The occurrence and biogeochemical cycling of quaternary, ternary and volatile amines in marine systems

Abstract

This review provides a critical assessment of knowledge regarding the occurrence and behaviour of volatile, low molecular weight amines, particularly methylamines and quaternary amines, in marine aquatic systems. It provides an up-to-date evaluation of their presence within marine ecosystems, the processes likely to control their flux across the sea-air interface, and analytical techniques associated with their measurement. Interest in the occurrence and cycling of these groups of compounds in seawater has increased within the last 10–15 years, due to their potential role in climate regulation. As such, the need for wider measurements and mechanistic studies to elucidate their role within biological communities and, more widely, the nitrogen cycle and marine ecosystem models, is apparent. Finally, we make recommendations on what research questions are most suitable for future studies in this area.

Introduction

Nitrogen (N) is ubiquitous in marine systems and an essential macro-nutrient for primary production. It exists in both inorganic and organic form, with oxidation states ranging from +5 (e.g. nitrate; NO₃^-) to -3 (e.g. ammonia; NH_3, glycine; CO₂HCH₂NH₂). Molecules in the dissolved organic N (DON) pool can be ionised or neutral (gaseous), which influences both their volatility, aqueous residence time and atmospheric flux.

Trace gases play critical roles in marine biogeochemical cycles, atmospheric chemistry and climate (Carpenter et al., 2012; Almeida et al., 2013; Riccobono et al., 2014). Phytoplankton synthesise organic compounds as osmolytes and cryoprotectants, including dimethylsulfoniopropionate and quaternary amines (QAs). The former has received attention as a precursor of the cloud-promoting gas, dimethylsulfide (DMS); however, amines may be equally important (Almeida et al., 2013; Riccobono et al., 2014; Tilgner et al., 2021; Hoffmann et al., 2024). For example, glycine betaine, a QA commonly termed “betaine” in early literature, is among the most widely-used compatible solutes in nature (Yancey et al., 1982). Nitrogen-containing osmolytes (N-osmolytes), such as glycine betaine, are produced by marine phytoplankton to maintain osmotic pressure (Yancey, 2005; Burg and Ferraris, 2008). These molecules can degrade to produce methylamines (Jameson et al., 2016a; King, 1984; Oremland et al., 1982; King, 1988; Oren, 1990), chemical analogues of ammonia with the molecular formula (CH₃)_nNH_3-n. Marine bacteria use MAs as a source of energy and remineralise the nitrogen to ammonium (Lidbury et al., 2015). The MAs are also required by bacteria for conversion of DMS to dimethylsulfoxide (Lidbury et al., 2016), firmly establishing them as important components in marine biogeochemical cycles.

In dissolved, gaseous form, MAs can diffuse across the sea-air interface to participate in climate-regulation processes (Figure 1). Indeed, atmospheric MA concentrations above 65 nmol m^-3 could account for observed atmospheric particle-formation rates (Almeida et al., 2013).

Figure 1

In this article, we review current knowledge on the occurrence, cycling and measurement of quaternary and ternary amines used as osmolytes, and volatile, low molecular weight amines (MAs and other amines whose presence has been reported). Their behaviour is evaluated with reference to molecular structure, physico-chemical properties, and identified microbial interventions and pathways. Finally, we propose how our understanding of the roles and significance of these compounds within the marine environment might be progressed.

Quaternary and ternary amines

Occurrence and role

Quaternary and ternary amines are used extensively by both phytoplankton and bacteria as osmoprotective compounds (osmolytes). Cells alter the cytoplasmic concentration of these compounds in response to changing salinity via synthesis and/or uptake (Sleator and Hill, 2002). Most quaternary amines are compatible solutes, meaning that they are highly soluble molecules which carry no net charge in vivo and do not interact with cellular proteins. As well as maintaining osmotic balance, compatible solutes have a stabilising effect on proteins, protecting against salinity, temperature changes and desiccation (Sleator and Hill, 2002). Glycine betaine (GBT) is a commonly-used osmolyte among both phytoplankton and bacteria; others include carnitine, trigonelline, homarine and the ternary amines proline and ectoine (Table 1).

Table 1

Compound	Molecular mass	Reported occurrence	Reference
Carnitine	161.20	Dinophyceae  Amphidinium carterae  Alexandrium tamarense  Heterocapsa triqueta  Lingulodinium polyhedra   Prymnesiophyceae  Chrysochromulina acantha  Chrysochromulina rotalis  Chrysochromulina simplex  Chrysochromulina parva  Emiliania huxleyi   Bacillariophyceae  Thalassiosira pseudonana  Thalassiosira oceanica  Phaeodactylum tricornutum  Navicula pelliculosa  Cyclotella mereghiniana  Pseudo-nitzschia pungens   Gammaproteobacteria (Gram -ve)  Shewanella pacifica  Pseudomonas sp.  Chromohalobacter salexigens   Alphaproteobacteria  Sulfitobacter  Thalassospira   Bacilli  Bacillus subtilis	Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022     Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022     Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022     Ivanova et al., 2004 Hung and Kleber, 1985; Monnich et al., 1995 Meng et al., 2022     Durham et al., 2022 Durham et al., 2022     Hoffmann et al., 2013
Choline	104.17	Dinophyceae  Amphidinium carterae  Alexandrium tamarense  Heterocapsa triqueta  Lingulodinium polyhedra   Prymnesiophyceae  Chrysochromulina rotalis  Chrysochromulina simplex  Emiliania huxleyi   Bacillariophyceae  Thalassiosira pseudonana  Thalassiosira oceanica  Phaeodactylum tricornutum  Navicula pelliculosa  Navicula cf. perminuta  Cyclotella mereghiniana  Pseudo-nitzschia pungens  Fragillariopsis cylindris  Nitzschia lecointei   Cyanophyceae  Crocosphaera watsonii   Gammaproteobacteria (Gram -ve)  Shewanella putrefaciens  Colwellia psychrerythraea  Vibrio coralliilyticus  Moritella yayanosii   Alphaproteobacteria  Sulfitobacter sp.  Roseovarius sp.  Ruegeria pomeroyi	Durham et al., 2022 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022     Durham et al., 2022 Durham et al., 2022 Durham et al., 2022     Durham et al., 2022; Dawson et al., 2020 Durham et al., 2022 Durham et al., 2022 Durham et al., 2022; Dawson et al., 2020 Dawson et al., 2020 Durham et al., 2022 Durham et al., 2022 Dawson et al., 2020 Dawson et al., 2020     Durham et al., 2022     Leblanc et al., 2001 Firth et al., 2016 Lichty et al., 2024 Zhang et al., 2021     Durham et al., 2022 Durham et al., 2022 Durham et al., 2022
Cysteinolic acid	155.17	Dinophyceae  Amphidinium carterae  Prorocentrum minimum Prymnesiophyceae  Emiliania huxleyi Bacillariophyceae  Thalassiosira pseudonana  Thalassiosira weissflogii  Skeletonema costatum Haptophyceae  Isochrysis galbana  Prymnesium parvum Alphaproteobacteria  Ruegeria pomeroyi	Fenizia et al., 2021 Fenizia et al., 2021   Fenizia et al., 2021   Fenizia et al., 2021 Fenizia et al., 2021 Fenizia et al., 2021   Fenizia et al., 2021 Fenizia et al., 2021   Durham et al., 2019; Smith et al., 2021; Roman et al., 2024
Ectoine	142.16	Dinophyceae  Amphidinium carterae  Prorocentrum minimum Prymnesiophyceae  Emiliania huxleyi Bacillariophyceae  Thalassiosira pseudonana  Thalassiosira weissflogii  Skeletonema costatum  Phaeodactylum tricornatum Haptophyceae  Isochrysis galbana  Prymnesium parvum Gammaproteobacteria (Gram -ve)  Chromohalobacter israelensis  Chromohalobacter salexigens  Halorhodospira halochloris  Halomonas elongate  Halomonas variabilis  Methylarcula marina  Methylarcula terricola  Methylophaga alcalica  Methylophaga natronic  Vibrio parahaemolyticus  Vibrio cholerae  Vibrio fischeri  Vibrio costociola	Fenizia et al., 2021 Fenizia et al., 2020, 2021   Fenizia et al., 2020, 2021   Fenizia et al., 2021 Fenizia et al., 2020, 2021 Fenizia et al., 2020, 2021 Fenizia et al., 2020   Fenizia et al., 2020, 2021 Fenizia et al., 2020, 2021   Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Roberts, 2005 Ongagna-Yhombi and Boyd, 2013 Pflughoeft et al., 2003; Roberts, 2005 Pflughoeft et al., 2003 Roberts, 2005
Glycine betaine	117.15	Dinophyceae  Amphidinium carterae  Prorocentrum minimum   Prymnesiophyceae  Chrysochromulina sp.  Emiliania huxleyi   Bacillariophyceae  Thalassiosira pseudonana    Thalassiosira weissflogii  Skeletonema costatum  Phaeodactylum tricornutum  Navicula cf. perminuta  Nitzschia lecointei  Fragilariopsis cylindrus  Cyclotella cryptica  Cyclotella mereghiniana   Haptophyceae  Isochrysis galbana  Prymnesium parvum  Pavlova lutheri Cryptophyceae  Cryptochloris sp.  Rhodomonas sp. Chlorodendrophyceae  Tetraselmis chui  Prasinocladus Porphyridiophyceae  Porphyridium aerugineum Gammaproteobacteria (Gram -ve)  Vibrio parahaemolyticus  Vibrio costicola  Pseudomonas sp.  Alteromonas sp.  Acinetobacter sp.  Escherichia coli  Thioalkalivibrio versutus  Halorhodospira halochloris  Ectothiorhodospira marismortui Betaproteobacteria (Gram -ve)  Chromobacterium maris-mortui Actinobacteria (Gram -ve)  Micrococcus halbius  Micrococcus sp.  Actinopolyspora sp. Bacilli  Bacillus subtilis  Staphylococcus epidermisis Methanomicrobia  Mathanohalophilus portucalensis  Methanosarcina thermophila Cyanophyceae  Synechococcus   Synechocystis  Spirulina  Calothrix  Phormidium  Gloeocapsa	Keller et al., 1999a, b Spielmeyer et al., 2011; Gebser and Pohnert., 2013; Fenizia et al., 2020, 2021   Keller et al., 1999a Keller et al., 1999a, b; Gebser and Pohnert., 2013; Fenizia et al., 2020, 2021   Keller et al., 1999b; Spielmeyer et al., 2011, 2012, Dawson et al., 2020 Fenizia et al., 2021 Spielmeyer et al., 2011; Fenizia et al., 2020, 2021 Fenizia et al., 2020 Dickson and Kirst, 1987a; Spielmeyer et al., 2011, 2012 Dawson et al., 2020 Dawson et al., 2020 Dawson et al., 2020 Dickson and Kirst, 1987a     Spielmeyer et al., 2011; Fenizia et al., 2020, 2021 Spielmeyer et al., 2011; Fenizia et al., 2020, 2021 Spielmeyer et al., 2011   Spielmeyer et al., 2011 Spielmeyer et al., 2011   Dickson and Kirst, 1987b Dickson and Kirst, 1987b   Dickson and Kirst, 1987a   Ongagna-Yhombi and Boyd, 2013 Imhoff and Rodriguez-Valera, 1984 Imhoff and Rodriguez-Valera, 1984 Imhoff and Rodriguez-Valera, 1984 Imhoff and Rodriguez-Valera, 1984 Imhoff and Rodriguez-Valera, 1984 Roberts, 2005 Roberts, 2005 Galinski and Oren, 1991   Imhoff and Rodriguez-Valera, 1984   Imhoff and Rodriguez-Valera, 1984 Imhoff and Rodriguez-Valera, 1984 Roberts, 2005   Imhoff and Rodriguez-Valera, 1984; Brill et al., 2011 Imhoff and Rodriguez-Valera, 1984 Hoffmann et al., 2013 Roberts, 2005 Roberts, 2005   Reed et al., 1986; Roberts, 2005; Mackay et al., 1984; Fulda et al., 1999 Reed et al., 1986 Reed et al., 1986 Reed et al., 1986 Reed et al., 1986 Mackay et al., 1984
Homarine	137.14	Dinophyceae  Amphidinium carterae  Prorocentrum minimum Prymnesiophyceae  Emiliania huxleyi Bacillariophyceae  Thalassiosira pseudonana  Thalassiosira weissflogii  Skeletonema costatum  Navicula cf. perminuta  Fragilariopsis cylindrus  Cyclotella crytica  Cyclotella mereghiniana Haptophyceae  Isochrysis galbana  Prymnesium parvum Chlorodendrophyceae  Tetraselmis chui  Prasinocladus	Keller et al., 1999a; Fenizia et al., 2021 Fenizia et al., 2021   Keller et al., 1999a; Gebser and Pohnert., 2013; Fenizia et al., 2021 Dawson et al., 2020; Fenizia et al., 2021 Fenizia et al., 2020, 2021 Fenizia et al., 2021 Dawson et al., 2020 Dawson et al., 2020 Dickson and Kirst, 1987a Dickson and Kirst, 1987a   Fenizia et al., 2021 Fenizia et al., 2021   Dickson and Kirst, 1987b Dickson and Kirst, 1987b
Proline	115.13	Bacillariophyceae  Phaeodactylum tricornutum  Thalassiosira pseudonana  Navicula pelliculosa  Navicula cf. perminuta  Nitzschia lecointei  Fragilariopsis cylindrus  Cyclotella cryptica  Cyclotella mereghiniana Campylobacteria  Sulfurimonas denitrificans Bacilli  Bacillus subtilis	Dickson and Kirst, 1987a Dawson et al., 2020 Dawson et al., 2020 Dawson et al., 2020 Dawson et al., 2020 Dawson et al., 2020 Dickson and Kirst, 1987a Dickson and Kirst, 1987a   Götz et al., 2018   Brill et al., 2011; Hoffmann et al., 2013
Trigonelline	137.17	Dinophyceae  Prorocentrum minimum Bacillariophyceae  Skeletonema costatum  Thalassiosira pseudonana Prasinophyceae  Tetraselmis sp. Prymnesiophyceae  Chrysochromulina sp.  Emiliania huxleyi	Gebser and Pohnert., 2013  Keller et al., 1999a Dawson et al., 2020   Keller et al., 1999a   Keller et al., 1999a Gebser and Pohnert., 2013
Trimethylamine N-oxide	75.11	Bacillariophyceae  Fragillariopsis cylindris Gammaproteobacteria (Gram -ve)  Shewanella massilia  Shewanella baltica  Photobacterium angustum  Vibrio alginolyticus  Vibrio fluvialis  Vibrio neocaledonicus  Marinobacter hydrocarbonoclasticus Alphaproteobacteria  Aminobacter aminovorans  Ruegeria pomeroyi	Dawson et al., 2020   Dos Santos et al., 1998 Debevere et al., 2001 Yin et al., 2019 Yin et al., 2019 Yin et al., 2019 Yin et al., 2019 Yin et al., 2019 Raymond and Plopper, 2002 Lidbury et al., 2014

Nitrogenous osmolyte (N-osmolyte) distributions in marine phytoplankton and bacteria.

Of the N-osmolytes listed in Table 1 and reported in the literature, GBT has received the most attention (Mäkelä et al., 2019). While the role of GBT as a compatible solute has been extensively reported, it may also be used for the biosynthesis of other N-osmolytes, including chloine, sarcosine and carnitine (Boysen et al., 2022). As such, most of the studies reported in this section focus on GBT but we note that information is needed on a wider range of N-osmolytes to fully appreciate the significance of N-osmolytes in marine ecosystems.

The accumulation of specific osmolytes by bacteria depends on the level of osmotic stress, and the availability of substrates and osmolytes in the environment (Burg and Ferraris, 2008). Over diel cycles in the North Pacific Ocean, osmolytes exhibited the largest diel oscillations of all the metabolites detected, implying rapid turnover and metabolic roles beyond cell turgor maintenance (Boysen et al., 2021). This underlines the importance of GBT and other N-osmolytes as currencies for microbes in terms of the exchange of carbon (C) and N. In fact, labelling studies demonstrated that N derived from GBT made its way through the marine microbial community (Boysen et al., 2022). Although some groups of bacteria can access GBT as a source of N, C or energy, most bacteria target this compound for osmotic functions – many bacteria can transport it but not synthesise or break it down (McParland et al., 2021). In natural bacterial communities, 88% of GBT transported into cells remained unmetabolised (Boysen et al., 2022). The ability to break down GBT is a highly specialised metabolic activity (McParland et al., 2021). For example, SAR11 has a high affinity transporter for GBT (Noell and Giovannoni, 2019) and uses GBT as a source of methyl groups to fuel the methionine cycle (Boysen et al., 2022). Also, GBT transporters are found frequently in marine bacterial genomes and its transcripts can be detected in metatranscriptomic datasets (McParland et al., 2021). This further supports the importance of the compound in osmotic function. There was, however, substantial remineralisation of GBT as a C substrate in the global ocean transcriptome (McParland et al., 2021). In a seasonal study, prokaryotic GBT uptake was influenced mainly by sea surface temperature, salinity and macronutrient concentrations (Mausz et al., 2022). The uptake of this compound provides an effective alternative nutrient source for prokaryotes in marine systems and might be more widespread than previously thought (Mausz et al., 2022). Members of the Rhodobacteraceae have been found to metabolise MAs and GBT, providing an ammonium source to diatoms in co-culture (Zecher et al., 2020). This is proposed to occur in the phycosphere in the natural environment, demonstrating a nutritional benefit for diatoms to exude organic nitrogen compounds into the phycosphere (Zecher et al., 2020).

In a study of sinking particles across the South Atlantic Ocean, the metabolite profile was found to be dominated by GBT (Johnson et al., 2020). GBT also contributed a larger mole fraction in sinking material compared to surface material across several oceanic regions, indicating a widespread feature not linked to oceanographic location (Johnson et al., 2020). The high proportion of GBT was attributed to particle-associated microbial communities on the sinking particulates. Proline was also more dominant in sinking particles, suggesting both GBT and proline are important osmolytes at depth (Johnson et al., 2020).

GBT is also abundant in coral tissue, comprising 16% of coral tissue N (Hill, 2022). Corals have pathways for de novo synthesis as well as transport of GBT. It is proposed that GBT may be protective in warm water for reef-building corals, providing photoprotection from photon stress in these organisms, similar to descriptions for terrestrial plants (Hill, 2022).

Within phytoplankton, culture studies reveal that GBT production is relatively common, with GBT detected in 75% of the cultures analysed (Spielmeyer et al., 2011), though at lower concentrations than DMSP. GBT concentrations in phytoplankton have been found to depend strongly on growth conditions, including growth phase and nutrient limitation (Keller et al., 1999a; Keller et al., 1999b; Keller et al., 2004). In diatoms and a strain of the coccolithophore, Emiliania huxleyi, GBT production increased with both temperature and carbon dioxide levels (Spielmeyer and Pohnert, 2012). During a seasonal study in coastal temperate waters, GBT correlated with specific members of the dinoflagellate community in summer (Airs et al., 2023). Moreover a modelling study indicated GBT positively affects dinoflagellate fitness (Airs et al., 2023). The high cellular content of QA derivatives, such as GBT, has been shown to positively affect the buoyancy of marine phytoplankton (Boyd and Gradmann, 2002), indicating important roles beyond osmolarity. GBT is important for protection of drought, temperature and salt stress in higher plants (Sakamoto and Murata, 2002; Wang et al., 2010; Chen and Murata, 2011; Fan et al., 2012; Rivero et al., 2014). GBT has also been reported to stabilise antioxidant enzymes that can scavenge reactive oxygen species in plants (Liang et al., 2009), stabilise photosystem II (Papageorgiou and Murata, 1995; Huang et al., 2020) and accelerate the recovery of photosystem II in higher plants from heat stress (Li et al., 2014) or high light exposure (Kondo et al., 1999; Prasad and Saradhi, 2004) providing evidence of a photoprotective role for GBT (Wang et al., 2014; Li et al., 2021).

Analytical methods

Methods applied to the analysis of N-osmolytes have moved from stand-alone chromatography techniques, including thin layer chromatography (Storey and Wyn Jones, 1977; Dickson and Kirst, 1986) and high performance liquid chromatography, HPLC (Gorham, 1984), to hyphenated techniques utilising mass spectrometry, MS (Koc et al., 2002; Holm et al., 2003; Oufir et al., 2009; Airs and Archer, 2010; Spielmeyer et al., 2011; Beale and Airs, 2016; Ares et al., 2020). HPLC analysis typically comprised a cation exchange column and UV detection at a wavelength of 195 nm. The method required filtration of relatively large volumes of water (1-4 L) and was applied to measurements of phytoplankton cultures (Keller et al., 1999a; Keller et al., 1999b) and natural samples off the Gulf of Maine (Keller et al., 2004). The application of hyphenated LC-MS approaches yielded improvements in sensitivity (Airs and Archer, 2010; Beale and Airs, 2016), enabling smaller sample volumes. The LC-MS technique has been applied to QA analysis in coastal seawater (Airs and Archer, 2010; Beale and Airs, 2016), Atlantic Ocean (Airs and Archer, 2010) and Southern Ocean samples (Dall’Osto et al., 2017). Within the limited environmental sample sets analysed to date, osmolyte concentrations were highest in coastal systems (Keller et al., 2004; Airs and Archer, 2010; Airs et al., 2023), and Antarctic water influenced by sea ice (Dall’Osto et al., 2017). Osmolytes are particularly amenable to metabolomics methods, being among the most ubiquitous and abundant metabolites detected (Boysen et al., 2021; Johnson et al., 2020). This typically involves the filtration of large sample volumes, which is likely to be detrimental to accurate concentration measurements of osmolytes (Kiene and Slezak, 2006), but is very valuable for comparative studies of a wide range of metabolites (Boysen et al., 2021; Johnson et al., 2020). Absolute quantification is possible but requires addition of quantification standards for each compound to be quantified (Boysen et al., 2021). Normalisation techniques have been developed to optimise the use of internal standards for rectifying obscuring variation (the combined effect on peak areas of sample-matrix-induced ion suppression, injection volume, chromatographic quality and analytical drift) during analysis (Boysen et al., 2018).

While analysis of particulate-associated N-osmolytes has been possible for some time, methodology to determine dissolved concentrations of N-osmolytes in marine systems, together with other dissolved metabolites, has only recently been achieved via a cation exchange solid phase extraction method (Sacks et al., 2022). Sacks et al. (2022) achieved a limit of detection for dissolved GBT of 0.38 nM and reported concentrations of 2.5-5.2 nM in 3 marine samples. Mausz et al. (2022) applied an uptake kinetics approach of diluted and undiluted samples (Wright and Hobbie, 1966) to estimate the dissolved concentrations of GBT and choline in coastal seawater and determined them to be in the low nanomolar range (Mausz et al., 2022).

Volatile amines

Occurrence and role

Small volatile amines are nitrogen-containing molecules with the general formula R_nNH_(3-n); they are alkylated analogies of ammonia and N is in the -3 oxidation state. In seawater, the most reported low molecular weight amines are the methylamines (MAs), which exist as primary (monomethylamine; MMA), secondary (dimethylamine; DMA) and tertiary (trimethylamine; TMA) species (Abdul-Rashid et al., 1991; Gibb et al., 1999a; Gibb et al., 1999b; Gibb and Hatton, 2004; Dall’Osto et al., 2017; Cree et al., 2018; Dall’Osto et al., 2019). The MAs are highly soluble in water. At seawater pH they are predominantly protonated (cations), though in equilibrium with their neutral, gaseous forms. Table 2 shows physico-chemical characteristics of the MAs.

The MAs have been detected at micromolar levels in estuarine environments. In cation form they can sorb to particles and fractionate between sediment porewaters and particles (Wang and Lee, 1990; Wang and Lee, 1993; Fitzsimons et al., 2005; Fitzsimons et al., 2006). The sorptive interactions between the MA and a particle surface are identical to those reported for NH₃. An ionic bond can form between the cation and a negatively-charged surface group on the particle, while the neutral species can react with a carbonyl functional group (carbonyl addition) to form a covalent bond - this is not possible for TMA or QAs as the molecule must contain at least one N-H bond. Ionic bonding should be the major sorption pathway for MAs, given the predominance of the protonated form at seawater pH. However, carbonyl addition may occur, and has been proposed for amino acids (which contain a primary amino function group), analogous to melaniodin-type reactions (Henrichs and Sugai, 1993).

The sorption of MAs to particulates is reversible. For example, Wang and Lee (1993) compared adsorption and desorption coefficients for the MAs using ¹⁴C-MAs on an inter-tidal sediment, and found that 63-90% of the label was desorbed, with the extent of desorption corresponding to the number of methyl substituents (MMA < DMA < TMA). A study on the influence of sediment resuspension on estuarine water column concentrations of MAs revealed that particulate release accounted for > 90% of the dissolved MA increase measured over a tidal cycle (Fitzsimons et al., 2006).

Wang and Lee (1990) reported seasonal control on the concentrations of MAs in inter-tidal sediments, where an increase corresponded with annual senescence of salt marsh grasses. While increasing the land-air flux of MAs, this process also provides non-competitive substrates for methanogenic bacteria (King, 1984) and allows them to co-exist with sulphate-reducing bacteria that outcompete them for more energetically favourable molecules, such as acetate. As concentrations of the MAs are thought to represent under 1% of total sedimentary N (Burdige et al., 1995; Lee and Olsen, 1984), it was suggested that this N-fraction has limited environmental significance (Burdige et al., 1995). However, as interest grows in their potential influence on climate (Almeida et al., 2013), quantification of the MA flux from sediments, particularly inter-tidal sediments, will be an important part of elucidating their role in atmospheric processes.

Concentrations of volatile amines have been measured in both coastal and oceanic waters (e.g. Gibb et al., 1999a; Gibb and Hatton, 2004; Cree et al., 2018). In addition, concurrent water and air concentrations have been reported from a number of studies (Gibb et al., 1999b; Dall’Osto et al., 2017; Dall’Osto et al., 2019; Van Pinxteren et al., 2019); these are summarised in Table 3. Concentrations of MAs of up to 38 nM were measured in seawater by Gibb et al. (1995), though the most abundant MAs measured varied between studies. For example, MMA was the most abundant MA measured in the Mediterranean (Gibb et al., 1995) and Arabian Seas (Gibb et al., 1999a), while TMA was most abundant in samples measured in the English Channel and the Southern Ocean (Cree et al., 2018), where MMA was not detected. Higher MA concentrations were measured in samples from the Sea Surface Microlayer (up to 50 nM) but this study did not include analysis of TMA (Van Pinxteren et al., 2019).

The concurrent detection of MAs in seawater and atmospheric samples has suggested an oceanic source for these analytes (Gibb et al., 1999a; Gibb et al., 1999b; Dall’Osto et al., 2017; Dall’Osto et al., 2019). Although Facchini et al. (2008) did not measure amine concentrations in waters of the North Atlantic, concentrations of DMA and diethylamine (DEA) in marine aerosol were highest during periods of increased biological activity. Interestingly, while Van Pinxteren et al. (2019) associated highest MA concentrations with biological activity through correlation with chlorophyll-a and fucoxanthin, a diatom pigment, flux calculations suggested that seawater may be a sink for DMA. While the production of MAs in the water column can be linked to the degradation of quaternary amines, such as GBT, trimethylamine oxide and choline (Lidbury et al., 2015), precursors for other detected amines, namely mono-, di- and triethylamine do not have obvious sources, via C-N bond cleavage, from within the marine organic nitrogen pool.

Figure 2 shows a range of MA concentrations reported for porewaters and seawater, and the atmospheric concentrations estimated, assuming sea-air exchange based on Henry’s Law (Leng et al., 2015; Dall’Osto et al., 2019). TMA was used as the representative MA for these calculations with its physical constants applied. Although the maximum values calculated are higher than reported atmospheric concentrations (Table 3) there is substantial overlap.

Figure 2

Analytical methods

Given their low concentrations in marine samples, analytical methods employed for volatile amine analysis have typically employed a pre-concentration step. This step aims to both bring the compounds within the sensitivity of the instrument used for separation and detection and remove them from a complex sample matrix in advance of instrumental measurement. An early method employed microdiffusion of 50 mL seawater samples in an adapted Quikfit flask, adjusted to pH > 12, where the amines diffused into the flask headspace under heating over 24 hours, and were then captured in a small volume of dilute hydrochloric acid (Abdul-Rashid et al., 1991). While this method was applied to estuarine sediments and inshore waters, the small sample volume precluded measurements of oceanic samples with the lowest amine concentrations. Flow injection has been coupled with chromatography to achieve in-line pre-concentration of samples in several oceanic studies (Gibb et al., 1999a; Gibb et al., 1999b; Gibb and Hatton, 2004), where both seawater and atmospheric measurements were reported. Circulation diffusion was coupled with gas chromatography to measure amines in porewater and seawater (Yang et al., 1993). This method could detect amines in seawater down to 3 nM but required a sample volume of 1 L to measure the lowest concentrations, while a 0.5 L sample was sufficient for porewater samples.

Solid phase microextraction (SPME) coupled with gas chromatography (optimised for nitrogen molecules) has been recently used for analysis of seawater samples and has achieved limits of detection as low as any previously reported (Cree et al., 2018), enabling measurement of amines in water samples from the Southern Ocean (Dall’Osto et al., 2017; Dall’Osto et al., 2019). Limitations of this technique are the large sample volume required, and the time needed to extract each sample (1 L and 2.5 h, respectively). While the water samples are preserved after filtration (Cree et al., 2018), sample analysis and storage are limited with such large seawater volumes so installation of the gas chromatograph on board ship has been necessary for oceanic studies. Akenga and Fitzsimons (2024) developed an automated, in-line, preconcentration and sample injection procedure. The analytical method also employed SPME but with separate sample equilibration and extraction steps, which enabled them to achieve limits of detection for seawater samples that were close to those of Cree et al. (2018) while sample volumes (10 mL) were 100 x lower. This advance offers a systematic and standardized method for MA analysis in seawater and can significantly advance understanding of their abundance and role in marine systems.

The studies included in Table 3 show which MAs (and other volatile amines) were measured, the methodology employed, and which was most abundant. The number of analytes potentially detected was dependent on the method used (e.g. derivatization of analytes excludes TMA). Although each dataset of measurements is of considerable value, the low number of studies and the application of different analytical methods makes it difficult to compare data (Fitzsimons et al., 2023). Nonetheless, it is encouraging to see that the methods reported have been suitable for the measurement of MAs at the low concentrations expected for oceanic waters, and that the concentration ranges for water column measurements are broadly similar.

Synthesis and degradation of MAs and QAs

It is not completely understood how MAs can be formed in oxygenated marine waters. The fact that their concentration in marine sediments is at least one order of magnitude higher than in marine water columns suggests that MAs likely originate from anoxic marine sediment through microbial transformation of DOM. It is likely that TMA is the key molecule bridging the QA degradation cycle to the formation of MAs in oceanic waters through microbe-dependent and -independent pathways (see below).

There are at least four independent microbial pathways bridging the marine QA cycle to TMA formation: 1) bacterial degradation of choline to TMA via a glycyl radical containing choline-TMA lyase (Craciun and Balskus, 2012; Jameson et al., 2016b; Jameson et al., 2018); 2) degradation of GBT to TMA using a GBT reductase (Meyer et al., 1995); 3) reduction of TMAO to TMA through TMAO reductase (Barrett and Kwan, 1985) and 4) TMA formation from carnitine using a Rieske-containing carnitine oxygenase aerobically (Zhu et al., 2014) or through a coenzyme A (Co-A) dependent anaerobic pathway (Rajakovich et al., 2021). The first three pathways and Co-A dependent carnitine degradation are found in strict or facultative anaerobes. The carnitine oxygenase pathway was first characterized in aerobic human gut microbiota, and it remains to be established whether marine bacteria can indeed transform carnitine to TMA using this enzyme.

It is important to note that TMA may also be formed in the oxygenated marine water column independent of microbial transformation. A previous study has noted that betaine-containing lipids (e.g. diacylglyceryl trimethyl-β-alanine, DGTA) can spontaneously degrade to TMA. These non-phosphorus containing lipids are abundant in marine phytoplankton and may therefore represent an important source of oceanic TMA that has been overlooked (Vogel et al., 1990; Dembitsky, 1996).

The transformation of TMA to other MAs in the marine environment has also been studied over the past decade. TMA can be oxidised to DMA via either TMA dehydrogenase (Burgess et al., 2008) or through TMAO as the intermediate (Chen et al., 2011; Lidbury et al., 2014). Similarly, DMA oxidation to MMA can be catalysed by either a DMA dehydrogenase (Yang et al., 1995) or a DMA monooxygenase (Lidbury et al., 2017). MMA is further degraded to ammonium and CO₂ through MMA dehydrogenase or a multi-step enzyme system involving two methylated amino acids as key intermediates (reviewed in Mausz and Chen, 2019). In the marine water column, MAs appear to serve as important C, N and energy sources for cosmopolitan marine microbes, particularly Alphaproteobacteria of the marine Roseobacter clade and the SAR11 clade (Chen et al., 2011; Sun et al., 2011; Lidbury et al., 2014; Lidbury et al., 2015; Lidbury et al., 2017).

The way forward

Interest in the occurrence and cycling of low molecular weight volatile amines and their precursor N-osmolytes in marine systems has increased considerably, with the former linked to processes influencing climate regulation. However, relatively little is known about the absolute concentrations of QAs and MAs in the global ocean compared to other biogeochemically relevant compounds, and this data is a key requirement for their future inclusion within marine models. While several analytical methods have been successfully applied to their determination, standardisation of methodology or inter-laboratory comparison studies would optimise confidence in datasets produced, through increased understanding of analytical variation and biases that can be incorporated into data interpretation. Small sample volume methods (50 mL) have been developed for measurement of QAs (Beale and Airs, 2016) and volatile amines (Akenga and Fitzsimons, 2024) in seawater, and these analytical advances can facilitate uncomplicated collection and preservation of samples throughout the world ocean for measurement of standing stocks and through dynamic periods of biological productivity. This will make a major contribution to the development of a substantial global database on their seawater concentrations, and can form the basis of models to quantify their significance within marine ecosystems.

Knowledge of metabolic pathways around the production and catabolism of these nitrogenous compounds is more advanced, but there remain significant gaps. For example, a convincing source of TMA in surface waters independent of anaerobic pathways has not been put forward. Given their widespread occurrence and utilisation by microbes, these low molecular weight compounds are emerging as a crucial underpinning currency in microbial food webs. As such, combined studies addressing biogeochemistry, analytical chemistry, transcriptomics and labelling studies are required to fully address research questions around these molecules.

The importance of QAs and MAs to marine biogeochemistry is further emphasised by the coupling of the nitrogen and sulphur cycles via their reliance on MAs for the oxidation of DMS to DMSO via the enzyme Tmm, and the use of the same enzyme for the oxidation of TMA to trimethylamine oxide (TMAO). The full ramifications of these intriguing links are yet to be established. Like DMSP and MAs, GBT can be a substrate for methanogens, providing important links to biological methane production.

Finally, metabolomics studies are really valuable for providing context across a wide range of marine metabolites (Durham et al., 2022). They can also provide focus for more targeted studies to better understand important processes, such as diel fluctuations of osmolytes and osmolyte use with depth.

References

• 1

  Abdul-Rashid M. K. Riley J. P. Fitzsimons M. F. Wolff G. A. (1991). Determination of volatile amines in sediment and water samples. Anal. Chim. Acta252, 223–226. doi: 10.1016/0003-2670(91)87219-W

  • CrossRef
  • Google Scholar

• 2

  Airs R. Archer S. (2010). Analysis of glycine betaine and choline in seawater particulates by liquid chromatography/electrospray ionization/mass spectrometry. Limnol. Oceanogr. Meth.8, 499–506. doi: 10.4319/lom.2010.8.499

  • CrossRef
  • Google Scholar

• 3

  Airs R. L. Beale R. Polimene L. Chen Y. Mausz M. A. Scanlan D. J. et al . (2023). Seasonal measurements of the nitrogenous osmolyte glycine betaine in marine temperate coastal waters. Biogeochemistry162, 309–323. doi: 10.1007/s10533-022-01006-7

  • CrossRef
  • Google Scholar

• 4

  Akenga P. C. Fitzsimons M. F. (2024). Automated method for the sensitive analysis of volatile amines in seawater. ACS ES&T Water4, 2504–2510. doi: 10.1021/acsestwater.4c00007

  • CrossRef
  • Google Scholar

• 5

  Almeida J. Schobesberger S. Kurten A. Ortega I. K. Kupiainen-Maatta O. Praplan A. P. . (2013). Molecular understanding of sulphuric acid-amine particle nucleation in the atmosphere. Nature502, 359–363. doi: 10.1038/nature12663

  • CrossRef
  • Google Scholar

• 6

  Ares A. M. Toribio L. Nozal M. J. Martín M. T. Bernal J. (2020). Simultaneous determination of betaines and other quaternary ammonium related compounds in bee pollen by hydrophilic interaction liquid chromatography-mass spectrometry. Microchem. J.157, 105000. doi: 10.1016/j.microc.2020.105000

  • CrossRef
  • Google Scholar

• 7

  Barrett E. L. Kwan H. S. (1985). Bacterial reduction of trimethylamine oxide. Annu. Rev. Microbiol.39, 131–149. doi: 10.1146/annurev.mi.39.100185.001023

  • CrossRef
  • Google Scholar

• 8

  Beale R. Airs R. (2016). Quantification of glycine betaine, choline and trimethylamine N-oxide in seawater particulates: Minimisation of seawater associated ion suppression. Anal. Chim. Acta938, 114–122. doi: 10.1016/j.aca.2016.07.016

  • CrossRef
  • Google Scholar

• 9

  Boyd C. Gradmann D. (2002). Impact of osmolytes on buoyancy of marine phytoplankton. Mar. Biol.141, 605–618. doi: 10.1007/s00227-002-0872-z

  • CrossRef
  • Google Scholar

• 10

  Boysen A. K. Carlson L. T. Durham B. P. Groussman R. D. Aylward F. O. Ribalet F. et al . (2021). Particulate metabolites and transcripts reflect diel oscillations of microbial activity in the surface ocean. mSystems6, e00896–e00820. doi: 10.1128/mSystems.00896-20

  • CrossRef
  • Google Scholar

• 11

  Boysen A. K. Durham B. P. Kumler W. Key R. S. Heal K. R. Carlson L. T. et al . (2022). Glycine Betaine uptake and metabolism in marine microbial communities. Environ. Microbiol.24, 2380–2240. doi: 10.1111/1462-2920.16020

  • CrossRef
  • Google Scholar

• 12

  Boysen A. K. Heal K. R. Carlson L. T. Ingalls A. E. (2018). Best-matched internal standard normalization in liquid chromatography-mass spectrometry metabolomics applied to environmental samples. Anal. Chem.90, 1363–1369. doi: 10.1021/acs.analchem.7b04400

  • CrossRef
  • Google Scholar

• 13

  Brill J. Hoffmann T. Bleisteiner M. Bremer E. (2011). Osmotically controlled synthesis of the compatible solute proline is critical for cellular defense of Bacillus subtilis against high osmolarity. J. Bacteriol.193, 5335–5346. doi: 10.1128/JB.05490-11

  • CrossRef
  • Google Scholar

• 14

  Burdige D. J. Huang C. M. Krishna N. Scully F. E. (1995). Aliphatic amines in chesapeake bay sediments. Mar. Chem.51, 45–54. doi: 10.1016/0304-4203(95)00042-P

  • CrossRef
  • Google Scholar

• 15

  Burg M. B. Ferraris J. D. (2008). Intracellular organic osmolytes: function and regulation. J. Biol. Chem.283, 7309–7313. doi: 10.1074/jbc.R700042200

  • CrossRef
  • Google Scholar

• 16

  Burgess S. G. Messiha H. L. Katona G. Rigby S. E. J. Leys D. Scrutton N. S. (2008). Probing the dynamic interface between trimethylamine dehydrogenase (TMADH) and electron transferring flavoprotein (ETF) in the TMADH–2ETF complex: role of the Arg-α237 (ETF) and Tyr-442 (TMADH) residue pair. Biochemistry47, 5168–5181. doi: 10.1021/bi800127d

  • CrossRef
  • Google Scholar

• 17

  Carpenter L. J. Archer S. D. Beale R. (2012). Ocean-atmosphere trace gas exchange. Chem. Soc Rev.41, 6473–6506. doi: 10.1039/c2cs35121h

  • CrossRef
  • Google Scholar

• 18

  Chen T. H. H. Murata N. (2011). Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ.34, 1–20. doi: 10.1111/j.1365-3040.2010.02232.x

  • CrossRef
  • Google Scholar

• 19

  Chen Y. Patel N. A. Crombie A. Scrivens J. H. Murrell J. C. (2011). Bacterial flavin-containing monooxygenase is trimethylamine monooxygenase. Proc. Natl. Acad. Sci. U.S.A.108, 17791–17796. doi: 10.1073/pnas.1112928108

  • CrossRef
  • Google Scholar

• 20

  Craciun S. Balskus E. P. (2012). Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. Proc. Natl. Acad. Sci. U.S.A.109, 21307–21312. doi: 10.1073/pnas.1215689109

  • CrossRef
  • Google Scholar

• 21

  Cree C. Airs R. Archer S. D. Fitzsimons M. F. (2018). Measurement of methylamines in seawater using solid phase microextraction and gas chromatography. Limnol. Oceanogr. Meth.16, 411–420. doi: 10.1002/lom3.10255

  • CrossRef
  • Google Scholar

• 22

  Dall’Osto M. Airs R. L. Beale R. Cree C. Fitzsimons M. F. Beddows D. et al . (2019). Simultaneous detection of alkylamines in the surface ocean and atmosphere of the antarctic sympagic environment. ACS Earth Space Chem.3, 854–862. doi: 10.1021/acsearthspacechem.9b00028

  • CrossRef
  • Google Scholar

• 23

  Dall’Osto M. Ovadnevaite J. Paglione M. Beddows D. C. S. Ceburnis D. Cree C. . (2017). Antarctic sea ice region as a source of biogenic organic nitrogen in aerosols. Sci. Rep.7, 6047. doi: 10.1038/s41598-017-06188-x

  • CrossRef
  • Google Scholar

• 24

  Dawson H. M. Heal K. R. Torstensson A. Carlson L. T. Ingalls A. E. Young J. (2020). Large diversity in nitrogen- and sulfur-containing compatible solute profiles in polar and temperate diatoms. N. Integr. Comparat. Biol.60, 1401–1413. doi: 10.1093/icb/icaa133

  • CrossRef
  • Google Scholar

• 25

  Debevere J. Devlieghere F. Van Sprundel P. De Meulenaer B. (2001). Influence of acetate and CO2 on the TMAO-reduction reaction by Shewanella baltica Int. J. Food Microbiol.68, 115–123. doi: 10.1016/S0168-1605(01)00484-6

  • CrossRef
  • Google Scholar

• 26

  Dembitsky V. M. (1996). Betaine ether-linked glycerolipids: Chemistry and biology. Prog. Lipid Res.35, 1–51. doi: 10.1016/0163-7827(95)00009-7

  • CrossRef
  • Google Scholar

• 27

  Dickson D. M. J. Kirst G. O. (1986). The role of ß-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta167, 536–543. doi: 10.1007/BF00391230

  • CrossRef
  • Google Scholar

• 28

  Dickson D. M. J. Kirst G. O. (1987a). Osmotic adjustment in marine eukaryotic algae—the role of inorganic-ions, quarternary ammonium, tertiary sulfonium and carbohydrate solutes. 1. Diatoms and a rhodophyte. New Phytol.106, 645–655. doi: 10.1111/j.1469-8137.1987.tb00165.x

  • CrossRef
  • Google Scholar

• 29

  Dickson D. M. J. Kirst G. O. (1987b). Osmotic adjustment in marine eukaryotic algae-the role of inorganic-ions, quarternary ammonium, tertiary sulfonium and carbohydrate solutes. 2. Prasinophytes and haptophytes. New Phytol.106, 657–666. doi: 10.1111/j.1469-8137.1987.tb00166.x

  • CrossRef
  • Google Scholar

• 30

  Dos Santos J. Iobbi-Nivol C. Couillault C. Giordano G. Méjean V. (1998). Molecular analysis of the trimethylamine N -oxide (TMAO) reductase respiratory system from a Shewanella species. J. Mol. Biol.284, 421–433. doi: 10.1006/jmbi.1998.2155

  • CrossRef
  • Google Scholar

• 31

  Durham B. P. Boysen A. K. Carlson L. T. Groussman R. D. Heal K. R. Cain K. R. et al . (2019). Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat. Microbiol.4, 1706–1715. doi: 10.1038/s41564-019-0507-5

  • CrossRef
  • Google Scholar

• 32

  Durham B. P. Boysen A. K. Heal K. Carlson L. T. Boccamazzo R. Deodato C. R. et al . (2022). Chemotaxonomic patterns in intracellular metabolites of marine microbial plankton. Front. Mar. Sci.9. doi: 10.3389/fmars.2022.864796

  • CrossRef
  • Google Scholar

• 33

  Facchini M. C. Decesari S. Rinaldi M. Carbone C. Finessi E. Mircea M. et al . (2008). Important source of marine secondary organic aerosol from biogenic amines. D. Environ. Sci. Technol.42, 9116–9121. doi: 10.1021/es8018385

  • CrossRef
  • Google Scholar

• 34

  Fan W. Zhang M. Zhang H. Zhang P. (2012). Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PloS One7, e37344. doi: 10.1371/journal.pone.0037344

  • CrossRef
  • Google Scholar

• 35

  Fenizia S. Thume K. Wirgenings M. Pohnert G. (2020). Ectoine from bacterial and algal origin is a compatible solute in microalgae. Mar. Drugs18, 42. doi: 10.3390/md18010042

  • CrossRef
  • Google Scholar

• 36

  Fenizia S. Weissflog J. Pohnert G. (2021). Cysteinolic acid is a widely distributed compatible solute of marine microalgae. Mar. Drugs19, 683. doi: 10.3390/md19120683

  • CrossRef
  • Google Scholar

• 37

  Fessenden R. J. Fessenden J. S. (1994). Organic chemistry. Fifth Edition (Pacific Grove. CA, USA: Brooks Cole), 1122.

  • Google Scholar

• 38

  Firth E. Carpenter S. D. Sørensen H. L. Collins R. E. Deming J. W. (2016). Bacterial use of choline to tolerate salinity shifts in sea-ice brines. Elementa: Sci. Anthropocene4, 120. doi: 10.12952/journal.elementa.000120

  • CrossRef
  • Google Scholar

• 39

  Fitzsimons M. F. Dawit M. Revitt D. M. Rocha C. (2005). Effects of early tidal inundation on the cycling of methylamines in inter-tidal sediments. Mar. Ecol. Prog. Ser.294, 51–61. doi: 10.3354/meps294051

  • CrossRef
  • Google Scholar

• 40

  Fitzsimons M. F. Millward G. E. Revitt D. M. Dawit M. D. (2006). Desorption kinetics of ammonium and methylamines from estuarine sediments: Consequences for the cycling of nitrogen. Mar. Chem.101, 12–26. doi: 10.1016/j.marchem.2005.12.006

  • CrossRef
  • Google Scholar

• 41

  Fitzsimons M. F. Tilley M. Cree C. H. L. (2023). The determination of volatile amines in aquatic marine systems : A review. Anal. Chim. Acta1241, 340707. doi: 10.1016/j.aca.2022.340707

  • CrossRef
  • Google Scholar

• 42

  Fulda S. Huckauf J. Schoor A. Hagemann M. (1999). Analysis of stress responses in the cyanobacterial strains Synechococcus sp. PCC 7942, Synechocystis sp. PCC 6803, and Synechococcus sp. PCC 7418: osmolyte accumulation and stress protein synthesis. J. Plant Physiol.154, 240–249. doi: 10.1016/S0176-1617(99)80215-6

  • CrossRef
  • Google Scholar

• 43

  Galinski E. A. Oren A. (1991). Isolation and structure determination of a novel compatible solute from the moderately halophilic purple sulfur bacterium Ectothiorhodospira marismortui. Eur. J. Biochem.198, 593–598. doi: 10.1111/j.1432-1033.1991.tb16055.x

  • CrossRef
  • Google Scholar

• 44

  Gebser B. Pohnert. G. (2013). Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs11, 2168–2182. doi: 10.3390/md11062168

  • CrossRef
  • Google Scholar

• 45

  Gibb S. W. Hatton A. D. (2004). The occurrence and distribution of trimethylamine-N oxide in Antarctic coastal waters. Mar. Chem.91, 65–75. doi: 10.1016/j.marchem.2004.04.005

  • CrossRef
  • Google Scholar

• 46

  Gibb S. W. Mantoura R. F. C. Liss P. S. (1995). Analysis of ammonia and methylamines in natural waters by flow injection gas diffusion coupled to ion chromatography, anal. Chim. Acta316, 291–304.

  • Google Scholar

• 47

  Gibb S. W. Mantoura R. F. C. Liss P. S. Barlow R. G. (1999a). Distributions and biogeochemistries of methylamines and ammonium in the Arabian Sea. Deep Sea Res. Part II Top. Stud. Oceanogr.46, 593–615. doi: 10.1016/S0967-0645(98)00119-2

  • CrossRef
  • Google Scholar

• 48

  Gibb S. W. Mantoura R. F. C. Liss P. S. Barlow R. G. (1999b). Ocean-atmosphere exchange and atmospheric speciation of ammonia and methylamines in the region of the NW Arabian Sea. Global Biogeochem. Cy.13, 161–177. doi: 10.1029/98GB00743

  • CrossRef
  • Google Scholar

• 49

  Gorham J. (1984). Separation of plant betaines and their sulphur analogues by cation exchange high performance liquid chromatography. J. Chromatogr.287, 345–351. doi: 10.1016/S0021-9673(01)87710-4

  • CrossRef
  • Google Scholar

• 50

  Götz F. Longnecker K. Soule M. C. K. Becker K. W. McNichol J. Kujawinski E. B. et al . (2018). Targeted metabolomics reveals proline as a major osmolyte in the chemolithoautotroph Sulfurimonas denitrificans. Microbiol. Open7, e00586. doi: 10.1002/mbo3.586

  • CrossRef
  • Google Scholar

• 51

  Grönberg' L. Lövkvist P. Jönsson J. (1992). Measurement of aliphatic amines in ambient air and rainwater. Chemosphere24, 1533–1540.

  • Google Scholar

• 52

  Henrichs S. M. Sugai S. F. (1993). Adsorption of amino-acids and glucose by sediments of Resurrection Bay, Alaska, USA – functional-group effects. Geochim. Cosmochim. Acta57, 823–835. doi: 10.1016/0016-7037(93)90171-R

  • CrossRef
  • Google Scholar

• 53

  Hill R. W. (2022). Quarternary ammonium compounds as candidate photoprotective compounds in reef-building compounds. Front. Mar. Sci.9. doi: 10.3389/fmars.2022.869739

  • CrossRef
  • Google Scholar

• 54

  Hoffmann E. H. Tilgner A. Herrmann H. (2024). An improved multiphase chemistry mechanism for methylamines: significant dimethylamine cloud production. NPJ Clim. Atmos. Sci.7, 119. doi: 10.1038/s41612-024-00665-7

  • CrossRef
  • Google Scholar

• 55

  Hoffmann T. Wensing A. Brosius M. Steil L. Völker U. Bremer E. (2013). Osmotic control of opuA expression in Bacillus subtilis and its modulation in response to intracellular glycine betaine and proline pools. J. Bacteriol.195, 510–522. doi: 10.1128/JB.01505-12

  • CrossRef
  • Google Scholar

• 56

  Holm P. I. Ueland P. M. Kvalheim G. Lien E. A. (2003). Determination of choline, betaine and dimethylglycine in plasma by a high-throughput method based on normal phase chromatography-tandem mass spectrometry. Clin. Chem.49, 286–294. doi: 10.1373/49.2.286

  • CrossRef
  • Google Scholar

• 57

  Huang S. Zuo T. Ni W. (2020). Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses. Planta251, 36. doi: 10.1007/s00425-019-0330-z

  • CrossRef
  • Google Scholar

• 58

  Hung K. Kleber H. P. (1985). Occurrence and regulation of carnitine dehydrogenase of Pseudomonas species. Wiss Z KarlMarx-Univ Leipzig Math-Nat R34, 293–296.

  • Google Scholar

• 59

  Imhoff J. F. Rodriguez-Valera F. (1984). Betaine is the main compatible solute of halophilic eubacteria. J. Bacteriol.160, 478–479. doi: 10.1128/jb.160.1.478-479.1984

  • CrossRef
  • Google Scholar

• 60

  Ivanova E. P. Gorshkova N. M. Bowman J. P. Lysenko A. M. Zhukova N. V. Sergeev A. F. et al . (2004). Shewanella pacifica sp. nov., a polyunsaturated fatty acid-producing bacterium isolated from sea water. Int. J. Syst. Evol. Microbiol.54, 1083–1087. doi: 10.1099/ijs.0.02993-0

  • CrossRef
  • Google Scholar

• 61

  Jameson E. Doxey A. C. Airs R. Purdy K. J. Murrell J. C. Chen. Y. (2016a). Metagenomic data-mining reveals contrasting microbial populations responsible for trimethylamine formation in human gut and marine ecosystems. Microb. Genom.2, e000080. doi: 10.1099/mgen.0.000080

  • CrossRef
  • Google Scholar

• 62

  Jameson E. Fu T. Brown I. R. Paszkiewicz K. Purdy K. J. Frank S. et al . (2016b). Anaerobic choline metabolism in microcompartments promotes growth and swarming of Proteus mirabilis. Environ. Microbiol.18, 2886–2898. doi: 10.1111/1462-2920.13059

  • CrossRef
  • Google Scholar

• 63

  Jameson E. Stephenson J. Jones H. Millard A. Kaster A. K. Purdy K. J. et al . (2018). Deltaproteobacteria (Pelobacter) and Methanococcides are responsible for choline-dependent methanogenesis in a coastal saltmarsh sediment. ISME J.13, 277–289. doi: 10.1038/s41396-018-0269-8

  • CrossRef
  • Google Scholar

• 64

  Johnson W. M. Longnecker K. Kido Soule M. C. Arnold W. A. Bhatia M. P. Hallam S. J. et al . (2020). Metabolite composition of sinking particles differs from surface suspended particles across a latitudinal transect in the South Atlantic. Limnol. Oceanogr.65, 111–127. doi: 10.1002/lno.11255

  • CrossRef
  • Google Scholar

• 65

  Keller M. Matrai P. Kiene R. Bellows W. (2004). Responses of coastal phytoplankton populations to nitrogen additions: dynamics of cell-associated dimethylsulfoniopropionate (DMSP), glycine betaine (GBT), and homarine. Can. J. Fish. Aquat. Sci.61, 685–699. doi: 10.1139/f04-058

  • CrossRef
  • Google Scholar

• 66

  Keller M. D. Kiene R. P. Matrai P. A. Bellows W. K. (1999a). Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. I. Batch cultures. Mar. Biol.135, 237–248. doi: 10.1007/s002270050621

  • CrossRef
  • Google Scholar

• 67

  Keller M. D. Kiene R. P. Matrai P. A. Bellows W. K. (1999b). Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat cultures. Mar. Biol.135, 249–257. doi: 10.1007/s002270050622

  • CrossRef
  • Google Scholar

• 68

  Kiene R. Slezak D. (2006). Low dissolved DMSP concentrations in seawater revealed by small volume gravity filtration and dialysis sampling. Limnol. Oceanogr. Meth.4, 80–95. doi: 10.4319/lom.2006.4.80

  • CrossRef
  • Google Scholar

• 69

  King G. M. (1984). Metabolism of trimethylamine, choline and glycine betaine by sulfate-reducing and methanogenic bacteria in marine sediments. Appl. Environ. Microbiol.48, 719–725. doi: 10.1128/aem.48.4.719-725.1984

  • CrossRef
  • Google Scholar

• 70

  King G. M. (1988). Methanogenesis from methylated amines in a hypersaline algal mat. Appl. Environ. Microbiol.54, 130–136. doi: 10.1128/aem.54.1.130-136.1988

  • CrossRef
  • Google Scholar

• 71

  Koc H. Mar M. H. Ranasinghe A. Swenberg J. A. Zeisel S. H. (2002). Quantitation of choline and its metabolites in tissues and foods by liquid chromatography/electrospray ionization-isotope dilution mass spectrometry. Anal. Chem.74, 4734–4740. doi: 10.1021/ac025624x

  • CrossRef
  • Google Scholar

• 72

  Kondo Y. Sakamoto A. Nonaka H. Hayashi H. Saradhi P. P. Chen T. H. et al . (1999). Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol. Biol.40, 279–288. doi: 10.1023/A:1006121821883

  • CrossRef
  • Google Scholar

• 73

  Leblanc L. Gouffi K. Leroi F. Hartke A. Blanco C. Auffray Y. et al . (2001). Uptake of choline from salmon flesh and its conversion to glycine betaine in response to salt stress in Shewanella putrefaciens. Int. J. Food Microbiol.65, 93–103. doi: 10.1016/S0168-1605(00)00516-X

  • CrossRef
  • Google Scholar

• 74

  Lee C. Olson B. L. (1984). Dissolved, exchangeable and bound aliphatic amines in marine sediments: initial results, org. Geochem6, 259–263.

  • Google Scholar

• 75

  Leng C. Kish J. D. Roberts J. E. Dwebi I. Chon N. Liu Y. (2015). J. Phys. Chem. A119, 8884–8891. doi: 10.1021/acs.jpca.5b05174

  • CrossRef
  • Google Scholar

• 76

  Li M. Li Z. Li S. Guo S. Meng Q. Li G. et al . (2014). Genetic engineering of glycine betaine biosynthesis reduces heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Mol. Biol. Rep.32, 42–51. doi: 10.1007/s11105-013-0594-z

  • CrossRef
  • Google Scholar

• 77

  Li D. Wang M. Zhang T. Chen X. Li C. Liu Y. et al . (2021). Glycinebetaine mitigated the photoinhibition of photosystem II at high temperature in transgenic tomato plants. Photosyn. Res.147, 301–315. doi: 10.1007/s11120-020-00810-2

  • CrossRef
  • Google Scholar

• 78

  Liang C. Zhang X. Y. Luo Y. Wang G. P. Zou Q. Wang W. (2009). Overaccumulation of glycine betaine alleviates the negative effects of salt stress in wheat. Russ. J. Plant Physiol.56, 370–376. doi: 10.1134/S1021443709030108

  • CrossRef
  • Google Scholar

• 79

  Lichty K. E. B. Loughran R. M. Ushijima B. Richards G. P. Boyd E. F. (2024). Osmotic stress response of the coral and oyster pathogen Vibrio coralliilyticus: acquisition of catabolism gene clusters for the compatible solute and signaling molecule myo-inositol. Appl. Environ. Microbiol.90, e00920–e00924. doi: 10.1128/aem.00920-24

  • CrossRef
  • Google Scholar

• 80

  Lidbury I. Kröber E. Zhang Z. Zhu Y. Murrell J. C. Chen Y. et al . (2016). A mechanism for bacterial transformation of dimethylsulfide to dimethylsulfoxide: a missing link in the marine organic sulfur cycle. Environ. Microbiol.18, 2754–2766. doi: 10.1111/1462-2920.13354

  • CrossRef
  • Google Scholar

• 81

  Lidbury I. Mausz M. Scanlan D. J. Chen Y. (2017). Identification of dimethylamine monooxygenase in marine bacteria reveals a metabolic bottleneck in the marine methylated amine degradation pathway. ISME J.11, 1592–1601. doi: 10.1038/ismej.2017.31

  • CrossRef
  • Google Scholar

• 82

  Lidbury I. Murrell J. C. Chen Y. (2014). Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria. P. Natl. Acad. Sci. U.S.A.111-, 2715. doi: 10.1073/pnas.1317834111

  • CrossRef
  • Google Scholar

• 83

  Lidbury I. Murrell J. C. Chen Y. (2015). Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: Implications for marine carbon and nitrogen cycling. ISME J.9, 760–769. doi: 10.1038/ismej.2014.149

  • CrossRef
  • Google Scholar

• 84

  Mackay M. A. Norton R. S. Borowitzka L. J. (1984). Organic osmoregulatory solutes in cyanobacteria. J. Gen. Microbiol.130, 2177–2191. doi: 10.1099/00221287-130-9-2177

  • CrossRef
  • Google Scholar

• 85

  Mausz M. A. Airs R. L. Dixon J. L. Widdicombe C. E. Tarran G. A. Polimene L. et al . (2022). Microbial uptake dynamics of choline and glycine betaine in coastal seawater. Limnol. Oceanogr.67, 1052–1064. doi: 10.1002/lno.12056

  • CrossRef
  • Google Scholar

• 86

  Mausz M. A. Chen Y. (2019). Microbiology and ecology of methylated amine metabolism in the marine environment. Curr. Issues Mol. Biol.33, 133–148. doi: 10.21775/cimb.033.133

  • CrossRef
  • Google Scholar

• 87

  McParland E. L. Alexander H. Johnson W. M. (2021). The osmolyte ties that bind: genomic insights into synthesis and breakdown of organic osmolytes in marine microbes. Front. Mar. Sci.8. doi: 10.3389/fmars.2021.689306

  • CrossRef
  • Google Scholar

• 88

  Meng X. L. Gao X. Si Y. M. Xu L. L. Guo L. Z. Lu W. D. (2022). Role of carnitine in adaptation of Chromohalobacter salexigens DSM 3043 and its mutants to osmotic and temperature stress in defined medium. Extremophiles26, 28. doi: 10.1007/s00792-022-01276-x

  • CrossRef
  • Google Scholar

• 89

  Meyer M. Granderath K. Andreesen J. R. (1995). Purification and characterization of protein PB of betaine reductase and its relationship to the corresponding proteins glycine reductase and sarcosine reductase from Eubacterium acidaminophilum. Eur. J. Biochem.234, 184–191. doi: 10.1111/j.1432-1033.1995.184_c.x

  • CrossRef
  • Google Scholar

• 90

  Monnich K. Hanschmann H. Kleber H. P. (1995). Utilization of D-carnitine by pseudomonas sp. AK 1. FEMS Microbiol. Lett.132, 51–55. doi: 10.1111/j.1574-6968.1995.tb07809.x

  • CrossRef
  • Google Scholar

• 91

  Mäkelä P. S. A. Jokinen K. Himanen K. (2019). “Roles of endogenous glycinebetaine in plant abiotic stress responses”. In: HossainM.KumarV.BurrittD.FujitaM.MäkeläP. (eds) Osmoprotectant-mediated abiotic stress tolerance in plants. Springer, Cham. doi: 10.1007/978-3-030-27423-8_7

  • CrossRef
  • Google Scholar

• 92

  Noell S. Giovannoni S. (2019). SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter. Environ. Microbiol.21, 2559–2575. doi: 10.1111/1462-2920.14649

  • CrossRef
  • Google Scholar

• 93

  Ongagna-Yhombi S. Y. Boyd E. F. (2013). Biosynthesis of the osmoprotectant ectoine, but not glycine betaine, is critical for survival of osmotically stressed Vibrio parahaemolyticus cells. Appl. Environ. Microbiol.79, 5038–3049. doi: 10.1128/AEM.01008-13

  • CrossRef
  • Google Scholar

• 94

  Oremland R. S. Marsh L. M. Polcin S. (1982). Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature296, 143–145. doi: 10.1038/296143a0

  • CrossRef
  • Google Scholar

• 95

  Oren A. (1990). Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie van Leeuwenhoek58, 291–298. doi: 10.1007/BF00399342

  • CrossRef
  • Google Scholar

• 96

  Oufir M. Schulz N. Vallikhan P. S. S. Wilhelm E. Burg K. Hausman J. F. et al . (2009). Simultaneous measurement of proline and related compounds in oak leaves by high-performance ligand-exchange chromatography and electrospray ionization mass spectrometry for environmental stress studies. J. Chromatogr. A1216, 1094–1099. doi: 10.1016/j.chroma.2008.12.030

  • CrossRef
  • Google Scholar

• 97

  Papageorgiou G. C. Murata N. (1995). The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem-II complex. Photosynth. Res.44, 243–252. doi: 10.1007/BF00048597

  • CrossRef
  • Google Scholar

• 98

  Pflughoeft K. J. Kierek K. Watnick P. I. (2003). Role of Ectoine in Vibrio cholerae osmoadaptation. Appl. Environ. Microbiol.69, 5919–5927. doi: 10.1128/AEM.69.10.5919-5927.2003

  • CrossRef
  • Google Scholar

• 99

  Prasad K. V. S. K. Saradhi P. P. (2004). Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycine betaine biosynthesis into the chloroplasts. Plant Sci.166, 1197–1212. doi: 10.1016/j.plantsci.2003.12.031

  • CrossRef
  • Google Scholar

• 100

  Rajakovich L. J. Fu B. Bollenbach M. Balskus E. P. (2021). Elucidation of an aerobic pathway for metabolism of L-carnitine-derived butyrobetaine to trimethylamine in human gut bacteria. P. Natl. Acad. Sci. U.S.A.118, e2101498118. doi: 10.1073/pnas.2101498118

  • CrossRef
  • Google Scholar

• 101

  Raymond J. A. Plopper G. E. (2002). A bacterial TMAO transporter. Comp. Biochem. Physiol. B Biochem. Mol. Biol.133, 29–34. doi: 10.1016/S1096-4959(02)00097-0

  • CrossRef
  • Google Scholar

• 102

  Reed R. H. Borowitzka L. J. Mackay M. Chudek J. A. Foster R. Warr S. R. C. et al . (1986). Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol. Lett.39, 51–56. doi: 10.1111/j.1574-6968.1986.tb01842.x

  • CrossRef
  • Google Scholar

• 103

  Riccobono F. Schobesberger S. Scott C. E. Dommen J. Ortega I. K. Rondo L. et al . (2014). Oxidation products of biogenic emissions contribute to nucleation of atmospheric particles. Science344, 717–721. doi: 10.1126/science.1243527

  • CrossRef
  • Google Scholar

• 104

  Rivero R. M. Mestre T. C. Mittler R. Rubio F. Garcia-Sanchez F. Martinez V . (2014). Stress combination in tomato plants. Plant Cell Environ.37, 1059–1073. doi: 10.1111/pce.12199

  • CrossRef
  • Google Scholar

• 105

  Roberts M. F. (2005). Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst.1, 5. doi: 10.1186/1746-1448-1-5

  • CrossRef
  • Google Scholar

• 106

  Roman D. Meisinger P. Guillonneau R. Peng C. C. Peltner L. K. Jordan P. M. et al . (2024). Structure revision of a widespread marine sulfonolipid class based on isolation and total synthesis. Angew Chem. Int. Ed Engl.63, e202401195. doi: 10.1002/anie.202401195

  • CrossRef
  • Google Scholar

• 107

  Sacks J. S. Heal K. R. Boysen A. K. Carlson L. T. Ingalls A. E. (2022). Quantification of dissolved metabolites in environmental samples through cation-exchange solid-phase extraction paired with liquid chromatography–mass spectrometry. Limnol. Oceanogr. Meth.20, 683–700. doi: 10.1002/lom3.10513

  • CrossRef
  • Google Scholar

• 108

  Sakamoto A. Murata N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ.25, 163–171. doi: 10.1046/j.0016-8025.2001.00790.x

  • CrossRef
  • Google Scholar

• 109

  Sleator R. D. Hill C. (2002). Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev.26, 49–71. doi: 10.1016/S0168-6445(01)00071-7

  • CrossRef
  • Google Scholar

• 110

  Smith A. F. Silvano E. Päuker O. Guillonneau R. Quareshy M. Murphy A. et al . (2021). A novel class of sulfur-containing aminolipids widespread in marine roseobacters. ISME J.15, 2440–2453. doi: 10.1038/s41396-021-00933-x

  • CrossRef
  • Google Scholar

• 111

  Spielmeyer A. Gebser B. Pohnert G. (2011). Dimethylsulfide sources from microalgae: Improvement and application of a derivitization-based method for the detemination of dimethylsulfoniopropionate and other zwitterionic osmolytes in phytoplankton. Mar. Chem.124, 48–56. doi: 10.1016/j.marchem.2010.12.001

  • CrossRef
  • Google Scholar

• 112

  Spielmeyer A. Pohnert G. (2012). Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Mar. Environ. Res.73, 62–69. doi: 10.1016/j.marenvres.2011.11.002

  • CrossRef
  • Google Scholar

• 113

  Storey R. Wyn Jones R. G. (1977). Quaternary ammonium compounds in plants in relation to salt resistance. Phytochemistry16, 447–453. doi: 10.1016/S0031-9422(00)94326-7

  • CrossRef
  • Google Scholar

• 114

  Sun J. Steindler L. Thrash J. C. Halsey K. H. Smith D. P. Carter A. E. et al . (2011). One carbon metabolism in SAR11 pelagic marine bacteria. PloS One6, e23973. doi: 10.1371/journal.pone.0023973

  • CrossRef
  • Google Scholar

• 115

  Tilgner A. Schaefer T. Alexander B. Barth M. Collett J. L. Jr. Fahey K. M. et al . (2021). Acidity and the multiphase chemistry of atmospheric aqueous particles and clouds. Atmos. Chem. Phys.21, 13483–13536. doi: 10.5194/acp-21-13483-2021

  • CrossRef
  • Google Scholar

• 116

  Van Neste A. Duce R. A. Lee C. (1987). Methylamines in the marine atmosphere. Geophysical Res. Lett.7, 711–714. doi: 10.1029/GL014i007p00711

  • CrossRef
  • Google Scholar

• 117

  Van Pinxteren M. Fomba K. van Pinxteren D. Triesch N. Hoffmann E. Cree C. et al . (2019). Aliphatic amines at the Cape Verde Atmospheric Observatory: abundance, origins and sea-air fluxes. Atmos. Environ.203, 183–195. doi: 10.1016/j.atmosenv.2019.02.011

  • CrossRef
  • Google Scholar

• 118

  Vogel G. Woznica M. Gfeller H. Müller C. Stämpfli A. A. Jenny T. A. et al . (1990). 1(3),2-Diacylglyceryl-3(1)-O-2′-(hydroxymethyl)(N,N,N,-trimethyl)-β-alanine (DGTA): A novel betaine lipid from Ochoromonas danica (Chrysophyceae). Chem. Phys. Lipids52, 99–109. doi: 10.1016/0009-3084(90)90154-J

  • CrossRef
  • Google Scholar

• 119

  Wang G. P. Hui Z. Li F. Zhao M.-R. Zhank J. Wang W. (2010). Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycinebetaine. Plant Biotechnol. Rep.4, 213–222. doi: 10.1007/s11816-010-0139-y

  • CrossRef
  • Google Scholar

• 120

  Wang X. C. Lee C. (1990). The distribution and adsorption behavior of aliphatic-amines in marine and lacustrine sediments. Geochim. Cosmochim. Acta54, 2759–2774. doi: 10.1016/0016-7037(90)90010-I

  • CrossRef
  • Google Scholar

• 121

  Wang X. C. Lee C. (1993). Adsorption and desorption of aliphatic amines, amino acids and acetate by clay minerals and marine sediments. Mar. Chem.44, 1–23. doi: 10.1016/0304-4203(93)90002-6

  • CrossRef
  • Google Scholar

• 122

  Wang Y. Liu S. Zhang H. Zhao Y. Zhao H. Liu H. (2014). Glycine betaine application in grain filling wheat plants alleviates heat and high light-induced photoinhibition by enhancing the psbA transcription and stomatal conductance. Acta Physiol. Plant36, 2195–2202. doi: 10.1007/s11738-014-1596-7

  • CrossRef
  • Google Scholar

• 123

  Wright R. R. Hobbie J. E. (1966). Use of glucose and acetate by bacteria and algae in aquatic ecosystems. Ecology47, 447–464. doi: 10.2307/1932984

  • CrossRef
  • Google Scholar

• 124

  Yancey P. H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol.208, 2819–2830. doi: 10.1242/jeb.01730

  • CrossRef
  • Google Scholar

• 125

  Yancey P. H. Clark M. E. Hand S. C. Bowlus R. D. Somero G. N. (1982). Living with water stress: evolution of osmolyte systems. Science217, 1214–1222. doi: 10.1126/science.7112124

  • CrossRef
  • Google Scholar

• 126

  Yang X. H. Lee C. Scranton M. I. (1993). Determination of nanomolar concentrations of individual dissolved low molecular weight amines and organic acids in seawater. Anal. Chem.65, 572–576. doi: 10.1021/ac00053a014

  • CrossRef
  • Google Scholar

• 127

  Yang C. C. Packman L. C. Scrutton N. S. (1995). The primary structure of Hyphomicrobium X dimethylamine dehydrogenase. Relationship to Trimethylamine Dehydrogenase and Implications for Substrate Recognition. Eur. J. Biochem.232, 264–271. doi: 10.1111/j.1432-1033.1995.tb20808.x

  • CrossRef
  • Google Scholar

• 128

  Yin Q. Zhang W. Li X. Zhou L. Qi X. Zhang C. et al . (2019). Contribution of trimethylamine N-oxide on the growth and pressure tolerance of deep-sea bacteria. J. Ocean. Limnol.37, 210–222. doi: 10.1007/s00343-019-7377-9

  • CrossRef
  • Google Scholar

• 129

  Zecher K. Hayes K. R. Philipp B. (2020). Evidence of interdomain ammonium cross-feeding from methylamine- and glycine betaine-degrading Rhodobacteraceae to diatoms as a widespread interaction in the marine phycosphere. Front. Microbiol.11. doi: 10.3389/fmicb.2020.533894

  • CrossRef
  • Google Scholar

• 130

  Zhang W. J. Zhang C. Zhou S. Li X. G. Mangenot S. Fouteau S. et al . (2021). Comparative genomic analysis of obligately piezophilic Moritella yayanosii DB21MT-5 reveals bacterial adaptation to the challenger deep, Mariana Trench. Microb. Genom.7, 7. doi: 10.1099/mgen.0.000591

  • CrossRef
  • Google Scholar

• 131

  Zhu Y. Jameson E. Crosatti M. Schäfer H. Rajakumar K. Bugg T. D. et al . (2014). Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota. Proc. Natl. Acad. Sci. U.S.A.111, 4268–4273. doi: 10.1073/pnas.1316569111

  • CrossRef
  • Google Scholar