Hongyue Dang- State Key Laboratory of Marine Environmental Science, Institute of Marine Microbes and Ecospheres, College of Ocean and Earth Sciences, Frontiers Science Center for Ocean Carbon Sink and Climate Change, Fujian Key Laboratory of Marine Carbon Sequestration, Xiamen University, Xiamen, China
Given the climate change crisis, it is urgent to reduce anthropogenic CO2 emissions and explore climate geoengineering opportunities. The ocean plays critical roles in global carbon cycling and may provide a solution for climate change mitigation (Buesseler et al., 2008; Yoon et al., 2018). An accurate understanding of the processes and mechanisms of the marine carbon cycle and its interactions with human-driven climate change is fundamentally important. The Aquatic Microbiology Section made important contributions of new knowledge and insights to this research field, including focused investigations on marine primary production, organic matter biodegradation and biotransformation, and microbial responses to natural and anthropogenic environmental gradients and stressors (e.g., Bullerjahn and Post, 2014; Labbate et al., 2016; Daniel et al., 2018; Gutierrez et al., 2018; Mayali, 2018; Villar-Argaiz et al., 2018; Wilson and Church, 2018; Dang et al., 2019; Murillo et al., 2019; Sala et al., 2019; Wietz et al., 2019).
Coastal vs. Oceanic Blue Carbon Sinks
Vegetated coastal ecosystems (VCEs), including mangrove forests, salt marshes, seagrass meadows, and seaweed beds, constitute intense blue carbon sinks at the land–ocean transition zones (Nellemann et al., 2009; Macreadie et al., 2019). Conserving and restoring VCEs for maintaining and enhancing blue carbon sequestration have been proposed as an integral part of strategies for climate remediation (Geraldi et al., 2019). However, the VCEs are also hotspots of non-CO2 greenhouse gas emissions due to anthropogenic eutrophication-enhanced microbial activities including CH4 and N2O production (Angell et al., 2018; Dang and Li, 2018). Although VCEs may contribute to climate change mitigation at the local and national scales, they occupy a very limited spatial extent on Earth and thus their climate remediation potential is small at the global scale (Taillardat et al., 2018).
The ocean is a huge carbon sink and of enormous climate remediation potential. It absorbs atmospheric CO2 via both physical and biological processes. Unfortunately, excess CO2 absorbed via physical processes causes ocean acidification (Doney et al., 2009). Decreasing seawater pH and carbonate saturation states change the food web structure and biogeochemical cycles of the ocean, causing loss of marine ecosystem stability and services (Cooley et al., 2016; Hurd et al., 2018). Ocean acidification may even trigger a sixth mass extinction event (Veron, 2008). Therefore, it is inappropriate to inject more CO2 into the ocean via physical methods for climate remediation (IPCC, 2005; Reith et al., 2019). On the contrary, biological CO2 fixation converts inorganic carbon into organic matter, providing a more favorable mechanism of the ocean to absorb atmospheric CO2 (Falkowski and Raven, 2007; Siegel et al., 2016).
Biological Carbon Pump vs. Microbial Carbon Pump
Marine ecosystems contribute half of all biological carbon fixation on Earth. However, in order for long-term carbon sequestration, photosynthetically fixed carbon needs to be transported to and stored in deep ocean waters and sediments. The biological carbon pump (BCP) helps fulfill this function, transporting particulate organic carbon (POC) from the ocean surface to its interior and thus contributing to climate modulation on geological time scales (Falkowski and Raven, 2007; Le Moigne, 2019). The microbial carbon pump (MCP) is another biological carbon sequestration mechanism (Jiao et al., 2010). The essence of MCP is the microbial transformation of labile dissolved organic carbon (LDOC) into recalcitrant dissolved organic carbon (RDOC) that is resistant to further biological degradation and thus maintained in the ocean for decades to millennia (Ogawa et al., 2001; Jiao et al., 2014). Both structural recalcitrance and low concentration of DOC molecules contribute to their persistence (Jiao et al., 2014, 2015; Arrieta et al., 2015). However, there are debates on the relative contributions of these two distinct mechanisms to the formation of the huge RDOC pool in the ocean (Arrieta et al., 2015; Zark et al., 2017; Wang et al., 2018; Shen and Benner, 2019). These debates advance studies examining the marine DOC molecular composition (Petras et al., 2017; Zark et al., 2017). The MCP generates both structural recalcitrance and a huge molecular diversity of DOC compounds each present at picomolar or subpicomolar concentrations (i.e., below microbial uptake thresholds) to evade being further consumed (Mentges et al., 2017; Jiao et al., 2018; Zark and Dittmar, 2018; Noriega-Ortega et al., 2019).
Microorganisms shape the marine ecosystems and drive the biogeochemical cycles (Azam et al., 1983; Azam and Malfatti, 2007; Falkowski et al., 2008). The carbon sequestration efficiency of both BCP and MCP is mainly regulated by microbial communities (Dang and Lovell, 2016; Zhang et al., 2018). POC and dissolved organic carbon (DOC) are the two distinct forms of organic carbon in the ocean, supporting distinct carbon sequestration processes, respectively. The formulation of the BCP concept started more than 35 years ago (Volk and Hoffert, 1985), and research on this front has been being highly active ever since (Siegel et al., 2016; Le Moigne, 2019). Although the concept of MCP is quite new, its research is gaining recognition and momentum (Zhang et al., 2018). In spite of the great research efforts, neither MCP nor BCP has achieved full understanding, regarding their respective quantitative contribution to climate modulation and the environmental and biological factors that may control their contributions and dynamics (Boyd, 2015; Robinson et al., 2018).
Primary Production vs. Respiration
Organic matter provides the basis for the BCP and MCP to function. Most organic matter in the surface ocean is produced by primary producers. Thus, the marine primary production, which is subject to both top-down and bottom-up controls, is a key factor influencing BCP and MCP (Lechtenfeld et al., 2015; Siegel et al., 2016). Zooplankton grazing and viral lysis affect the composition, biomass, productivity, and partitioning of produced organic matter (particulate vs. dissolved) of the primary producer communities (Jiao et al., 2010; Sime-Ngando, 2014; Worden et al., 2015; Steinberg and Landry, 2017; Zimmerman et al., 2020). The availability and chemical speciation of nutrients play a critical role in determining the composition, abundance, and productivity of the marine photosynthetic microbial communities as well, and different phytoplankton may have distinct carbon export potentials (Herndl and Reinthaler, 2013; Richardson, 2019). Warming and nutrient scarcity may shift the phytoplankton communities, favoring taxa with small cell sizes, such as picocyanobacteria (Hutchins and Fu, 2017). Prochlorococcus are the most abundant and productive picocyanobacteria in oligotrophic oceans (Partensky et al., 1999; García-Fernández et al., 2004). They can hardly sink quickly enough on their own to directly contribute to BCP. However, this typical view is recently challenged (Richardson, 2019). Prochlorococcus are a potential source of transparent exopolymer particles (TEPs) that enhance marine aggregate formation and thus facilitate the BCP (Iuculano et al., 2017). Heterotrophic bacteria may also play a role in prompting TEP production and aggregate formation of Prochlorococcus (Cruz and Neuer, 2019). DOC released from Prochlorococcus via viral lysis and other processes may fuel the MCP for RDOC production (Zhao et al., 2017). The whole ecosystem structure has recently been proposed to majorly set the carbon sequestration efficiency (Guidi et al., 2016; Moriceau et al., 2018; Bach et al., 2019; Henson et al., 2019). These examples highlight the need of systematic and mechanistic investigations on the marine ecosystem key players and interactions, particularly in terms of their carbon sequestration roles and quantitative contributions.
Chemolithoautotrophic bacteria and archaea contribute organic carbon to the ocean as well (Herndl and Reinthaler, 2013; Dang and Chen, 2017). They not only play a key role in sustaining the chemosynthetic ecosystems related to deep-sea hydrothermal vents and cold seeps (McNichol et al., 2018; Dick, 2019) but also may contribute significantly to food web and energy transfer in non-extreme environments (Herndl and Reinthaler, 2013). Dark carbon fixation may provide substantial primary production in certain marine waters (Taylor et al., 2001; Yakimov et al., 2011; Celussi et al., 2017; Guerrero-Feijóo et al., 2018; La Cono et al., 2018). Microbial degradation and remineralization of marine particulate organic matter (POM) significantly lower the BCP efficiency (Turner, 2015; Dang and Lovell, 2016). However, the same processes regenerate nutrients and energy sources, likely playing a role in fueling chemolithoautotrophy and partially offsetting fixed carbon loss during sinking POM remineralization (Wright et al., 2012; Herndl and Reinthaler, 2013; Dang and Chen, 2017). Chemolithoautotrophy may help fuel the MCP as well. Ammonia-oxidizing archaea, usually dominant in mesopelagic and bathypelagic marine waters, release DOC to partially support in situ prokaryotic heterotrophy (Bayer et al., 2019). The contribution of chemolithoautotrophy to the global ocean's primary production, BCP, and MCP warrants further investigation.
Although the ocean's total primary production is very high (up to 50 Gt C/year), only a small fraction (<10%) is transported to the deep ocean via the BCP and even a smaller fraction (<1%) is sequestered for millennia (Henson et al., 2011; Bach et al., 2019; Fender et al., 2019; Giering et al., 2020). The majority of the marine primary production is converted back to CO2 in the ocean's twilight zone via community respiration, to which the microbes usually contribute the most (~50% to >90%) (Rivkin and Legendre, 2001; Sanders et al., 2016). Heterotrophic microbes uptake and respire DOC, and many particle-associated microbes secrete extracellular enzymes to hydrolyze POC into DOC (Arnosti, 2011; Orcutt et al., 2011; Dang and Lovell, 2016; Baltar, 2018). Respiration not only significantly lowers the BCP efficiency but also may cause deoxygenation and acidification in the affected marine waters (Cai et al., 2011; Oschlies et al., 2018; Robinson, 2019). Respiration may constrain the MCP as well (Robinson and Ramaiah, 2011; Dang and Jiao, 2014).
Although respiration is a fundamental metabolic process and the balance between respiration and primary production controls the ecosystem carbon storage capacity, respiration is much less investigated than primary production in the ocean (del Giorgio and Duarte, 2002; Arístegui et al., 2009; Robinson, 2019). This situation hinders our understanding of the ocean's carbon cycle. For example, the subtropical gyres cover ~40% of the Earth surface (Karl and Church, 2014). However, whether these oligotrophic open oceans are overall autotrophic (i.e., net CO2 sinks) or heterotrophic (i.e., net CO2 sources) is still being debated (Duarte et al., 2013; Ducklow and Doney, 2013; Williams et al., 2013; Koeve and Kähler, 2016), let alone confident prediction of their climate modulation potentials.
Perspectives
The BCP (~0.2–0.5 Gt C/year) and MCP (~0.2 Gt C/year) may make similar contributions to long-term organic carbon sequestration (Guidi et al., 2015; Legendre et al., 2015; Giering et al., 2020), and both show climate geoengineering potentials (Le Moigne, 2019; Richardson, 2019). However, the BCP export efficiency has reduced ~1.5% over the past 33 years of climate warming (Cael et al., 2017), and warmer conditions will induce larger reductions (Boyd, 2015; Barange et al., 2017). The negative response of BCP to warming constitutes a positive feedback on climate change. The response of the MCP to climate change is currently not clearly known. Under the impacts of climate change and other anthropogenic perturbations, the global nitrogen cycle and ecosystem biodiversity may have already crossed the safe planetary boundaries (Rockström et al., 2009), exerting further negative impacts on the carbon cycle and climate through disrupting the coupled biogeochemical cycles (Schlesinger et al., 2011; Boyd et al., 2015). Research on fundamental processes and mechanisms of the BCP and MCP under varying oceanographic and climatic conditions is urgently needed, with a particular focus on integrating the major biogeochemical cycles and the ocean's biological, chemical, and physical processes for a better understanding of the marine carbon cycle and its response to climate change (Lucas et al., 2016; Hwang et al., 2017; Bif et al., 2018; Igarza et al., 2019; Quigley et al., 2019; Romera-Castillo et al., 2019). Mechanistic insights and implementation strategies have recently been proposed (Robinson et al., 2018; Yoon et al., 2018; Zhang et al., 2018; Boyd et al., 2019). Advances in upcoming marine carbon cycling research may also help overcome the uncertainty and difficulty in developing environmental-friendly ocean geoengineering techniques for climate change mitigation, the success of which may as well require interdisciplinary collaborations, strategic planning, technique innovations, and systematic investigations including both BCP and MCP for integrated ocean carbon sequestration enhancement (Polimene et al., 2018; Emerson, 2019; Sloyan et al., 2019; Sogin et al., 2019; Zhang et al., 2019).
Author Contributions
The author confirms being the sole contributor of this work and has approved it for publication.
Funding
This research was supported by the National Key Research and Development Program of China (grant 2016YFA0601303), the National Natural Science Foundation of China (grants 41676122, 91328209, and 41861144018), and the China Ocean Mineral Resources R&D Association (grant DY135-E2-1-04).
Conflict of Interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Angell, J. H., Peng, X., Ji, Q., Craick, I., Jayakumar, A., Kearns, P. J., et al. (2018). Community composition of nitrous oxide-related genes in salt marsh sediments exposed to nitrogen enrichment. Front. Microbiol. 9:170. doi: 10.3389/fmicb.2018.00170
Arístegui, J., Gasol, J. M., Duarte, V. M., and Herndl, G. J. (2009). Microbial oceanography of the dark ocean's pelagic realm. Limnol. Oceanogr. 54, 1501–1529. doi: 10.4319/lo.2009.54.5.1501
Arnosti, C. (2011). Microbial extracellular enzymes and the marine carbon cycle. Annu. Rev. Mar. Sci. 3, 401–425. doi: 10.1146/annurev-marine-120709-142731
Arrieta, J. M., Mayol, E., Hansman, R. L., Herndl, G. J., Dittmar, T., and Duarte, C. M. (2015). Dilution limits dissolved organic carbon utilization in the deep ocean. Science 348, 331–333. doi: 10.1126/science.1258955
Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F. (1983). The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263. doi: 10.3354/meps010257
Azam, F., and Malfatti, F. (2007). Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782–791. doi: 10.1038/nrmicro1747
Bach, L. T., Stange, P., Taucher, J., Achterberg, E. P., Algueró-Muñiz, M., Horn, H., et al. (2019). The influence of plankton community structure on sinking velocity and remineralization rate of marine aggregates. Glob. Biogeochem. Cycles 33, 971–994. doi: 10.1029/2019GB006256
Baltar, F. (2018). Watch out for the “living dead”: cell-free enzymes and their fate. Front. Microbiol. 8:2438. doi: 10.3389/fmicb.2017.02438
Barange, M., Butenschön, M., Yool, A., Beaumont, N., Fernandes, J. A., Martin, A. P., et al. (2017). The cost of reducing the North Atlantic Ocean biological carbon pump. Front. Mar. Sci. 3:290. doi: 10.3389/fmars.2016.00290
Bayer, B., Hansman, R. L., Bittner, M. J., Noriega-Ortega, B. E., Niggemann, J., Dittmar, T., et al. (2019). Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean. Environ. Microbiol. 21, 4062–4075. doi: 10.1111/1462-2920.14755
Bif, M. B., Hansell, D. A., and Popendorf, K. J. (2018). Controls on the fate of dissolved organic carbon under contrasting upwelling conditions. Front. Mar. Sci. 5:463. doi: 10.3389/fmars.2018.00463
Boyd, P. W. (2015). Toward quantifying the response of the oceans' biological pump to climate change. Front. Mar. Sci. 2:77. doi: 10.3389/fmars.2015.00077
Boyd, P. W., Claustre, H., Levy, M., Siegel, D. A., and Weber, T. (2019). Multi-faceted particle pumps drive carbon sequestration in the ocean. Nature 568, 327–335. doi: 10.1038/s41586-019-1098-2
Boyd, P. W., Lennartz, S. T., Glover, D. M., and Doney, S. C. (2015). Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5, 71–79. doi: 10.1038/nclimate2441
Buesseler, K. O., Doney, S. C., Karl, D. M., Boyd, P. W., Caldeira, K., Chai, F., et al. (2008). Ocean iron fertilization—moving forward in a sea of uncertainty. Science 319, 162. doi: 10.1126/science.1154305
Bullerjahn, G. S., and Post, A. F. (2014). Physiology and molecular biology of aquatic cyanobacteria. Front. Microbiol. 5:359. doi: 10.3389/fmicb.2014.00359
Cael, B. B., Bisson, K., and Follows, M. J. (2017). How have recent temperature changes affected the efficiency of ocean biological carbon export? Limnol. Oceanogr. Lett. 2, 113–118. doi: 10.1002/lol2.10042
Cai, W. J., Hu, X. P., Huang, W. J., Murrell, M. C., Lehrter, J. C., Lohrenz, S. E., et al. (2011). Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4, 766–770. doi: 10.1038/ngeo1297
Celussi, M., Malfatti, F., Ziveri, P., Giani, M., and Del Negro, P. (2017). Uptake-release dynamics of the inorganic and organic carbon pool mediated by planktonic prokaryotes in the deep Mediterranean Sea. Environ. Microbiol. 19, 1163–1175. doi: 10.1111/1462-2920.13641
Cooley, S. R., Ono, C. R., Melcer, S., and Roberson, J. (2016). Community-level actions that can address ocean acidification. Front. Mar. Sci. 2:128. doi: 10.3389/fmars.2015.00128
Cruz, B. N., and Neuer, S. (2019). Heterotrophic bacteria enhance the aggregation of the marine picocyanobacteria Prochlorococcus and Synechococcus. Front. Microbiol. 10:1864. doi: 10.3389/fmicb.2019.01864
Dang, H., and Chen, C.-T. A. (2017). Ecological energetic perspectives on responses of nitrogen-transforming chemolithoautotrophic microbiota to changes in the marine environment. Front. Microbiol. 8:1246. doi: 10.3389/fmicb.2017.01246
Dang, H., and Jiao, N. (2014). Perspectives on the microbial carbon pump with special reference to microbial respiration and ecosystem efficiency in large estuarine systems. Biogeosciences 11, 3887–3898. doi: 10.5194/bg-11-3887-2014
Dang, H., Klotz, M. G., Lovell, C. R., and Sievert, S. M. (2019). Editorial: The responses of marine microorganisms, communities and ecofunctions to environmental gradients. Front. Microbiol. 10:115. doi: 10.3389/fmicb.2019.00115
Dang, H., and Li, J. (2018). Climate tipping-point potential and paradoxical production of methane in a changing ocean. Sci. China Earth Sci. 61, 1714–1727. doi: 10.1007/s11430-017-9265-y
Dang, H., and Lovell, C. R. (2016). Microbial surface colonization and biofilm development in marine environments. Microbiol. Mol. Biol. Rev. 80, 91–138. doi: 10.1128/MMBR.00037-15
Daniel, R., Simon, M., and Wemheuer, B. (2018). Editorial: molecular ecology and genetic diversity of the Roseobacter clade. Front. Microbiol. 9:1185. doi: 10.3389/fmicb.2018.01185
del Giorgio, P. A., and Duarte, C. M. (2002). Respiration in the open ocean. Nature 420, 379–384. doi: 10.1038/nature01165
Dick, G. J. (2019). The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17, 271–283. doi: 10.1038/s41579-019-0160-2
Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. (2009). Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192. doi: 10.1146/annurev.marine.010908.163834
Duarte, C. M., Regaudie-de-Gioux, A., Arrieta, J. M., Delgado-Huertas, A., and Agustí, S. (2013). The oligotrophic ocean is heterotrophic. Annu. Rev. Mar. Sci. 5, 551–569. doi: 10.1146/annurev-marine-121211-172337
Ducklow, H. W., and Doney, S. C. (2013). What is the metabolic state of the oligotrophic ocean? A debate. Annu. Rev. Mar. Sci. 5, 525–533. doi: 10.1146/annurev-marine-121211-172331
Emerson, D. (2019). Biogenic iron dust: a novel approach to ocean iron fertilization as a means of large scale removal of carbon dioxide from the atmosphere. Front. Mar. Sci. 6:22. doi: 10.3389/fmars.2019.00022
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
Falkowski, P. G., and Raven, J. A. (2007). Aquatic Photosynthesis, 2nd Edn. Princeton, NJ: Princeton University Press.
Fender, C. K., Kelly, T. B., Guidi, L., Ohman, M. D., Smith, M. C., and Stukel, M. R. (2019). Investigating particle size-flux relationships and the biological pump across a range of plankton ecosystem states from coastal to oligotrophic. Front. Mar. Sci. 6:603. doi: 10.3389/fmars.2019.00603
García-Fernández, J. M., de Marsac, N. T., and Diez, J. (2004). Streamlined regulation and gene loss as adaptive mechanisms in Prochlorococcus for optimized nitrogen utilization in oligotrophic environments. Microbiol. Mol. Biol. Rev. 68, 630–638. doi: 10.1128/MMBR.68.4.630-638.2004
Geraldi, N. R., Ortega, A., Serrano, O., Macreadie, P. I., Lovelock, C. E., Krause-Jensen, D., et al. (2019). Fingerprinting blue carbon: rationale and tools to determine the source of organic carbon in marine depositional environments. Front. Mar. Sci. 6:263. doi: 10.3389/fmars.2019.00263
Giering, S. L. C., Cavan, E. L., Basedow, S. L., Briggs, N., Burd, A. B., Darroch, L. J., et al. (2020). Sinking organic particles in the ocean—flux estimates from in situ optical devices. Front. Mar. Sci. 6:834. doi: 10.3389/fmars.2019.00834
Guerrero-Feijóo, E., Sintes, E., Herndl, G. J., and Varela, M. M. (2018). High dark inorganic carbon fixation rates by specific microbial groups in the Atlantic off the Galician coast (NW Iberian margin). Environ. Microbiol. 20, 602–611. doi: 10.1111/1462-2920.13984
Guidi, L., Chaffron, S., Bittner, L., Eveillard, D., Larhlimi, A., Roux, S., et al. (2016). Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465–470. doi: 10.1038/nature16942
Guidi, L., Legendre, L., Reygondeau, G., Uitz, J., Stemmann, L., and Henson, S. A. (2015). A new look at ocean carbon remineralization for estimating deepwater sequestration. Glob. Biogeochem. Cycles 29, 1044–1059. doi: 10.1002/2014GB005063
Gutierrez, T., Teske, A., Ziervoge, K., Passow, U., and Quigg, A. (2018). Editorial: Microbial exopolymers: Sources, chemico-physiological properties, and ecosystem effects in the marine environment. Front. Microbiol. 9:1822. doi: 10.3389/fmicb.2018.01822
Henson, S., Le Moigne, F., and Giering, S. (2019). Drivers of carbon export efficiency in the global ocean. Glob. Biogeochem. Cycles 33, 891–903. doi: 10.1029/2018GB006158
Henson, S. A., Sanders, R., Madsen, E., Morris, P. J., Le Moigne, F., and Quartly, G. D. (2011). A reduced estimate of the strength of the ocean's biological carbon pump. Geophys. Res. Lett. 38:L04606. doi: 10.1029/2011GL046735
Herndl, G. J., and Reinthaler, T. (2013). Microbial control of the dark end of the biological pump. Nat. Geosci. 6, 718–724. doi: 10.1038/ngeo1921
Hurd, C. L., Lenton, A., Tilbrook, B., and Boyd, P. W. (2018). Current understanding and challenges for oceans in a higher-CO2 world. Nat. Clim. Change 8, 686–694. doi: 10.1038/s41558-018-0211-0
Hutchins, D. A., and Fu, F. (2017). Microorganisms and ocean global change. Nat. Microbiol. 2:17058. doi: 10.1038/nmicrobiol.2017.58
Hwang, J., Manganini, S. J., Park, J., Montlucon, D. B., Toole, J. M., and Eglinton, T. I. (2017). Biological and physical controls on the flux and characteristics of sinking particles on the Northwest Atlantic margin. J. Geophys. Res. Oceans 122, 4539–4553. doi: 10.1002/2016JC012549
Igarza, M., Dittmar, T., Graco, M., and Niggemann, J. (2019). Dissolved organic matter cycling in the coastal upwelling system off Central Peru during an “El Niño” year. Front. Mar. Sci. 6:198. doi: 10.3389/fmars.2019.00198
IPCC (2005). IPCC Special Report on Carbon Dioxide Capture and Storage. Cambridge: Cambridge University Press.
Iuculano, F., Mazuecos, I. P., Reche, I., and Agusti, S. (2017). Prochlorococcus as a possible source for transparent exopolymer particles (TEP). Front. Microbiol. 8:709. doi: 10.3389/fmicb.2017.00709
Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W., et al. (2010). Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599. doi: 10.1038/nrmicro2386
Jiao, N., Legendre, L., Robinson, C., Thomas, H., Luo, Y. W., Dang, H., et al. (2015). Comment on “Dilution limits dissolved organic carbon utilization in the deep ocean”. Science 350:1483. doi: 10.1126/science.aab2713
Jiao, N., Robinson, C., Azam, F., Thomas, H., Baltar, F., Dang, H., et al. (2014). Mechanisms of microbial carbon sequestration in the ocean – future research directions. Biogeosciences 11, 5285–5306. doi: 10.5194/bg-11-5285-2014
Jiao, N. Z., Cai, R. H., Zheng, Q., Tang, K., Liu, J. H., Jiao, F. L. E., et al. (2018). Unveiling the enigma of refractory carbon in the ocean. Natl. Sci. Rev. 5, 459–463. doi: 10.1093/nsr/nwy020
Karl, D. M., and Church, M. J. (2014). Microbial oceanography and the Hawaii Ocean time-series programme. Nat. Rev. Microbiol. 12, 699–713. doi: 10.1038/nrmicro3333
Koeve, W., and Kähler, P. (2016). Oxygen utilization rate (OUR) underestimates ocean respiration: a model study. Glob. Biogeochem. Cycles 30, 1166–1182. doi: 10.1002/2015GB005354
La Cono, V., Ruggeri, G., Azzaro, M., Crisafi, F., Decembrini, F., Denaro, R., et al. (2018). Contribution of bicarbonate assimilation to carbon pool dynamics in the deep Mediterranean Sea and cultivation of actively nitrifying and CO2-fixing bathypelagic prokaryotic consortia. Front. Microbiol. 9:3. doi: 10.3389/fmicb.2018.00003
Labbate, M., Seymour, J. R., Lauro, F., and Brown, M. V. (2016). Editorial: anthropogenic impacts on the microbial ecology and function of aquatic environments. Front. Microbiol. 7:1044. doi: 10.3389/fmicb.2016.01044
Le Moigne, F. A. C. (2019). Pathways of organic carbon downward transport by the oceanic biological carbon pump. Front. Mar. Sci. 6:634. doi: 10.3389/fmars.2019.00634
Lechtenfeld, O. J., Hertkorn, N., Shen, Y., Witt, M., and Benner, R. (2015). Marine sequestration of carbon in bacterial metabolites. Nat. Commun. 6:6711. doi: 10.1038/ncomms7711
Legendre, L., Rivkin, R. B., Weinbauer, M. G., Guidi, L., and Uitz, J. (2015). The microbial carbon pump concept: Potential biogeochemical significance in the globally changing ocean. Prog. Oceanogr. 134, 432–450. doi: 10.1016/j.pocean.2015.01.008
Lucas, J., Koester, I., Wichels, A., Niggemann, J., Dittmar, T., Callies, U., et al. (2016). Short-term dynamics of North Sea bacterioplankton-dissolved organic matter coherence on molecular level. Front. Microbiol. 7:321. doi: 10.3389/fmicb.2016.00321
Macreadie, P. I., Anton, A., Raven, J. A., Beaumont, N., Connolly, R. M., Friess, D. A., et al. (2019). The future of Blue Carbon science. Nat. Commun. 10:3998. doi: 10.1038/s41467-019-11693-w
Mayali, X. (2018). Editorial: metabolic interactions between bacteria and phytoplankton. Front. Microbiol. 9:727. doi: 10.3389/fmicb.2018.00727
McNichol, J., Stryhanyuk, H., Sylva, S. P., Thomas, F., Musat, N., Seewald, J. S., et al. (2018). Primary productivity below the seafloor at deep-sea hot springs. Proc. Natl. Acad. Sci. U.S.A. 115, 6756–6761. doi: 10.1073/pnas.1804351115
Mentges, A., Feenders, C., Seibt, M., Blasius, B., and Dittmar, T. (2017). Functional molecular diversity of marine dissolved organic matter is reduced during degradation. Front. Mar. Sci. 4:194. doi: 10.3389/fmars.2017.00194
Moriceau, B., Iversen, M. H., Gallinari, M., Evertsen, A.-J. O., Le Goff, M., Beker, B., et al. (2018). Copepods boost the production but reduce the carbon export efficiency by diatoms. Front. Mar. Sci. 5:82. doi: 10.3389/fmars.2018.00082
Murillo, A. A., Molina, V., Salcedo-Castro, J., and Harrod, C. (2019). Editorial: Marine microbiome and biogeochemical cycles in marine productive areas. Front. Mar. Sci. 6:657. doi: 10.3389/fmars.2019.00657
Nellemann, C., Corcoran, E., Duarte, C. M., Valdés, L., de Young, C., Fonseca, L., et al. (2009). Blue Carbon. A Rapid Response Assessment. Birkeland: GRID-Arendal: United Nations Environment Programme.
Noriega-Ortega, B. E., Wienhausen, G., Mentges, A., Dittmar, T., Simon, M., and Niggemann, J. (2019). Does the chemodiversity of bacterial exometabolomes sustain the chemodiversity of marine dissolved organic matter? Front. Microbiol. 10:215. doi: 10.3389/fmicb.2019.00215
Ogawa, H., Amagai, Y., Koike, I., Kaiser, K., and Benner, R. (2001). Production of refractory dissolved organic matter by bacteria. Science 292, 917–920. doi: 10.1126/science.1057627
Orcutt, B. N., Sylvan, J. B., Knab, N. J., and Edwards, K. J. (2011). Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361–422. doi: 10.1128/MMBR.00039-10
Oschlies, A., Brandt, P., Stramma, L., and Schmidtko, S. (2018). Drivers and mechanisms of ocean deoxygenation. Nat. Geosci. 11, 467–473. doi: 10.1038/s41561-018-0152-2
Partensky, F., Hess, W. R., and Vaulot, D. (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127. doi: 10.1128/MMBR.63.1.106-127.1999
Petras, D., Koester, I., Da Silva, R., Stephens, B. M., Haas, A. F., Nelson, C. E., et al. (2017). High-resolution liquid chromatography tandem mass spectrometry enables large scale molecular characterization of dissolved organic matter. Front. Mar. Sci. 4:405. doi: 10.3389/fmars.2017.00405
Polimene, L., Rivkin, R. B., Luo, Y. W., Kwon, E. Y., Gehlen, M., Peña, M. A., et al. (2018). Modelling marine DOC degradation time scales. Natl. Sci. Rev. 6, 468–474. doi: 10.1093/nsr/nwy066
Quigley, L. N. M., Edwards, A., Steen, A. D., and Buchan, A. (2019). Characterization of the interactive effects of labile and recalcitrant organic matter on microbial growth and metabolism. Front. Microbiol. 10:493. doi: 10.3389/fmicb.2019.00493
Reith, F., Koeve, W., Keller, D. P., Getzlaff, J., and Oschlies, A. (2019). Meeting climate targets by direct CO2 injections: what price would the ocean have to pay? Earth Syst. Dynam. 10, 711–727. doi: 10.5194/esd-10-711-2019
Richardson, T. L. (2019). Mechanisms and pathways of small-phytoplankton export from the surface ocean. Annu. Rev. Mar. Sci. 11, 57–74. doi: 10.1146/annurev-marine-121916-063627
Rivkin, R. B., and Legendre, L. (2001). Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291, 2398–2400. doi: 10.1126/science.291.5512.2398
Robinson, C. (2019). Microbial respiration, the engine of ocean deoxygenation. Front. Mar. Sci. 5:533. doi: 10.3389/fmars.2018.00533
Robinson, C., and Ramaiah, N. (2011). “Microbial heterotrophic metabolic rates constrain the microbial carbon pump,” in Microbial Carbon Pump in the Ocean, eds F. Azam, N. Jiao, and S. Sanders (Washington, DC: Science/AAAS, 52–53.
Robinson, C., Wallace, D., Hyun, J. H., Polimene, L., Benner, R., Zhang, Y., et al. (2018). An implementation strategy to quantify the marine microbial carbon pump and its sensitivity to global change. Natl. Sci. Rev. 5, 474–480. doi: 10.1093/nsr/nwy070
Rockström, J., Steffen, W., Noone, K., Persson, A., Chapin, F. S. III., Lambin, E. F., et al. (2009). A safe operating space for humanity. Nature 461, 472–475. doi: 10.1038/461472a
Romera-Castillo, C., Álvarez, M., Pelegrí, J. L., Hansell, D. A., and Álvarez-Salgado, X. A. (2019). Net additions of recalcitrant dissolved organic carbon in the deep Atlantic Ocean. Glob. Biogeochem. Cycles 33, 1162–1173. doi: 10.1029/2018GB006162
Sala, M. M., Piontek, J., Endres, S., Romani, A. M., Dyhrman, S., and Steen, A. D. (2019). Editorial: extracellular enzymes in aquatic environments: exploring the link between genomic potential and biogeochemical consequences. Front. Microbiol. 10:1463. doi: 10.3389/fmicb.2019.01463
Sanders, R. J., Henson, S. A., Martin, A. P., Anderson, T. R., Bernardello, R., Enderlein, P., et al. (2016). Controls over ocean mesopelagic interior carbon storage (COMICS): fieldwork, synthesis, and modeling efforts. Front. Mar. Sci. 3:136. doi: 10.3389/fmars.2016.00136
Schlesinger, W. H., Cole, J. J., Finzi, A. C., and Holland, E. A. (2011). Introduction to coupled biogeochemical cycles. Front. Ecol. Environ. 9, 5–8. doi: 10.1890/090235
Shen, Y., and Benner, R. (2019). Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean. Limnol. Oceanogr. 65, 1061–1071. doi: 10.1002/lno.11369
Siegel, D. A., Buesseler, K. O., Behrenfeld, M. J., Benitez-Nelson, C. R., Boss, E., Brzezinski, M. A., et al. (2016). Prediction of the export and fate of global ocean net primary production: the EXPORTS science plan. Front. Mar. Sci. 3:22. doi: 10.3389/fmars.2016.00022
Sime-Ngando, T. (2014). Environmental bacteriophages: viruses of microbes in aquatic ecosystems. Front. Microbiol. 5:355. doi: 10.3389/fmicb.2014.00355
Sloyan, B. M., Wanninkhof, R., Kramp, M., Johnson, G. C., Talley, L. D., Tanhua, T., et al. (2019). The global ocean ship-based hydrographic investigations program (GO-SHIP): A platform for integrated multidisciplinary ocean science. Front. Mar. Sci. 6:445. doi: 10.3389/fmars.2019.00445
Sogin, E. M., Puskás, E., Dubilier, N., and Liebeke, M. (2019). Marine metabolomics: a method for nontargeted measurement of metabolites in seawater by gas chromatography-mass spectrometry. mSystems 4:e00638-19. doi: 10.1128/mSystems.00638-19
Steinberg, D. K., and Landry, M. R. (2017). Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9, 413–444. doi: 10.1146/annurev-marine-010814-015924
Taillardat, P., Friess, D. A., and Lupascu, M. (2018). Mangrove blue carbon strategies for climate change mitigation are most effective at the national scale. Biol. Lett. 14:20180251. doi: 10.1098/rsbl.2018.0251
Taylor, G. T., Iabichella, M., Ho, T. Y., Scranton, M. I., Thunell, R. C., Muller-Karger, F., et al. (2001). Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol. Oceanogr. 46, 148–163. doi: 10.4319/lo.2001.46.1.0148
Turner, J. T. (2015). Zooplankton fecal pellets, marine snow, phytodetritus and the ocean's biological pump. Prog. Oceanogr. 130, 205–248. doi: 10.1016/j.pocean.2014.08.005
Veron, J. E. N. (2008). Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27, 459–472. doi: 10.1007/s00338-008-0381-8
Villar-Argaiz, M., Medina-Sánchez, J. M., Biddanda, B. A., and Carrillo, P. (2018). Predominant non-additive effects of multiple stressors on autotroph C:N:P ratios propagate in freshwater and marine food webs. Front. Microbiol. 9:69. doi: 10.3389/fmicb.2018.00069
Volk, T., and Hoffert, M. I. (1985). “Ocean carbon pumps: analysis of relative strengths and efficiencies in ocean-driven atmospheric CO2 changes,” in The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present, eds E. T. Sundquist and W. S. Broecker (Washington, DC: American Geophysical Union), 99–110. doi: 10.1029/GM032p0099
Wang, N., Luo, Y. W., Polimene, L., Zhang, R., Zheng, Q., Cai, R., et al. (2018). Contribution of structural recalcitrance to the formation of the deep oceanic dissolved organic carbon reservoir. Environ. Microbiol. Rep. 10, 711–717. doi: 10.1111/1758-2229.12697
Wietz, M., Lau, S. C., and Harder, T. (2019). Editorial: socio-ecology of microbes in a changing ocean. Front. Mar. Sci. 6:190. doi: 10.3389/fmars.2019.00190
Williams, P. J., Quay, P. D., Westberry, T. K., and Behrenfeld, M. J. (2013). The oligotrophic ocean is autotrophic. Annu. Rev. Mar. Sci. 5, 535–549. doi: 10.1146/annurev-marine-121211-172335
Wilson, S. T., and Church, M. J. (2018). Editorial: microbial ecology in the North Pacific subtropical gyre. Front. Mar. Sci. 5:334. doi: 10.3389/fmars.2018.00334
Worden, A. Z., Follows, M. J., Giovannoni, S. J., Wilken, S., Zimmerman, A. E., and Keeling, P. J. (2015). Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science 347:1257594. doi: 10.1126/science.1257594
Wright, J. J., Konwar, K. M., and Hallam, S. J. (2012). Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381–394. doi: 10.1038/nrmicro2778
Yakimov, M. M., La Cono, V., Smedile, F., Deluca, T. H., Juárez, S., Ciordia, S., et al. (2011). Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea). ISME J. 5, 945–961. doi: 10.1038/ismej.2010.197
Yoon, J.-E., Yoo, K.-C., Macdonald, A. M., Yoon, H.-I., Park, K.-T., Yang, E. J., et al. (2018). Reviews and syntheses: ocean iron fertilization experiments – past, present, and future looking to a future Korean Iron Fertilization Experiment in the Southern Ocean (KIFES) project. Biogeosciences 15, 5847–5889. doi: 10.5194/bg-15-5847-2018
Zark, M., Christoffers, J., and Dittmar, T. (2017). Molecular properties of deep-sea dissolved organic matter are predictable by the central limit theorem: evidence from tandem FT-ICR-MS. Mar. Chem. 191, 9–15. doi: 10.1016/j.marchem.2017.02.005
Zark, M., and Dittmar, T. (2018). Universal molecular structures in natural dissolved organic matter. Nat. Commun. 9:3178. doi: 10.1038/s41467-018-05665-9
Zhang, C. L., Dang, H. Y., Azam, F., Benner, R., Legendre, L., Passow, U., et al. (2018). Evolving paradigms in biological carbon cycling in the ocean. Natl. Sci. Rev. 5, 481–499. doi: 10.1093/nsr/nwy074
Zhang, Y., Ryan, J. P., Kieft, B., Hobson, B. W., McEwen, R. S., Godin, M. A., et al. (2019). Targeted sampling by autonomous underwater vehicles. Front. Mar. Sci. 6:415. doi: 10.3389/fmars.2019.00415
Zhao, Z., Gonsior, M., Luek, J., Timko, S., Ianiri, H., Hertkorn, N., et al. (2017). Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties. Nat. Commun. 8:15284. doi: 10.1038/ncomms15284
Keywords: biological carbon pump, blue carbon, chemolithoautotroph, climate change, climate remediation, greenhouse gases, marine carbon cycle, microbial carbon pump
Citation: Dang H (2020) Grand Challenges in Microbe-Driven Marine Carbon Cycling Research. Front. Microbiol. 11:1039. doi: 10.3389/fmicb.2020.01039
Received: 12 November 2019; Accepted: 27 April 2020;
Published: 23 June 2020.
Edited by:
Martin G. Klotz, Washington State University, United StatesReviewed by:
Eric Pieter Achterberg, GEOMAR Helmholtz Center for Ocean Research Kiel, GermanyIan Hewson, Cornell University, United States
Copyright © 2020 Dang. 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: Hongyue Dang, danghy@xmu.edu.cn