO2 fixation seem mainly relevant under low N conditions or when N is released slowly, such as under manure fertilization. In conditions of high N availability, AOB dominate NH3 oxidation and are the primary contributors to N2O emissions. Replacing mineral fertilizers with manure can potentially favour AOA and reduce N2O emissions from nitrification, as AOA are suggested to produce less N2O per NH3 molecule oxidized. Shifting the balance from AOB to AOA through fertilizer treatment could therefore be a suitable strategy for lowering N2O emissions from agriculture soils. More specifically, management strategies can focus on shifting the AOA population to enhance the abundance of certain AOA lineages. Fertilizer application has shown to influence the abundance of AOA lineages in soil. To incorporate this knowledge into management strategies, insight is needed on the N2O production rates of all AOA lineages and how soil conditions such as N availability and pH affect these production rates.
More research is also needed into the CO2 fixation capabilities of AOA. Further studies, for example using stable isotope probing, are needed to confirm this relationship and to determine the actual rate of CO2 fixation of AOA in agricultural soils, as data from forest soils and marine environments suggests different fixation rates. If CO2 fixation by AOA significantly contributes to soil C formation, it would be promising to investigate strategies to increase the CO2 fixation rate of this archaeal group. Currently, the effect of manure treatments on CO2 fixation by AOA remains unclear, and manure addition, in the studies that are published on this topic, did not see an increase in accA abundance. This suggests that nutrient input might not be a suitable strategy to increase CO2 fixation by AOA. In this regard, setting up a field experiment to determine the effect of different fertilizers on the CO2 fixation rates will be required. In addition, exploring other strategies independent of nutrient input such as microbiome engineering might be a promising future direction. A recent study indicates that the CO2 fixation rates of bacterial autotrophs could be significantly increased through virus infection (Lu et al., 2025). No such effect has been documented for archaea yet, but this appears to be a promising approach to be explored.
Methanogens are primarily relevant in anaerobic environments. Specifically, hydrogenotrophic methanogens can contribute to CO2 fixation. Considering CO2 fixation is linked to CH4 production, an increase in CO2 fixation will also lead to an increase in CH4 emissions. Hence, from a sustainability perspective, methanogens are not a good target for increasing CO2 sequestration in agricultural soils. The same limitation is true for N2 fixation by methanogens, as N2 fixation depends on the ATP produced through methanogenesis. Low detection of N2-fixing methanogens through nifH targeted qPCR, further raises the question if methanogens are relevant for agricultural environments. Adjusting current primers or designing specific primers targeting nifH of N2-fixating archaea will help determine the significance of N2 fixation by this archaeal group.
Overall, due to their specific occurrence, increasing methanogen abundance is likely not an appropriate strategy for increasing C or N in most agricultural soils. Therefore, management strategies in agriculture should prioritize other approaches and focus on other CO2−- or N2-fixing microorganisms that provide nutrients without environmental costs. A potential alternative could be directed evolution to achieve expression of nitrogenase in crops, which might allow plants to directly carry out N transformation without relying on the soil microbiome. This approach currently has several challenges however, including the anaerobic nature of nitrogenase and potential growth defects in host cells due to high metabolic burden (Bennett et al., 2023).
Recent research revealed that a consortium of N-DAMO archaea and bacteria could be used as a promising strategy to reduce NO3− and CH4 emissions in brackish ecosystems (Legierse et al., 2023). Using bioaugmentation, N-DAMO abundance reached 47–73% of the total archaeal population in sediment microcosms (Legierse et al., 2023). Implementation in situ has yet to be tested, however it might be a promising strategy in paddy soils or in other waterlogged environments to increase the removal of CH4 and NO3− from the system.
While the abundance of N-DAMO archaea is likely low in most soils, N-DAMO growth could be stimulated through fertilization or potentially through bioaugmentation. Before N-DAMO archaea can be used for bioaugmentation in soil environments, several questions need to be answered first, including: (1) Can N-DAMO archaea survive and remain active in anaerobic soils? and (2) If so, what delivery or inoculation strategies would allow bioaugmentation without disruption of the native microbiome? Soils have different redox potentials and nutrient concentrations compared to sediments (Kalev and Toor, 2018), and survival of N-DAMO under these conditions needs to be tested. After answering these questions, small-scale microcosm and controlled field experiments are needed to determine if N-DAMO archaea meaningfully contribute to CH4 emission mitigation. As current studies suggest that nutrient input can be used to regulate N-DAMO, microcosm and field experiments should examine the effect of different fertilizers on their activity.
The role of haloarchaea in C- and N-cycling remains ambiguous. Notably, out of the archaeal groups reviewed here, they are the only group that has not yet been detected with a specific primer set in soils. Designing specific primers for detection in soil samples should therefore be a priority. Many primers for bacterial denitrifiers are available, some might be suitable for the detection of archaeal denitrification genes (Wei et al., 2015; Ma et al., 2019). Compared to the other archaeal groups that are reviewed here, establishing molecular detection tools will be needed to further establish the ecological significance of haloarchaea.
Future research on haloarchaea should focus on significance of their contributions to C- and N-cycling. This is both important to understand their role in natural environments and for their usage as biofertilizer. In this regard, their contributions to N2O formation should be the priority for future research. In saline environments, studies should focus on which microbial groups contribute most to N2O formation. If haloarchaea are major contributors, management strategies could be incorporated to reduce N input in saline environments. Microcosm and field experiments should be used to determine if using haloarchaea as biofertilizer increases N2O emissions. If this is the case, mitigation strategies are needed. This could include co-amendment with N-DAMO archaea, to reduce the amount of NO3− in the soil. In addition, Stachler et al. (2020) showed that the endogenous CRIPSR system of haloarchaeon Haloferax volcani could be used to repress gene expression. This might indicate that a similar system can be used to repress genes involved in denitrification. This would reduce the risk of N2O emissions from haloarchaea used as biofertilizer.
In summary, archaea have diverse functional potential in agriculture soils, but the significance of their roles seems context dependent. Further development of molecular detection tools, specifically for haloarchaea, and culture dependent tools, such as culturing approaches and tracing studies can bridge knowledge gaps. Steering the composition of the soil microbiome might be possible through changes in nutrient management, such as application of organic fertilizer instead of chemical fertilizer, or through microbiome engineering. To harness the potential of N-DAMO archaea for the removal of CH4 and NO3−, bioaugmentation might be a suitable strategy. Nutrient cycling depends on contributions of the entire soil microbiome, therefore the specific context of the interactions between different groups of organisms in the microbiome should be further understood to fully leverage the functions of archaea in C- and N-cycling. This can then lead to improved nutrient management strategies in agriculture.
Author contributions
BS: Conceptualization, Writing – original draft, Writing – review & editing. AS: Conceptualization, Writing – review & editing. EK: Conceptualization, Writing – review & editing. VS: Conceptualization, Writing – review & editing. CB: Supervision, Writing – review & editing. TB: Conceptualization, Writing – review & editing.
Funding
The author(s) declared that financial support was received for this work and/or its publication. Wetsus is co-funded by the European Union (Horizon Europe, LIFE, Interreg and EDRF), the Province of Fryslân and the Dutch Government: Ministry of Economic Affairs (TTT, SBO & PPS-I/TKI Water Technology), Ministry of Education, Culture and Science (TTT & SBO) and Ministry of Infrastructure and Water Management (National Growth Fund—UPPWATER).
Acknowledgments
This work was performed in the cooperation framework of Wetsus, European Centre of Excellence for Sustainable Water Technology (www.wetsus.nl). The authors like to thank the participants of the research theme “Soil” for the fruitful discussions and their financial support. The authors would also like to thank Jidske Knigge for their helpful comments on the review.
Conflict of interest
BS, AS, and EK were employed by Bioclear Earth B.V.
The remaining author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Generative AI statement
The author(s) declared that Generative AI was not used in the creation of this manuscript.
Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Alori, E. T., Emmanuel, O. C., Glick, B. R., and Babalola, O. O. (2020). Plant–archaea relationships: a potential means to improve crop production in arid and semi-arid regions. World J. Microbiol. Biotechnol. 36:133. doi: 10.1007/s11274-020-02910-6,
Alves, K. J., Pylro, V. S., Nakayama, C. R., Vital, V. G., Taketani, R. G., Santos, D. G., et al. (2022). Methanogenic communities and methane emissions from enrichments of Brazilian Amazonia soils under land-use change. Microbiol. Res. 265:127178. doi: 10.1016/j.micres.2022.127178,
Ando, S., Goto, M., Meunchang, S., Thongra-ar, P., Fujiwara, T., Hayashi, H., et al. (2005). Detection of nifH sequences in sugarcane (Saccharum officinarum L.) and pineapple (Ananas comosus [L.] Merr.). Soil Sci. Plant Nutr. 51, 303–308. doi: 10.1111/j.1747-0765.2005.tb00034.x
Angel, R., Claus, P., and Conrad, R. (2012). Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 6, 847–862. doi: 10.1038/ismej.2011.141,
Angel, R., Nepel, M., Panhölzl, C., Schmidt, H., Herbold, C. W., Eichorst, S. A., et al. (2018). Evaluation of primers targeting the diazotroph functional gene and Development of NifMAP – a bioinformatics pipeline for Analyzing nifH amplicon data. Front. Microbiol. 9:703. doi: 10.3389/fmicb.2018.00703,
Angle, J. C., Morin, T. H., Solden, L. M., Narrowe, A. B., Smith, G. J., Borton, M. A., et al. (2017). Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. Nat. Commun. 8:1567. doi: 10.1038/s41467-017-01753-4,
Asakawa, S. (2021). Ecology of methanogenic and methane-oxidizing microorganisms in paddy soil ecosystem. Soil Sci. Plant Nutr. 67, 520–526. doi: 10.1080/00380768.2021.1953355
Babbin, A. R., Bianchi, D., Jayakumar, A., and Ward, B. B. (2015). Rapid nitrous oxide cycling in the suboxic ocean. Science 348, 1127–1129. doi: 10.1126/science.aaa8380,
Bae, H.-S., Morrison, E., Chanton, J. P., and Ogram, A. (2018). Methanogens are major contributors to nitrogen fixation in soils of the Florida Everglades. Appl. Environ. Microbiol. 84, e02222–e02217. doi: 10.1128/AEM.02222-17,
Baker, B. A., Gutiérrez-Preciado, A., Rodríguez del Río, Á., McCarthy, C., López-García, P., Huerta-Cepas, J., et al. (2024). Expanded phylogeny of extremely halophilic archaea shows multiple independent adaptations to hypersaline environments. Nat. Microbiol. 9, 964–975. doi: 10.1038/s41564-024-01647-4,
Bakken, L. R., Bergaust, L., Liu, B., and Frostegård, A. (2012). Regulation of denitrification at the cellular level: a clue to the understanding of N2O emissions from soils. Philos. Trans. Royal Soc. B 367, 1226–1234. doi: 10.1098/rstb.2011.0321,
Bao, Z., et al. (2025). Metatranscriptomic analysis to reveal the coupling between nitrogen fixation and CH4 oxidation in root tissues of Phragmites australis. Biol. Fertil. Soils 61, 57–70. doi: 10.1007/s00374-024-01869-y
Bapteste, É., Brochier, C., and Boucher, Y. (2005). Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1, 353–363. doi: 10.1155/2005/859728,
Bates, S. T., Berg-Lyons, D., Caporaso, J. G., Walters, W. A., Knight, R., and Fierer, N. (2011). Examining the global distribution of dominant archaeal populations in soil. ISME J. 5, 908–917. doi: 10.1038/ismej.2010.171,
Bennett, E. M., Murray, J. W., and Isalan, M. (2023). Engineering nitrogenases for synthetic nitrogen fixation: from pathway engineering to directed evolution. BioDesign Res. 5:0005. doi: 10.34133/bdr.0005,
Bindraban, P. S., Dimkpa, C., Nagarajan, L., Roy, A., and Rabbinge, R. (2015). Revisiting fertilisers and fertilisation strategies for improved nutrient uptake by plants. Biol. Fertil. Soils 51, 897–911. doi: 10.1007/s00374-015-1039-7
Borrel, G., Adam, P. S., and Gribaldo, S. (2016). Methanogenesis and the wood–Ljungdahl pathway: an ancient, versatile, and fragile association. Genome Biol. Evol. 8, 1706–1711. doi: 10.1093/gbe/evw114,
Bothe, H., Jost, G., Schloter, M., Ward, B. B., and Witzel, K. (2000). Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiol. Rev. 24, 673–690. doi: 10.1111/j.1574-6976.2000.tb00566.x,
Boyd, E. S., and Peters, J. W. (2013). New insights into the evolutionary history of biological nitrogen fixation. Front. Microbiol. 4:201. doi: 10.3389/fmicb.2013.00201,
Buée, M., De Boer, W., Martin, F., Van Overbeek, L., and Jurkevitch, E. (2009). The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321, 189–212. doi: 10.1007/s11104-009-9991-3
Caranto, J. D., and Lancaster, K. M. (2017). Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. Proc. Natl. Acad. Sci. 114, 8217–8222. doi: 10.1073/pnas.1704504114,
Caranto, J. D., Vilbert, A. C., and Lancaster, K. M. (2016). Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission. Proc. Natl. Acad. Sci. 113, 14704–14709. doi: 10.1073/pnas.1611051113,
Chanderban, M., Hill, C. A., Dhamad, A. E., and Lessner, D. J. (2023). Expression of V-nitrogenase and Fe-nitrogenase in Methanosarcina acetivorans is controlled by molybdenum, fixed nitrogen, and the expression of Mo-nitrogenase. Appl. Environ. Microbiol. 89:e0103323. doi: 10.1128/aem.01033-23,
Chen, X., Ottosen, L. D. M., and Kofoed, M. V. W. (2019). How low can You go: methane production of Methanobacterium congolense at low CO2 concentrations. Front. Bioeng. Biotechnol. 7:34. doi: 10.3389/fbioe.2019.00034,
Chen, X., Zhu, Y. G., Xia, Y., Shen, J. P., and He, J. Z. (2008). Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol. 10, 1978–1987. doi: 10.1111/j.1462-2920.2008.01613.x,
Chow, C., Padda, K. P., Puri, A., and Chanway, C. P. (2022). An archaic approach to a modern issue: endophytic Archaea for sustainable agriculture. Curr. Microbiol. 79:322. doi: 10.1007/s00284-022-03016-y,
Clark, D. R., McKew, B. A., Dong, L. F., Leung, G., Dumbrell, A. J., et al. (2020). Mineralization and nitrification: Archaea dominate ammonia-oxidising communities in grassland soils. Soil Biol. Biochem. 143:107725. doi: 10.1016/j.soilbio.2020.107725
Conrad, R. (2020). Methane production in soil environments—anaerobic biogeochemistry and microbial Life between flooding and desiccation. Microorganisms 8:881. doi: 10.3390/microorganisms8060881,
Cui, J., Yu, C., Qiao, N., Xu, X., Tian, Y., and Ouyang, H. (2017). Plant preference for NH4+ versus NO3− at different growth stages in an alpine agroecosystem. Field Crop Res. 201, 192–199. doi: 10.1016/j.fcr.2016.11.009
Danny Harvey, L. D. (1993). A guide to global warming potentials (GWPs). Energy Policy 21, 24–34. doi: 10.1016/0301-4215(93)90205-T
Dekas, A. E., Poretsky, R. S., and Orphan, V. J. (2009). Deep-Sea Archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326, 422–426. doi: 10.1126/science.1178223,
Derwent, R. G. (2020). Global warming potential (GWP) for methane: Monte Carlo analysis of the uncertainties in global tropospheric model predictions. Atmos. 11:486. doi: 10.3390/atmos11050486
Di, H. J., Cameron, K. C., Shen, J. P., Winefield, C. S., O’Callaghan, M., Bowatte, S., et al. (2013). “The role of Bacteria and Archaea in nitrification, nitrate leaching and nitrous oxide emissions in nitrogen-rich grassland soils” in Molecular Environmental Soil Science (Dordrecht: Springer Netherlands), 79–89.
Diaz, C., Saliba-Colombani, V., Loudet, O., Belluomo, P., Moreau, L., Daniel-Vedele, F., et al. (2006). Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant Cell Physiol. 47, 74–83. doi: 10.1093/pcp/pci225,
Ding, J., Ding, Z. W., Fu, L., Lu, Y. Z., Cheng, S. H., and Zeng, R. J. (2015). New primers for detecting and quantifying denitrifying anaerobic methane oxidation archaea in different ecological niches. Appl. Microbiol. Biotechnol. 99, 9805–9812. doi: 10.1007/s00253-015-6893-6,
Ding, J., Fu, L., Ding, Z. W., Lu, Y. Z., Cheng, S. H., and Zeng, R. J. (2016). Environmental evaluation of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a paddy field. Appl. Microbiol. Biotechnol. 100, 439–446. doi: 10.1007/s00253-015-6986-2,
Ding, J., Ma, M., Jiang, X., Liu, Y., Zhang, J., Suo, L., et al. (2020). Effects of applying inorganic fertilizer and organic manure for 35 years on the structure and diversity of ammonia-oxidizing archaea communities in a Chinese Mollisols field. MicrobiologyOpen 9:e00942. doi: 10.1002/mbo3.942,
Ding, L., Wang, K. J., Jiang, G. M., Biswas, D. K., Xu, H., Li, L. F., et al. (2005). Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Ann. Bot. 96, 925–930. doi: 10.1093/aob/mci244,
Du, J., Meng, L., Qiu, M., Chen, S., Zhang, B., Song, W., et al. (2022). Ammonia-oxidizing archaea and ammonia-oxidizing bacteria communities respond differently in oxy-gen-limited habitats. Front. Environ. Sci. 10:976618. doi: 10.3389/fenvs.2022.976618
Enrich-Prast, A., Bastviken, D., Crill, P., Santoro, A. L., Signori, C. N., and Sanseverino, A. M. (2014). “Chemosynthesis” in Reference module in earth systems and environmental sciences (Elsevier).
Enzmann, F., Mayer, F., Rother, M., and Holtmann, D. (2018). Methanogens: biochemical background and biotechnological applications. AMB Express 8:1. doi: 10.1186/s13568-017-0531-x,
Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z., and Winiwarter, W. (2008). How a century of ammonia synthesis changed the world. Nat. Geosci. 1, 636–639. doi: 10.1038/ngeo325
Falb, M., Müller, K., Königsmaier, L., Oberwinkler, T., Horn, P., von Gronau, S., et al. (2008). Metabolism of halophilic archaea. Extremophiles 12, 177–196. doi: 10.1007/s00792-008-0138-x,
Falkowski, P. G., Fenchel, T., and Delong, E. F. (2008). The microbial engines that drive earth’s biogeochemical cycles. Science 320, 1034–1039. doi: 10.1126/science.1153213
Fan, K., Delgado-Baquerizo, M., Guo, X., Wang, D., Wu, Y., Zhu, M., et al. (2019). Suppressed N fixation and diazotrophs after four decades of fertilization. Microbiome 7:143. doi: 10.1186/s40168-019-0757-8,
Fani, R., Gallo, R., and Liò, P. (2000). Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J. Mol. Evol. 51, 1–11. doi: 10.1007/s002390010061,
Francis, C. A., Beman, J. M., and Kuypers, M. M. M. (2007). New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19–27. doi: 10.1038/ismej.2007.8,
Frink, C. R., Waggoner, P. E., and Ausubel, J. H. (1999). Nitrogen fertilizer: retrospect and prospect. Proc. Natl. Acad. Sci. 96, 1175–1180. doi: 10.1073/pnas.96.4.1175,
Gaby, J. C., and Buckley, D. H. (2012). A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS One 7:e42149. doi: 10.1371/journal.pone.0042149,
Gao, H., Li, S., and Wu, F. (2021). Impact of intercropping on the diazotrophic Community in the Soils of continuous cucumber cropping systems. Front. Microbiol. 12:630302. doi: 10.3389/fmicb.2021.630302,
Garrity, G. M., Holt, J. G., Whitman, W. B., Keswani, J., Boone, D. R., Koga, Y., et al. (2001). “Phylum all. Euryarchaeota phy. Nov” in Bergey’s manual® of systematic bacteriology (Springer New York: New York, NY), 211–355.
Grant, W. D. (2001). “Class III. Halobacteria” in Bergey’s manual of systematic bacteriology. eds. D. R. Boone, R. W. Castenholz, and G. M. Garrity (Springer New York: New York, NY), 294–333.
Gubry-Rangin, C., Nicol, G. W., and Prosser, J. I. (2010). Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol. Ecol. 74, 566–574. doi: 10.1111/j.1574-6941.2010.00971.x,
Guo, S., Bol, R., Li, Z., Wu, J., Lin, H., Bo, X., et al. (2025). Patterns and drivers of soil autotrophic nitrification and associated N2O emissions. Soil Biol. Biochem. 203:109730. doi: 10.1016/j.soilbio.2025.109730
Hallam, S. J., Mincer, T. J., Schleper, C., Preston, C. M., Roberts, K., Richardson, P. M., et al. (2006). Pathways of carbon assimilation and Ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4:e95. doi: 10.1371/journal.pbio.0040095,
Hallam, S. J., Putnam, N., Preston, C. M., Detter, J. C., Rokhsar, D., Richardson, P. M., et al. (2004). Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462. doi: 10.1126/science.1100025,
Han, L.-L., Wang, Q., Shen, J. P., di, H. J., Wang, J. T., Wei, W. X., et al. (2019). Multiple factors drive the abundance and diversity of the diazotrophic community in typical farmland soils of China. FEMS Microbiol. Ecol. 95:fiz113. doi: 10.1093/femsec/fiz113,
Haroon, M. F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., et al. (2013). Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500, 567–570. doi: 10.1038/nature12375,
Harris, D. L. (2002). Cytochrome P450nor: a nitric oxide reductase—structure, spectra, and mechanism. Int. J. Quantum Chem. 88, 183–200. doi: 10.1002/qua.10111
Hartmann, M., and Six, J. (2022). Soil structure and microbiome functions in agroecosystems. Nat. Rev. Earth Environ. 4, 4–18. doi: 10.1038/s43017-022-00366-w
Hei, Z., Peng, Y., Hao, S., Li, Y., Yang, X., Zhu, T., et al. (2023). Full substitution of chemical fertilizer by organic manure decreases soil N2O emissions driven by ammonia oxidizers and gross nitrogen transformations. Glob. Chang. Biol. 29, 7117–7130. doi: 10.1111/gcb.16957,
Hernández-Magaña, E., and Kraft, B. (2024). Nitrous oxide production and consumption by marine ammonia-oxidizing archaea under oxygen depletion. Front. Microbiol. 15:1410251. doi: 10.3389/fmicb.2024.1410251,
Higgins, S. A., Schadt, C. W., Matheny, P. B., and Löffler, F. E. (2018). Phylogenomics reveal the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism. Genome Biol. Evol. 10, 2474–2489. doi: 10.1093/gbe/evy187,
Hink, L., Nicol, G. W., and Prosser, J. I. (2017). Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ. Microbiol. 19, 4829–4837. doi: 10.1111/1462-2920.13282,
Hirsch, P. R., and Mauchline, T. H. (2015). The importance of the microbial N cycle in soil for crop plant nutrition. Adv. Appl. Microbiol. 93, 45–71. doi: 10.1016/bs.aambs.2015.09.001,
Hofmann, K., Praeg, N., Mutschlechner, M., Wagner, A. O., and Illmer, P. (2016). Abundance and potential metabolic activity of methanogens in well-aerated forest and grassland soils of an alpine region. FEMS Microbiol. Ecol. 92:fiv171. doi: 10.1093/femsec/fiv171,
Hu, L., Dong, Z., Wang, Z., Xiao, L., and Zhu, B. (2022). The contributions of ammonia oxidizing bacteria and archaea to nitrification-dependent N2O emission in alkaline and neutral purple soils. Sci. Rep. 12:19928. doi: 10.1038/s41598-022-23084-1,
Hu, W., Hou, Q., Delgado-Baquerizo, M., Stegen, J. C., du, Q., Dong, L., et al. (2022). Continental-scale niche differentiation of dominant topsoil archaea in drylands. Environ. Microbiol. 24, 5483–5497. doi: 10.1111/1462-2920.16099,
Hua, Z., Ouellette, M., Makkay, A. M., Papke, R. T., and Zhaxybayeva, O. (2021). Nutrient supplementation experiments with saltern microbial communities implicate utilization of DNA as a source of phosphorus. ISME J. 15, 2853–2864. doi: 10.1038/s41396-021-00960-8,
Ishfaq, M., Wang, Y., Xu, J., Hassan, M. U., Yuan, H., Liu, L., et al. (2023). Improvement of nutritional quality of food crops with fertilizer: a global meta-analysis. Agron. Sustain. Dev. 43:74. doi: 10.1007/s13593-023-00923-7
Jiang, P., Xiao, L. Q., Wan, X., Yu, T., Liu, Y. F., et al. (2022). Research Progress on microbial carbon sequestration in soil: a review. Eurasian Soil Sci. 55, 1395–1404. doi: 10.1134/S1064229322100064
Jiao, S., Xu, Y., Zhang, J., Hao, X., and Lu, Y. (2019a). Core microbiota in agricultural soils and their potential associations with nutrient cycling. mSystems 4, 10–128. doi: 10.1128/mSystems.00313-18,
Jiao, S., Xu, Y., Zhang, J., and Lu, Y. (2019b). Environmental filtering drives distinct continental atlases of soil archaea between dryland and wetland agricultural ecosystems. Microbiome 7:15. doi: 10.1186/s40168-019-0630-9,
Jung, M.-Y., Gwak, J. H., Rohe, L., Giesemann, A., Kim, J. G., Well, R., et al. (2019). Indications for enzymatic denitrification to N2O at low pH in an ammonia-oxidizing archaeon. ISME J. 13, 2633–2638. doi: 10.1038/s41396-019-0460-6,
Jung, M.-Y., Park, S.-J., Kim, S. J., Kim, J. G., Sinninghe Damsté, J. S., Jeon, C. O., et al. (2014a). A mesophilic, autotrophic, Ammonia-oxidizing archaeon of Thaumarchaeal group I.1a cultivated from a deep oligotrophic soil horizon. Appl. Environ. Microbiol. 80, 3645–3655. doi: 10.1128/AEM.03730-13,
Jung, M.-Y., Sedlacek, C. J., Kits, K. D., Mueller, A. J., Rhee, S. K., Hink, L., et al. (2022). Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. ISME J. 16, 272–283. doi: 10.1038/s41396-021-01064-z,
Jung, M.-Y., Well, R., Min, D., Giesemann, A., Park, S. J., Kim, J. G., et al. (2014b). Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. ISME J. 8, 1115–1125. doi: 10.1038/ismej.2013.205,
Kalev, S. D., and Toor, G. S. (2018). “The composition of soils and sediments” in Green chemistry (Elsevier), 339–357.
Kallenbach, C. M., Frey, S. D., and Grandy, A. S. (2016). Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7:13630. doi: 10.1038/ncomms13630,
Kandeler, E., Deiglmayr, K., Tscherko, D., Bru, D., and Philippot, L. (2006). Abundance of narG, nirS, nirK, and nosZ genes of denitrifying Bacteria during primary successions of a glacier foreland. Appl. Environ. Microbiol. 72, 5957–5962. doi: 10.1128/AEM.00439-06
Kim, W., and Whitman, W. B. (2014). “Methanogens” in Encyclopedia of food microbiology (Elsevier), 602–606.
Kobayashi, S., Hira, D., Yoshida, K., Toyofuku, M., Shida, Y., Ogasawara, W., et al. (2018). Nitric oxide production from nitrite reduction and hydroxylamine oxidation by copper-containing dissimilatory nitrite reductase (NirK) from the aerobic Ammonia-oxidizing archaeon, Nitrososphaera viennensis. Microbes Environ. 33, 428–434. doi: 10.1264/jsme2.ME18058,
Koirala, A., and Brözel, V. S. (2021). Phylogeny of nitrogenase structural and assembly components reveals new insights into the origin and distribution of nitrogen fixation across Bacteria and Archaea. Microorganisms 9:1662. doi: 10.3390/microorganisms9081662,
Kong, D., Li, S., Jin, Y., Wu, S., Chen, J., Hu, T., et al. (2019). Linking methane emissions to methanogenic and methanotrophic communities under different fertilization strategies in rice paddies. Geoderma 347, 233–243. doi: 10.1016/j.geoderma.2019.04.008
Könneke, M., Bernhard, A. E., de la Torre, J. R., Walker, C. B., Waterbury, J. B., and Stahl, D. A. (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546. doi: 10.1038/nature03911,
Könneke, M., Schubert, D. M., Brown, P. C., Hügler, M., Standfest, S., Schwander, T., et al. (2014). Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc. Natl. Acad. Sci. 111, 8239–8244. doi: 10.1073/pnas.1402028111,
Kono, T., Mehrotra, S., Endo, C., Kizu, N., Matusda, M., Kimura, H., et al. (2017). A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea. Nat. Commun. 8:14007. doi: 10.1038/ncomms14007,
Kopittke, P. M., Menzies, N. W., Wang, P., McKenna, B. A., and Lombi, E. (2019). Soil and the intensification of agriculture for global food security. Environ. Int. 132:105078. doi: 10.1016/j.envint.2019.105078
Kouzuma, A., Tsutsumi, M., Ishii, S., Ueno, Y., Abe, T., and Watanabe, K. (2017). Non-autotrophic methanogens dominate in anaerobic digesters. Sci. Rep. 7:1510. doi: 10.1038/s41598-017-01752-x,
Kraft, B., Jehmlich, N., Larsen, M., Bristow, L. A., Könneke, M., Thamdrup, B., et al. (2022). Oxygen and nitrogen production by an ammonia-oxidizing archaeon. Science 375, 97–100. doi: 10.1126/science.abe6733,
Legierse, A., Struik, Q., Smith, G., Echeveste Medrano, M. J., Weideveld, S., van Dijk, G., et al. (2023). Nitrate-dependent anaerobic methane oxidation (N-DAMO) as a bioremediation strategy for waters affected by agricultural runoff. FEMS Microbiol. Lett. 370:fnad041. doi: 10.1093/femsle/fnad041,
Lehtovirta-Morley, L. E., Ge, C., Ross, J., Yao, H., Hazard, C., Gubry-Rangin, C., et al. (2024). Nitrosotalea devaniterrae gen. Nov., sp. nov. and Nitrosotalea sinensis sp. nov., two acidophilic ammonia oxidising archaea isolated from acidic soil, and proposal of the new order Nitrosotaleales Ord. Nov. within the class Nitrososphaeria of the phylum Nitrososphaerota. Int. J. Syst. Evol. Microbiol. 74:006387. doi: 10.1099/ijsem.0.006387
Leigh, J. A. (2000). Nitrogen fixation in methanogens: the archaeal perspective. Curr. Issues Mol. Biol. 4, 125–131. doi: 10.21775/cimb.002.125
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G. W., et al. (2006). Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809. doi: 10.1038/nature04983,
Lemaire, O. N., Jespersen, M., and Wagner, T. (2020). CO2-fixation strategies in energy extremophiles: what can we learn from acetogens? Front. Microbiol. 11:486. doi: 10.3389/fmicb.2020.00486,
Li, Z., Zeng, Z., Tian, D., Wang, J., Fu, Z., Zhang, F., et al. (2020). Global patterns and controlling factors of soil nitrification rate. Glob. Chang. Biol. 26, 4147–4157. doi: 10.1111/gcb.15119,
Li, H., Zhuang, L., Cai, H., Ni, Y., Chu, T., Chen, L., et al. (2025). Nitrosarchaeum haohaiensis sp. Nov. CL1T: isolation and characterisation of a novel Ammonia-oxidising archaeon from aquatic environments. Environ. Microbiol. Rep. 17:e70100. doi: 10.1111/1758-2229.70100,
Li, X., et al. (2023). Control factors of soil diazotrophic community assembly and nitrogen fixation rate across eastern China. Geoderma 432:116410. doi: 10.1016/j.geoderma.2023.116410
Liao, H., Qin, F., Wang, K., Zhang, Y., Hao, X., Chen, W., et al. (2020). Long-term chemical fertilization-driving changes in soil autotrophic microbial community depresses soil CO2 fixation in a Mollisol. Sci. Total Environ. 748:141317. doi: 10.1016/j.scitotenv.2020.141317,
Liu, H., Li, J., Zhao, Y., Xie, K., Tang, X., Wang, S., et al. (2018). Ammonia oxidizers and nitrite-oxidizing bacteria respond differently to long-term manure application in four paddy soils of south of China. Sci. Total Environ. 633, 641–648. doi: 10.1016/j.scitotenv.2018.03.108,
Liu, Z., Liu, J., Yu, Z., Li, Y., Hu, X., Gu, H., et al. (2022). Archaeal communities perform an important role in maintaining microbial stability under long term continuous cropping systems. Sci. Total Environ. 838:156413. doi: 10.1016/j.scitotenv.2022.156413,
Liu, Y., and Whitman, W. B. (2008). Metabolic, phylogenetic, and ecological diversity of the methanogenic Archaea. Ann. N. Y. Acad. Sci. 1125, 171–189. doi: 10.1196/annals.1419.019
Lu, J., Chao, Y., Tian, L., Zhong, X., Chen, Z., He, H., et al. (2025). DNA viral community enhances microbial carbon fixation capacity via auxiliary metabolic genes in contaminated soils. Nat. Commun. 16:9984. doi: 10.1038/s41467-025-64938-2,
Luo, Z.-H., Narsing Rao, M. P., Chen, H., Hua, Z. S., Li, Q., Hedlund, B. P., et al. (2021). Genomic insights of "Candidatus Nitrosocaldaceae" based on nine new metagenome-assembled genomes, including "Candidatus Nitrosothermus" gen Nov. and two new species of "Candidatus Nitrosocaldus". Front. Microbiol. 11:608832. doi: 10.3389/fmicb.2020.608832,
Lyu, Z., Shao, N., Akinyemi, T., and Whitman, W. B. (2018). Methanogenesis. Curr. Biol. 28, R727–R732. doi: 10.1016/j.cub.2018.05.021
Ma, Y., Zilles, J. L., and Kent, A. D. (2019). An evaluation of primers for detecting denitrifiers via their functional genes. Environ. Microbiol. 21, 1196–1210. doi: 10.1111/1462-2920.14555,
Manns, H. R., Parkin, G. W., and Martin, R. C. (2016). Evidence of a union between organic carbon and water content in soil. Can. J. Soil Sci. 96, 305–316. doi: 10.1139/cjss-2015-0084
Mao, Y., Wu, J., Yang, R., Ma, Y., Ye, J., Zhong, J., et al. (2024). Novel database for accA gene revealed a vertical variability pattern of autotrophic carbon fixation potential of ammonia oxidizing archaea in a permeable subterranean estuary. Mar. Environ. Res. 194:106342. doi: 10.1016/j.marenvres.2024.106342,
Martínez-Espinosa, R. M. (2024). Halophilic archaea as tools for bioremediation technologies. Appl. Microbiol. Biotechnol. 108:401. doi: 10.1007/s00253-024-13241-z,
Masuda, Y., Satoh, S., Miyamoto, R., Takano, R., Ishii, K., Ohba, H., et al. (2023). Biological nitrogen fixation in the long-term nitrogen-fertilized and unfertilized paddy fields, with special reference to diazotrophic iron-reducing bacteria. Arch. Microbiol. 205:291. doi: 10.1007/s00203-023-03631-8,
McGlynn, S. E. (2017). Energy metabolism during anaerobic methane oxidation in ANME Archaea. Microbes Environ. 32, 5–13. doi: 10.1264/jsme2.ME16166,
Megyes, M., Borsodi, A. K., Árendás, T., and Márialigeti, K. (2021). Variations in the diversity of soil bacterial and archaeal communities in response to different long-term fertilization regimes in maize fields. Appl. Soil Ecol. 168:104120. doi: 10.1016/j.apsoil.2021.104120
Mehta, M. P., and Baross, J. A. (2006). Nitrogen fixation at 92°C by a hydrothermal vent archaeon. Science 314, 1783–1786. doi: 10.1126/science.1134772,
Miralles-Robledillo, J. M., Bernabeu, E., Giani, M., Martínez-Serna, E., Martínez-Espinosa, R. M., and Pire, C. (2021). Distribution of denitrification among haloarchaea: a comprehensive study. Microorganisms 9:1669. doi: 10.3390/microorganisms9081669,
Miralles-Robledillo, J. M., Martínez-Espinosa, R. M., and Pire, C. (2024). Transcriptomic profiling of haloarchaeal denitrification through RNA-Seq analysis. Appl. Environ. Microbiol. 90:e0057124. doi: 10.1128/aem.00571-24,
Mise, K., Masuda, Y., Senoo, K., and Itoh, H. (2021). Undervalued Pseudo- nifH sequences in public databases distort metagenomic insights into biological nitrogen fixers. mSphere 6, e00785–e00721. doi: 10.1128/msphere.00785-21,
Miyazaki, J., Higa, R., Toki, T., Ashi, J., Tsunogai, U., Nunoura, T., et al. (2009). Molecular characterization of potential nitrogen fixation by anaerobic methane-oxidizing Archaea in the methane seep sediments at the number 8 Kumano knoll in the Kumano Basin, offshore of Japan. Appl. Environ. Microbiol. 75, 7153–7162. doi: 10.1128/AEM.01184-09,
Moissl-Eichinger, C., Pausan, M., Taffner, J., Berg, G., Bang, C., and Schmitz, R. A. (2018). Archaea are interactive components of complex microbiomes. Trends Microbiol. 26, 70–85. doi: 10.1016/j.tim.2017.07.004
Mukhtar, H., Lin, Y. P., Lin, C. M., and Lin, Y. R. (2019). Relative abundance of Ammonia oxidizing Archaea and Bacteria influences soil nitrification responses to temperature. Microorganisms 7:526. doi: 10.3390/microorganisms7110526,
Mukhtar, S., Zahra Shah, H., Mehnaz, S., and Abdulla Malik, K. (2024). Isolation and characterization of plant growth promoting and metal resistant Archaea associated with the rhizosphere of Salsola stocksii and Atriplex amnicola. Geomicrobiol J. 41, 755–768. doi: 10.1080/01490451.2024.2381008
Naitam, M. G., and Kaushik, R. (2021). Archaea: an Agro-ecological perspective. Curr. Microbiol. 78, 2510–2521. doi: 10.1007/s00284-021-02537-2,
Naitam, M. G., Ramakrishnan, B., Grover, M., and Kaushik, R. (2023). Rhizosphere-dwelling halophilic archaea: a potential candidate for alleviating salinity-associated stress in agriculture. Front. Microbiol. 14. doi: 10.3389/fmicb.2023.1212349,
Narrowe, A. B., Borton, M. A., Hoyt, D. W., Smith, G. J., Daly, R. A., Angle, J. C., et al. (2019). Uncovering the diversity and activity of methylotrophic methanogens in freshwater wetland soils. mSystems 4. doi: 10.1128/msystems.00320-19,
Nealson, K. H., and Stahl, D. A. (1997). “Chapter 1. Microorganisms and biogeochemical cycles: what can we learn from layered microbial communities?” in Geomicrobiology (Berlin, Boston: De Gruyter), 5–34.
Nepel, M., Angel, R., Borer, E. T., Frey, B., MacDougall, A., McCulley, R., et al. (2022). Global grassland diazotrophic communities are structured by combined abiotic, biotic, and spatial distance factors but resilient to fertilization. Front. Microbiol. 13:821030. doi: 10.3389/fmicb.2022.821030,
Nie, W.-B., Ding, J., Xie, G. J., Yang, L., Peng, L., Tan, X., et al. (2021). Anaerobic oxidation of methane coupled with dissimilatory nitrate reduction to ammonium fuels anaerobic ammonium oxidation. Environ. Sci. Technol. 55, 1197–1208. doi: 10.1021/acs.est.0c02664,
Norman, J. S., Lin, L., and Barrett, J. E. (2015). Paired carbon and nitrogen metabolism by ammonia-oxidizing bacteria and archaea in temperate forest soils. Ecosphere 6, 1–11. doi: 10.1890/ES14-00299.1
Odelade, K., and Babalola, O. (2019). Bacteria, Fungi and Archaea domains in Rhizospheric soil and their effects in enhancing agricultural productivity. Int. J. Environ. Res. Public Health 16:3873. doi: 10.3390/ijerph16203873,
Offre, P., Spang, A., and Schleper, C. (2013). Archaea in biogeochemical cycles. Ann. Rev. Microbiol. 67, 437–457. doi: 10.1146/annurev-micro-092412-155614
Oren, A. (2002). Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J. Ind. Microbiol. Biotechnol. 28, 56–63. doi: 10.1038/sj/jim/7000176,
Ouyang, Y., Norton, J. M., and Stark, J. M. (2017). Ammonium availability and temperature control contributions of ammonia oxidizing bacteria and archaea to nitrification in an agricultural soil. Soil Biol. Biochem. 113, 161–172. doi: 10.1016/j.soilbio.2017.06.010
Oxley, A. P. A., Lanfranconi, M. P., Würdemann, D., Ott, S., Schreiber, S., McGenity, T. J., et al. (2010). Halophilic archaea in the human intestinal mucosa. Environ. Microbiol. 12, 2398–2410. doi: 10.1111/j.1462-2920.2010.02212.x,
Pi, H.-W., Lin, J. J., Chen, C. A., Wang, P. H., Chiang, Y. R., Huang, C. C., et al. (2022). Origin and evolution of nitrogen fixation in prokaryotes. Mol. Biol. Evol. 39. doi: 10.1093/molbev/msac181,
Poly, F., Monrozier, L. J., and Bally, R. (2001). Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 152, 95–103. doi: 10.1016/S0923-2508(00)01172-4,
Poth, M., and Focht, D. D. (1985). 15 N kinetic analysis of N2O production by Nitrosomonas europaea: an examination of nitrifier denitrification. Appl. Environ. Microbiol. 49, 1134–1141. doi: 10.1128/aem.49.5.1134-1141.1985,
Pratscher, J., Dumont, M. G., and Conrad, R. (2011). Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc. Natl. Acad. Sci. 108, 4170–4175. doi: 10.1073/pnas.1010981108,
Prosser, J. I., Hink, L., Gubry-Rangin, C., and Nicol, G. W. (2020). Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Glob. Chang. Biol. 26, 103–118. doi: 10.1111/gcb.14877,
Prosser, J. I., and Nicol, G. W. (2012). Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523–531. doi: 10.1016/j.tim.2012.08.001,
Qin, W., Meinhardt, K. A., Moffett, J. W., Devol, A. H., Virginia Armbrust, E., Ingalls, A. E., et al. (2017). Influence of oxygen availability on the activities of ammonia-oxidizing archaea. Environ. Microbiol. Rep. 9, 250–256. doi: 10.1111/1758-2229.12525,
Qin, W., Wei, S. P., Zheng, Y., Choi, E., Li, X., Johnston, J., et al. (2024). Ammonia-oxidizing bacteria and archaea exhibit differential nitrogen source preferences. Nat. Microbiol. 9, 524–536. doi: 10.1038/s41564-023-01593-7,
Rafiq, M., Hassan, N., Rehman, M., Hayat, M., Nadeem, G., Hassan, F., et al. (2023). Challenges and approaches of culturing the unculturable Archaea. Biology 12:1499. doi: 10.3390/biology12121499,
Raghoebarsing, A. A., Pol, A., van de Pas-Schoonen, K., Smolders, A. J., Ettwig, K. F., Rijpstra, W. I., et al. (2006). A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440, 918–921. doi: 10.1038/nature04617,
Reeve, J. N., Nölling, J., Morgan, R. M., and Smith, D. R. (1997). Methanogenesis: genes, genomes, and who’s on first? J. Bacteriol. 179, 5975–5986. doi: 10.1128/jb.179.19.5975-5986.1997,
Rinke, C., Chuvochina, M., Mussig, A. J., Chaumeil, P. A., Davín, A. A., Waite, D. W., et al. (2021). A standardized archaeal taxonomy for the genome taxonomy database. Nat. Microbiol. 6, 946–959. doi: 10.1038/s41564-021-00918-8,
Ritchie, G. A. F., and Nicholas, D. J. D. (1972). Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochem. J. 126, 1181–1191. doi: 10.1042/bj1261181,
Riyaz, Z., and Khan, S. T. (2025). Nitrogen fixation by methanogenic Archaea, literature review and DNA database-based analysis; significance in face of climate change. Arch. Microbiol. 207:6. doi: 10.1007/s00203-024-04191-1,
Robinson, A., Di, H. J., Cameron, K. C., Podolyan, A., and He, J. (2014). The effect of soil pH and dicyandiamide (DCD) on N2O emissions and ammonia oxidiser abundance in a stimulated grazed pasture soil. J. Soils Sediments 14, 1434–1444. doi: 10.1007/s11368-014-0888-2
Rösch, C., Mergel, A., and Bothe, H. (2002). Biodiversity of denitrifying and dinitrogen-fixing Bacteria in an acid Forest soil. Appl. Environ. Microbiol. 68, 3818–3829. doi: 10.1128/AEM.68.8.3818-3829.2002,
Rusch, A. (2013). Molecular tools for the detection of nitrogen cycling Archaea. Archaea 2013, 1–10. doi: 10.1155/2013/676450,
Rütting, T., et al. (2021). The contribution of ammonia-oxidizing archaea and bacteria to gross nitrification under different substrate availability. Soil Biol. Biochem. 160:108353. doi: 10.1016/j.soilbio.2021.108353
Saghaï, A., Banjeree, S., Degrune, F., Edlinger, A., García-Palacios, P., Garland, G., et al. (2022). Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils. Environ. Microbiol. 24, 341–356. doi: 10.1111/1462-2920.15830,
Sahu, N., Vasu, D., Sahu, A., Lal, N., and Singh, S. K. (2017). “Strength of microbes in nutrient cycling: a key to soil health” in Agriculturally important microbes for sustainable agriculture (Singapore: Springer Singapore), 69–86.
Santoro, A. E., Buchwald, C., McIlvin, M., and Casciotti, K. L. (2011). Isotopic signature of N2O produced by marine Ammonia-oxidizing Archaea. Science 333, 1282–1285. doi: 10.1126/science.1208239,
Schleper, C., and Nicol, G. W. (2010). Ammonia-oxidising Archaea – physiology, ecology and evolution, 1–41. doi: 10.1016/B978-0-12-381045-8.00001-1
Serrano-Silva, N., et al. (2014). Methanogenesis and Methanotrophy in soil: a review. Pedosphere 24, 291–307. doi: 10.1016/S1002-0160(14)60016-3
Shah, T., Lateef, S., and Noor, M. A. (2020). “Carbon and nitrogen cycling in agroecosystems: an overview” in Carbon and nitrogen cycling in soil (Singapore: Springer Singapore), 1–15.
Shaw, L. J., Nicol, G. W., Smith, Z., Fear, J., Prosser, J. I., and Baggs, E. M. (2006). Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ. Microbiol. 8, 214–222. doi: 10.1111/j.1462-2920.2005.00882.x,
Shen, L., Yang, W. T., Yang, Y. L., Liu, X., Tian, M. H., Jin, J. H., et al. (2021). Spatial and temporal variations of the community structure and abundance of Candidatus Methanoperedens nitroreducens-like archaea in paddy soils. Eur. J. Soil Biol. 106:103345. doi: 10.1016/j.ejsobi.2021.103345
Shi, Y., Adams, J. M., Ni, Y., Yang, T., Jing, X., Chen, L., et al. (2016). The biogeography of soil archaeal communities on the eastern Tibetan plateau. Sci. Rep. 6:38893. doi: 10.1038/srep38893,
Shima, S., and Thauer, R. K. (2005). Methyl-coenzyme M reductase and the anaerobic oxidation of methane in methanotrophic Archaea. Curr. Opin. Microbiol. 8, 643–648. doi: 10.1016/j.mib.2005.10.002
Singh, D., Kaushik, R., Chakdar, H., and Saxena, A. K. (2023). Unveiling novel insights into haloarchaea (Halolamina pelagica CDK2) for alleviation of drought stress in wheat. World J. Microbiol. Biotechnol. 39:328. doi: 10.1007/s11274-023-03781-3,
Spiertz, J. H. J. (2010). Nitrogen, sustainable agriculture and food security. A review. Agron. Sustain. Dev. 30, 43–55. doi: 10.1051/agro:2008064
Stachler, A.-E., Schwarz, T. S., Schreiber, S., and Marchfelder, A. (2020). CRISPRi as an efficient tool for gene repression in archaea. Methods 172, 76–85. doi: 10.1016/j.ymeth.2019.05.023,
Stein, L. Y., Arp, D. J., Berube, P. M., Chain, P. S., Hauser, L., Jetten, M. S., et al. (2007). Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ. Microbiol. 9, 2993–3007. doi: 10.1111/j.1462-2920.2007.01409.x,
Sterngren, A. E., Hallin, S., and Bengtson, P. (2015). Archaeal Ammonia oxidizers dominate in numbers, but Bacteria drive gross nitrification in N-amended grassland soil. Front. Microbiol. 6:1350. doi: 10.3389/fmicb.2015.01350,
Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeister-Boltenstern, S., Richter, A., et al. (2014). Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J. 8, 1135–1146. doi: 10.1038/ismej.2013.220,
Stoltzfus, J. R., So, R. M. P. P., Malarvithi, P. P., Ladha, J. K., and De Bruijn, F. J. (1997). Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant Soil 194, 25–36. doi: 10.1023/A:1004298921641
Sun, Y., Liu, Y., Pan, J., Wang, F., and Li, M. (2020). Perspectives on cultivation strategies of Archaea. Microb. Ecol. 79, 770–784. doi: 10.1007/s00248-019-01422-7,
Tan, X., Lu, Y., Nie, W. B., Evans, P., Wang, X. W., Dang, C. C., et al. (2024). Nitrate-dependent anaerobic methane oxidation coupled to Fe(III) reduction as a source of ammonium and nitrous oxide. Water Res. 256:121571. doi: 10.1016/j.watres.2024.121571,
Thomson, A. J., Giannopoulos, G., Pretty, J., Baggs, E. M., and Richardson, D. J. (2012). Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philos. Trans. Royal Soc. B 367, 1157–1168. doi: 10.1098/rstb.2011.0415,
Torregrosa-Crespo, J., Bergaust, L., Pire, C., and Martínez-Espinosa, R. M. (2018). Denitrifying haloarchaea: sources and sinks of nitrogenous gases. FEMS Microbiol. Lett. 365:fnx270. doi: 10.1093/femsle/fnx270,
Torregrosa-Crespo, J., Pire, C., Bergaust, L., and Martínez-Espinosa, R. M. (2020b). Haloferax mediterranei, an archaeal model for denitrification in saline systems, characterized through integrated physiological and transcriptional analyses. Front. Microbiol. 11:768. doi: 10.3389/fmicb.2020.00768,
Torregrosa-Crespo, J., Pire, C., Martínez-Espinosa, R. M., and Bergaust, L. (2019). Denitrifying haloarchaea within the genus Haloferax display divergent respiratory phenotypes, with implications for their release of nitrogenous gases. Environ. Microbiol. 21, 427–436. doi: 10.1111/1462-2920.14474,
Torregrosa-Crespo, J., Pire, C., Richardson, D. J., and Martínez-Espinosa, R. M. (2020a). Exploring the molecular machinery of denitrification in Haloferax mediterranei through proteomics. Front. Microbiol. 11:605859. doi: 10.3389/fmicb.2020.605859,
Tully, K., and Ryals, R. (2017). Nutrient cycling in agroecosystems: balancing food and environmental objectives. Agroecol. Sustain. Food Syst. 41, 761–798. doi: 10.1080/21683565.2017.1336149
Vajrala, N., Martens-Habbena, W., Sayavedra-Soto, L. A., Schauer, A., Bottomley, P. J., Stahl, D. A., et al. (2013). Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc. Natl. Acad. Sci. 110, 1006–1011. doi: 10.1073/pnas.1214272110,
Vaksmaa, A., Lüke, C., Van Alen, T., Valè, G., Lupotto, E., Jetten, M. M., et al. (2016). Distribution and activity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soil. FEMS Microbiol. Ecol. 92:fiw181. doi: 10.1093/femsec/fiw181
Ventura, J. P., Lacerda-Júnior, G. V., Rados, T., Bisson, A., Fernandes-Júnior, P. I., and Melo, I. S. (2025). Harnessing haloarchaea from halophyte Atriplex nummularia rhizosphere to enhance salt stress tolerance in maize seedlings. Environ. Microb. [Preprint 21:12. doi: 10.1186/s40793-025-00698-2,
Walker, C. B., de la Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., et al. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. 107, 8818–8823. doi: 10.1073/pnas.0913533107,
Wan, X. S., Hou, L., Kao, S. J., Zhang, Y., Sheng, H. X., Shen, H., et al. (2023). Pathways of N2O production by marine ammonia-oxidizing archaea determined from dual-isotope labeling. Proc. Natl. Acad. Sci. 120:e2220697120. doi: 10.1073/pnas.2220697120,
Wang, H., Bier, R., Zgleszewski, L., Peipoch, M., Omondi, E., Mukherjee, A., et al. (2020). Distinct distribution of Archaea from soil to freshwater to estuary: implications of archaeal composition and function in different environments. Front. Microbiol. 11:576661. doi: 10.3389/fmicb.2020.576661,
Wang, X., Chi, Y., and Song, S. (2024). Important soil microbiota’s effects on plants and soils: a comprehensive 30-year systematic literature review. Front. Microbiol. 15:1347745. doi: 10.3389/fmicb.2024.1347745,
Wang, S., Chong, W., Wan, X., Sun, X., Wang, M., Lou, X., et al. (2024). Optimizing the activity of denitrifying anaerobic methane oxidation archaea by tailoring micronutrient compositions: a strategy for enhanced nitrate reduction. Chem. Eng. J. 502:158113. doi: 10.1016/j.cej.2024.158113
Wang, Q., Chu, C., Zhao, Z., Zhou, D., and Wu, S. (2024). A study of different agricultural practices over a dozen years: influence on soil CO2 fixation rates and soil autotrophic microbial communities. Soil Tillage Res. 239:106067. doi: 10.1016/j.still.2024.106067
Wang, Z., Li, Y., Zheng, W., Ji, Y., Duan, M., and Ma, L. (2023). Ammonia oxidizing archaea and bacteria respond to different manure application rates during organic vegetable cultivation in Northwest China. Sci. Rep. 13:8064. doi: 10.1038/s41598-023-35134-3,
Wang, S., Sun, P., Liu, J., Xu, Y., Dolfing, J., and Wu, Y. (2023). Distribution of methanogenic and methanotrophic consortia at soil-water interfaces in rice paddies across climate zones. iScience 26:105851. doi: 10.1016/j.isci.2022.105851,
Wang, X., Tan, X., Dang, C. C., Liu, L. Y., Wang, X. W., et al. (2025). Manganese-mediated dissimilatory nitrate reduction to ammonium of nitrate-dependent anaerobic methane oxidation. Chem. Eng. J. 506:159901. doi: 10.1016/j.cej.2025.159901
Wang, J., Yao, X., Jia, Z., Zhu, L., Zheng, P., Kartal, B., et al. (2022). Nitrogen input promotes denitrifying methanotrophs’ abundance and contribution to methane emission reduction in coastal wetland and paddy soil. Environ. Pollut. 302:119090. doi: 10.1016/j.envpol.2022.119090,
Wei, W., Isobe, K., Nishizawa, T., Zhu, L., Shiratori, Y., Ohte, N., et al. (2015). Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J. 9, 1954–1965. doi: 10.1038/ismej.2015.9,
Wei, H., Wang, M., Ya, M., and Xu, C. (2022). The denitrifying anaerobic methane oxidation process and microorganisms in the environments: a review. Front. Mar. Sci. 9:1038400. doi: 10.3389/fmars.2022.1038400
Wright, C. L., and Lehtovirta-Morley, L. E. (2023). Nitrification and beyond: metabolic versatility of ammonia oxidising archaea. ISME J. 17, 1358–1368. doi: 10.1038/s41396-023-01467-0,
Wu, J., Hong, Y., He, X., Liu, X., Ye, J., Jiao, L., et al. (2022). Niche differentiation of ammonia-oxidizing archaea and related autotrophic carbon fixation potential in the water column of the South China Sea. iScience 25:104333. doi: 10.1016/j.isci.2022.104333,
Wu, C., Tang, X., Tan, C., Sun, T., Zeng, Y., Liu, Y., et al. (2025). Long-term substitution of chemical fertilizer with organic manure enhances the activity and autotrophic growth of ammonia-oxidizing archaea and comammox nitrospira in paddy soil. J. Environ. Manag. 396:127816. doi: 10.1016/j.jenvman.2025.127816,
Wu, K., Zhou, L., Tahon, G., Liu, L., Li, J., Zhang, J., et al. (2024). Isolation of a methyl-reducing methanogen outside the Euryarchaeota. Nature 632, 1124–1130. doi: 10.1038/s41586-024-07728-y,
Xia, W., Bowatte, S., Jia, Z., and Newton, P. (2022). Offsetting N2O emissions through nitrifying CO2 fixation in grassland soil. Soil Biol. Biochem. 165:108528. doi: 10.1016/j.soilbio.2021.108528
Yadav, A. N., Sharma, D., Gulati, S., Singh, S., Dey, R., Pal, K. K., et al. (2015). Haloarchaea endowed with phosphorus solubilization attribute implicated in phosphorus cycle. Sci. Rep. 5:12293. doi: 10.1038/srep12293,
Yakimov, M.M., Cono, V.La, and Denaro, R. (2009) “A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota of Tyrrhenian Sea,” Deep-Sea Res. II Top. Stud. Oceanogr., 56, pp. 748–754. doi:doi: 10.1016/j.dsr2.2008.07.024.
Yao, H., Gao, Y., Nicol, G. W., Campbell, C. D., Prosser, J. I., Zhang, L., et al. (2011). Links between Ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl. Environ. Microbiol. 77, 4618–4625. doi: 10.1128/AEM.00136-11,
Yuan, J., Yuan, Y., Zhu, Y., and Cao, L. (2018). Effects of different fertilizers on methane emissions and methanogenic community structures in paddy rhizosphere soil. Sci. Total Environ. 627, 770–781. doi: 10.1016/j.scitotenv.2018.01.233,
Zehnle, H., and Schoelmerich, M. C. (2025). Candidatus Methanoperedens. Trends Microbiol. 33, 472–473. doi: 10.1016/j.tim.2025.01.015,
Zeng, Y., Tan, C., Zhang, L., You, L., Zheng, W., Chen, H., et al. (2024). Long-term addition of organic manure stimulates the growth and activity of comammox in a subtropical Inceptisol. Sci. Total Environ. 948:174839. doi: 10.1016/j.scitotenv.2024.174839,
Zhalnina, K., de Quadros, P. D., Camargo, F. A., and Triplett, E. W. (2012). Drivers of archaeal ammonia-oxidizing communities in soil. Front. Microbiol. 3:210. doi: 10.3389/fmicb.2012.00210,
Zhang, Y., Ning, D., Wu, L., Yuan, M. M., Zhou, X., Guo, X., et al. (2023). Experimental warming leads to convergent succession of grassland archaeal community. Nat. Clim. Chang. 13, 561–569. doi: 10.1038/s41558-023-01664-x
Zhang, Y., Wang, F., Xia, W., Cao, W., and Jia, Z. (2021). Anaerobic methane oxidation sustains soil organic carbon accumulation. Appl. Soil Ecol. 167:104021. doi: 10.1016/j.apsoil.2021.104021
Zhang, J. B., Zhu, T. B., Cai, Z. C., Qin, S. W., and Müller, C. (2012). Effects of long-term repeated mineral and organic fertilizer applications on soil nitrogen transformations. Eur. J. Soil Sci. 63, 75–85. doi: 10.1111/j.1365-2389.2011.01410.x
Zhao, L., Chen, J., Shen, G., Zhou, Y., Zhang, X., Zhou, Y., et al. (2025). Dissimilatory nitrate reduction to ammonia in the natural environment and wastewater treatment facilities: a comprehensive review. Environ. Technol. Innov. 37:104011. doi: 10.1016/j.eti.2024.104011
Zhao, J., Huang, L., Chakrabarti, S., Cooper, J., Choi, E., Ganan, C., et al. (2023). Nitrogen and phosphorous acquisition strategies drive coexistence patterns among archaeal lineages in soil. ISME J. 17, 1839–1850. doi: 10.1038/s41396-023-01493-y,
Zhao, Y., Liu, Y., Cao, S., Hao, Q., Liu, C., and Li, Y. (2024). Anaerobic oxidation of methane driven by different electron acceptors: a review. Sci. Total Environ. 946:174287. doi: 10.1016/j.scitotenv.2024.174287,
Zhao, S., van der Heijden, M., Banerjee, S., Liu, J. J., Gu, H. D., Zhou, N., et al. (2024). The role of halophyte-induced saline fertile islands in soil microbial biogeochemical cycling across arid ecosystems. Commun. Biol. 7:1061. doi: 10.1038/s42003-024-06741-1,
Zhao, J., Wang, B., Zhou, X., Alam, M. S., Fan, J., Guo, Z., et al. (2022). Long-term adaptation of acidophilic archaeal Ammonia oxidisers following different soil fertilisation histories. Microb. Ecol. 83, 424–435. doi: 10.1007/s00248-021-01763-2,
Zheng, Y., Hou, L., Chen, F., Zhou, J., Liu, M., Yin, G., et al. (2020). Denitrifying anaerobic methane oxidation in intertidal marsh soils: occurrence and environmental significance. Geoderma 357:113943. doi: 10.1016/j.geoderma.2019.113943
Zheng, Y., Wang, B., Gao, P., Yang, Y., Xu, B., Su, X., et al. (2024). Novel order-level lineage of ammonia-oxidizing archaea widespread in marine and terrestrial environments. ISME J. 18:wrad002. doi: 10.1093/ismejo/wrad002,
Zhou, G., Fan, K., Li, G., Gao, S., Chang, D., Liang, T., et al. (2023). Synergistic effects of diazotrophs and arbuscular mycorrhizal fungi on soil biological nitrogen fixation after three decades of fertilization. iMeta 2:e81. doi: 10.1002/imt2.81,
Keywords: ammonia-oxidizing archaea, haloarchaea, methanogenic archaea, n-damo archaea, nutrient cycling
Citation: Speek BM, Suleiman AKA, Keuning E, Sechi V, Buisman CJN and Bezemer TM (2026) The hidden potential of archaea in carbon and nitrogen cycling in agricultural soils: a review. Front. Microbiol. 17:1755559. doi: 10.3389/fmicb.2026.1755559
Edited by:
Huaihai Chen, Sun Yat-sen University, ChinaReviewed by:
Aiju Liu, Shandong University of Technology, ChinaZhan Wang, Ningxia Academy of Agriculture and Forestry Sciences, China
Copyright © 2026 Speek, Suleiman, Keuning, Sechi, Buisman and Bezemer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Brenda M. Speek, QnJlbmRhLlNwZWVrQHdldHN1cy5ubA==