Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean

ABSTRACT The biological pump is a process whereby CO2 in the upper ocean is fixed by primary producers and transported to the deep ocean as sinking biogenic particles or as dissolved organic

matter. The fate of most of this exported material is remineralization to CO2, which accumulates in deep waters until it is eventually ventilated again at the sea surface. However, a

proportion of the fixed carbon is not mineralized but is instead stored for millennia as recalcitrant dissolved organic matter. The processes and mechanisms involved in the generation of

this large carbon reservoir are poorly understood. Here, we propose the microbial carbon pump as a conceptual framework to address this important, multifaceted biogeochemical problem. Access

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SIMILAR CONTENT BEING VIEWED BY OTHERS CENTURY-SCALE CARBON SEQUESTRATION FLUX THROUGHOUT THE OCEAN BY THE BIOLOGICAL PUMP Article 27 November 2023 THE MICROBIAL CARBON PUMP AND CLIMATE

CHANGE Article 15 March 2024 EPIPELAGIC NITROUS OXIDE PRODUCTION OFFSETS CARBON SEQUESTRATION BY THE BIOLOGICAL PUMP Article Open access 19 December 2022 REFERENCES * Eppley, R. W. &

Peterson, B. J. Particulate organic matter flux and planktonic new production in the deep ocean. _Nature_ 282, 677–680 (1979). Article  Google Scholar  * Ducklow, H. W., Steinberg, D. K.

& Buesseler, K. O. Upper ocean carbon export and the biological pump. _Oceanography_ 14, 50–58 (2001). Article  Google Scholar  * Karl, D. et al. Biological pump working group summary.

_OCTET_ [online], (2001). Google Scholar  * Raven, J. A. & Falkowski, P. G. Oceanic sinks for atmospheric CO2 . _Plant Cell Environ._ 22, 741–755 (1999). Article  CAS  Google Scholar  *

Aristegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. J. Microbial oceanography of the dark ocean's pelagic realm. _Limnol. Oceanogr._ 54, 1501–1529 (2009). Article  CAS  Google

Scholar  * Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. _Nature Rev. Microbiol._ 5, 782–791 (2007). Article  CAS  Google Scholar  * Riebesell, U. et al. Enhanced

biological carbon consumption in a high CO2 ocean. _Nature_ 450, 545–548 (2007). Article  CAS  PubMed  Google Scholar  * Suttle, C. A. Marine viruses — major players in the global ecosystem.

_Nature Rev. Microbiol._ 5, 801–812 (2007). Article  CAS  Google Scholar  * Mou, X. Z., Sun, S. L., Edwards, R. A., Hodson, R. E. & Moran, M. A. Bacterial carbon processing by

generalist species in the coastal ocean. _Nature_ 451, 708–711 (2008). Article  CAS  PubMed  Google Scholar  * Azam, F., Smith, D. C., Steward, G. F. & Hagstrom, A. Bacteria-organic

matter coupling and its significance for oceanic carbon cycling. _Microb. Ecol._ 28, 167–179 (1993). Article  Google Scholar  * Verdugo, P. et al. The oceanic gel phase: a bridge in the

DOM–POM continuum. _Mar. Chem._ 92, 67–85 (2004). Article  CAS  Google Scholar  * Gehlen, M. et al. Reconciling surface ocean productivity, export fluxes and sediment composition in a global

biogeochemical ocean model. _Biogeosciences_ 3, 521–537 (2006). Article  CAS  Google Scholar  * Wassmann, P. Retention versus export food chains: processes controlling sinking loss from

marine pelagic systems. _Hydrobiologia_ 363, 29–57 (1998). Article  Google Scholar  * Arrigo, K. R. Carbon cycle: marine manipulations. _Nature_ 450, 491–492 (2007). Article  CAS  PubMed 

Google Scholar  * Ducklow, H. W., Carlson, C. A., Bates, N. R., Knap, A. H. & Michaels, A. F. Dissolved organic carbon as a component of the biological pump in the North Atlantic Ocean.

_Philos. Trans. R. Soc. Lond. B_ 348, 161–167 (1995). Article  CAS  Google Scholar  * Biddanda, B. & Benner, R. Carbon, nitrogen, and carbohydrate fluxes during the production of

particulate and dissolved organic matter by marine phytoplankton. _Limnol. Oceanogr._ 42, 506–518 (1997). Article  CAS  Google Scholar  * Nagata, T., Fukuda, H., Fukuda, R. & Koike, I.

Bacterioplankton distribution and production in deep Pacific waters: large-scale geographic variations and possible coupling with sinking particle fluxes. _Limnol. Oceanogr._ 45, 426–435

(2000). Article  CAS  Google Scholar  * Kirchman, D. L. et al. in _Towards a Model of Ocean Biogeochemical Processes_ (eds Evans, G. T. & Fasham, M. J. R.) 209–225 (Springer, Berlin,

1993). Google Scholar  * Eichinger, M., Poggiale, J. C., Van Wambeke, F., Lefevre, D. & Sempere, R. Modelling DOC assimilation and bacterial growth efficiency in biodegradation

experiments: a case study in the Northeast Atlantic Ocean. _Aquat. Microb. Ecol._ 43, 139–151 (2006). Article  Google Scholar  * Carlson, C. A. & Ducklow, H. W. Dissolved organic carbon

in the upper ocean of the central equatorial Pacific Ocean, 1992: daily and finescale vertical variation. _Deep-Sea Res. II_ 42, 639–656 (1995). Article  CAS  Google Scholar  * Bauer, J. E.,

Williams, P. M. & Druffel, E. R. M. 14C activity of dissolved organic carbon fractions in the north-central Pacific and Sargasso Sea. _Nature_ 357, 667–670 (1992). Article  CAS  Google

Scholar  * Kirchman, D. L. et al. Glucose fluxes and concentrations of dissolved combined neutral sugars (polysaccharides) in the Ross Sea and Polar Front Zone, Antarctica. _Deep-Sea Res.

II_ 48, 4179–4197 (2001). Article  CAS  Google Scholar  * Hopkinson, C. S. & Vallino, J. J. Efficient export of carbon to the deep ocean through dissolved organic matter. _Nature_ 433,

142–145 (2005). Article  CAS  PubMed  Google Scholar  * Carlson, C. A. et al. Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic

zone of the northwestern Sargasso Sea. _Limnol. Oceanogr._ 49, 1073–1083 (2004). Article  CAS  Google Scholar  * Jiao, N. Z. et al. Distinct distribution pattern of abundance and diversity

of aerobic anoxygenic phototrophic bacteria in the global ocean. _Environ. Microbiol._ 9, 3091–3099 (2007). Article  CAS  PubMed  Google Scholar  * Hoppe, H. G. & Ullrich, S. Profiles of

ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone. _Aquat. Microb. Ecol._ 19, 139–148 (1999). Article  Google Scholar  * Tamburini, C., Garcin, J.,

Ragot, M. & Bianchi, A. Biopolymer hydrolysis and bacterial production under ambient hydrostatic pressure through a 2000 m water column in the NW Mediterranean. _Deep-Sea Res. II_ 49,

2109–2123 (2002). Article  CAS  Google Scholar  * Hoefs, M. J. L. et al. Ether lipids of planktonic archaea in the marine water column. _Appl. Environ. Microb._ 63, 3090–3095 (1997). CAS 

Google Scholar  * Aluwihare, L. I. & Repeta, D. J. A comparison of the chemical characteristics of oceanic DOM and extracellular DOM produced by marine algae. _Mar. Ecol. Prog. Ser._

186, 105–117 (1999). Article  CAS  Google Scholar  * Gruber, D. F., Simjouw, J. P., Seitzinger, S. P. & Taghon, G. L. Dynamics and characterization of refractory dissolved organic matter

produced by a pure bacterial culture in an experimental predator-prey system. _Appl. Environ. Microb._ 72, 4184–4191 (2006). Article  CAS  Google Scholar  * Ogawa, H., Amagai, Y., Koike,

I., Kaiser, K. & Benner, R. Production of refractory dissolved organic matter by bacteria. _Science_ 292, 917–920 (2001). Article  CAS  PubMed  Google Scholar  * Yamashita, Y. &

Tanoue, E. Production of bio-refractory fluorescent dissolved organic matter in the ocean interior. _Nature Geosci._ 1, 579–582 (2008). Article  CAS  Google Scholar  * Hertkorn, N. et al.

Characterization of a major refractory component of marine dissolved organic matter. _Geochim. Cosmochim. Acta_ 70, 2990–3010 (2006). Article  CAS  Google Scholar  * Koch, B. P., Witt, M.

R., Engbrodt, R., Dittmar, T. & Kattner, G. Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron

resonance mass spectrometry. _Geochim. Cosmochim. Acta_ 69, 3299–3308 (2005). Article  CAS  Google Scholar  * Yamada, N. & Tanoue, E. Detection and partial characterization of dissolved

glycoproteins in oceanic waters. _Limnol. Oceanogr._ 48, 1037–1048 (2003). Article  CAS  Google Scholar  * Kaiser, K. & Benner, R. Major bacterial contribution to the ocean reservoir of

detrital organic carbon and nitrogen. _Limnol. Oceanogr._ 53, 99–112 (2008). Article  CAS  Google Scholar  * McCarthy, M. D., Hedges, J. I. & Benner, R. Major bacterial contribution to

marine dissolved organic nitrogen. _Science_ 281, 231–234 (1998). Article  CAS  PubMed  Google Scholar  * Benner, R. & Kaiser, K. Abundance of amino sugars and peptidoglycan in marine

particulate and dissolved organic matter. _Limnol. Oceanogr._ 48, 118–128 (2003). Article  CAS  Google Scholar  * Wakeham, S. G., Pease, T. K. & Benner, R. Hydroxy fatty acids in marine

dissolved organic matter as indicators of bacterial membrane material. _Org. Geochem._ 34, 857–868 (2003). Article  CAS  Google Scholar  * Stoderegger, K. & Herndl, G. J. Production and

release of bacterial capsular material and its subsequent utilization by marine bacterioplankton. _Limnol. Oceanogr._ 43, 877–884 (1998). Article  CAS  Google Scholar  * Nagata, T. &

Kirchman, D. L. in _Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology_ (eds Bell, C. R., Brylinsky, M. & Johnson-Green, P.) 153–158

(Atlantic Canada Society for Microbial Ecology, Halifax, Canada, 1999). Google Scholar  * Brussaard, C. P. D. et al. Global-scale processes with a nanoscale drive: the role of marine

viruses. _ISME J._ 2, 575–578 (2008). Article  CAS  PubMed  Google Scholar  * Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Viruses play critical roles in the

structure and function of aquatic food webs. _Bioscience_ 49, 781–788 (1999). Article  Google Scholar  * Karner, M. & Herndl, G. J. Extracelluar enzymatic activity and secondary

production in free-living and marine-snow-associated bacteria. _Mar. Biol._ 113, 341–347 (1992). CAS  Google Scholar  * Smith, D. C., Simon, M., Alldredge, A. L. & Azam, F. Intense

hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. _Nature_ 359, 139–142 (1992). Article  CAS  Google Scholar  * Strom, S. L., Benner, R.,

Ziegler, S. & Dagg, M. J. Planktonic grazers are a potentially important source of marine dissolved organic carbon. _Limnol. Oceanogr._ 42, 1364–1374 (1997). Article  CAS  Google Scholar

  * Benner, R. & Biddanda, B. Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth. _Limnol. Oceanogr._ 43, 1373–1378 (1998).

Article  CAS  Google Scholar  * Kieber, R. J., Hydro, L. H. & Seaton, P. J. Photooxidation of triglycerides and fatty acids in seawater: implication toward the formation of marine humic

substances. _Limnol. Oceanogr._ 42, 1454–1462 (1997). Article  CAS  Google Scholar  * Dittmar, T. & Paeng, J. A heat-induced molecular signature in marine dissolved organic matter.

_Nature Geosci._ 2, 175–179 (2009). Article  CAS  Google Scholar  * Ogawa, H. & Tanoue, E. Dissolved organic matter in oceanic waters. _J. Oceanogr._ 59, 129–147 (2003). Article  CAS 

Google Scholar  * Clark, L. L., Ingall, E. D. & Benner, R. Marine phosphorus is selectively remineralized. _Nature_ 393, 426–426 (1998). Article  CAS  Google Scholar  * Hansell, D. A.,

Carlson, C. A., Repeta, D. J. & Schlitzer, R. Dissolved organic matter in the ocean. A controversy stimulates new insights. _Oceanography_ 22, 52–61 (2009). Article  Google Scholar  *

Hedges, J. I. Global biogeochemical cycles: progress and problems. _Mar. Chem._ 39, 67–93 (1992). Article  CAS  Google Scholar  * Falkowski, P. et al. The global carbon cycle: a test of our

knowledge of earth as a system. _Science_ 290, 291–296 (2000). Article  CAS  PubMed  Google Scholar  * Chapman, M. R. & Shackleton, N. J. Evidence of 550-year and 1000-year cyclicities

in North Atlantic circulation patterns during the Holocene. _Holocene_ 10, 287–291 (2000). Article  Google Scholar  * Primeau, F. Characterizing transport between the surface mixed layer and

the ocean interior with a forward and adjoint global ocean transport model. _J. Phys. Oceanogr._ 35, 545–564 (2005). Article  Google Scholar  * Bartley, J. K. & Kah, L. C. Marine carbon

reservoir, Corg-Ccarb coupling, and the evolution of the Proterozoic carbon cycle. _Geology_ 32, 129–132 (2004). Article  CAS  Google Scholar  * Rothman, D. H., Hayes, J. M. & Summons,

R. E. Dynamics of the Neoproterozoic carbon cycle. _Proc. Natl Acad. Sci. USA_ 100, 8124–8129 (2003). Article  CAS  PubMed  PubMed Central  Google Scholar  * McFadden, K. A. et al. Pulsed

oxidation and biological evolution in the Ediacaran Doushantuo Formation. _Proc. Natl Acad. Sci. USA_ 105, 3197–3202 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * Hedges,

I. J. & Keil, R. G. Sedimentary organic matter preservation: an assessment and speculative synthesis. _Mar. Chem._ 49, 81–115 (1995). Article  CAS  Google Scholar  * Prentice, I. C. et

al. in _Climate Change 2001: The Scientific Basis_ (eds Houghton, J. T. et al.) 183–238 (Cambridge Univ. Press, Cambridge, UK, 2001). Google Scholar  * Engel, A., Thoms, S., Riebesell, U.,

Rochelle-Newall, E. & Zondervan, I. Polysaccharide aggregation as a potential sink of marine dissolved organic carbon. _Nature_ 428, 929–932 (2004). Article  CAS  PubMed  Google Scholar

  * Azam, F. & Long, R. A. Oceanography — sea snow microcosms. _Nature_ 414, 495–498 (2001). Article  CAS  PubMed  Google Scholar  * Hansell, D. A. & Carlson, C. A. Biogeochemistry

of total organic carbon and nitrogen in the Sargasso Sea: control by convective overturn. _Deep-Sea Res. II_ 48, 1649–1667 (2001). Article  CAS  Google Scholar  * Brophy, J. E. &

Carlson, D. J. Production of biologically refractory dissolved organic carbon by natural seawater microbial populations. _Deep-Sea Res. I_ 36, 497–507 (1989). Article  CAS  Google Scholar  *

Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. _Nature_ 437, 681–686 (2005). Article  CAS  PubMed  Google Scholar

  * Guo, L., Tanaka, T., Wang, D., Tanaka, N. & Murata, A. Distribution, speciation and stable isotope composition of organic matter in the southeastern Bering Sea. _Mar. Chem._ 91,

211–226 (2004). Article  CAS  Google Scholar  * Laws, E. A., Falkowski, P. G., Smith, W. O., Ducklow, H. & McCarthy, J. J. Temperature effects on export production in the open ocean.

_Global Biogeochem. Cy._ 14, 1231–1246 (2000). Article  CAS  Google Scholar  * Buesseler, K. O. et al. Revisiting carbon flux through the ocean's twilight zone. _Science_ 316, 567–570

(2007). Article  CAS  PubMed  Google Scholar  * Carlson, C. A., Ducklow, H. W., Hansell, D. A. & Smith, W. O. Organic carbon partitioning during spring phytoplankton blooms in the Ross

Sea polynya and the Sargasso Sea. _Limnol. Oceanogr._ 43, 375–386 (1998). Article  CAS  Google Scholar  * Carlson, C. A., Hansell, D. A., Peltzer, E. T. & Smith, W. O. Stocks and

dynamics of dissolved and particulate organic matter in the southern Ross Sea, Antarctica. _Deep-Sea Res. II_ 47, 3201–3225 (2000). Article  CAS  Google Scholar  * Manganelli, M. et al.

Major role of microbes in carbon fluxes during austral winter in the Southern Drake Passage. _PLoS ONE_ 4, e6941 (2009). Article  PubMed  PubMed Central  CAS  Google Scholar  * Druffel, E.

R. M. & Williams, P. M. Identification of a deep marine source of particulate organic carbon using bomb 14C. _Nature_ 347, 172–174 (1990). Article  CAS  Google Scholar  * Joos, F.,

Plattner, G. K., Stocker, T. F., Marchal, O. & Schmittner, A. Global warming and marine carbon cycle feedbacks an future atmospheric CO2 . _Science_ 284, 464–467 (1999). Article  CAS 

PubMed  Google Scholar  * Wohlers, J. et al. Changes in biogenic carbon flow in response to sea surface warming. _Proc. Natl Acad. Sci. USA_ 106, 7067–7072 (2009). Article  CAS  PubMed 

PubMed Central  Google Scholar  * Engel, A. et al. Effects of CO2 on particle size distribution and phytoplankton abundance during a mesocosm bloom experiment (PeECE II). _Biogeosciences_ 5,

509–521 (2008). Article  CAS  Google Scholar  * Jiao, N., Zhang, F. & Hong, N. Significant roles of bacteriochlorophylla supplemental to chlorophylla in the ocean. _ISME J._ 4, 595–597

(2010). Article  CAS  PubMed  Google Scholar  * Kirchman, D. L., Dittel, A. I., Findlay, S. E. G. & Fischer, D. Changes in bacterial activity and community structure in response to

dissolved organic matter in the Hudson River, New York. _Aquat. Microb. Ecol._ 35, 243–257 (2004). Article  Google Scholar  * Koch, B. P., Ludwichowski, K. U., Kattner, G., Dittmar, T. &

Witt, M. Advanced characterization of marine dissolved organic matter by combining reversed-phase liquid chromatography and FT-ICR-MS. _Mar. Chem._ 111, 233–241 (2008). Article  CAS  Google

Scholar  * Wu, L., Kellogg, L., Devol, A. H., Tiedje, J. M. & Zhou, J. Microarray-based characterization of microbial community functional structure and heterogeneity in marine

sediments from the gulf of Mexico. _Appl. Environ. Microb._ 74, 4516–4529 (2008). Article  CAS  Google Scholar  * Frias-Lopez, J. et al. Microbial community gene expression in ocean surface

waters. _Proc. Natl Acad. Sci. USA_ 105, 3805–3810 (2008). Article  CAS  PubMed  PubMed Central  Google Scholar  * DeLong, E. F. et al. Community genomics among stratified microbial

assemblages in the ocean's interior. _Science_ 311, 496–503 (2006). Article  CAS  PubMed  Google Scholar  * Gale, E. F. _The Chemical Activities of Bacteria_ (Academic, New York, 1952).

Google Scholar  * Copley, J. All at sea. _Nature_ 415, 572–574 (2002). Article  PubMed  Google Scholar  * McNichol, A. P. & Aluwihare, L. I. The power of radiocarbon in biogeochemical

studies of the marine carbon cycle: insights from studies of dissolved and particulate organic carbon (DOC and POC). _Chem. Rev._ 107, 443–466 (2007). Article  CAS  PubMed  Google Scholar 

Download references ACKNOWLEDGEMENTS We thank F. Malfatti, D. Ou, C.-T.A. Chen, C. Stedmon, M. Koblizek, X.A. Álvarez-Salgado, R. Sempére, C. Robinson, M. Simon and all Scientific Committee

on Ocean Research (SCOR) WG134 members for their comments and discussions. This work was supported by the National Basic Research Program of China (a pilot 973 project and grant 2007CB815904

to N.J.), the National Natural Science Foundation of China (grant 40632013/40841023 to N.J.), the SOA project (grant 201105021/DY1150243 to N.J.), the Gordon and Betty Moore Foundation

Marine Microbial Initiative (grant to F.A.), the US National Science Foundation (grant 648116 to F.A.; grant 0752972 to D.A.H.; grant 0851113 to S.W.W.; and grant MCB-0453993 to D.L.K.), the

French Science Ministry (the MAORY project, ANR07 BLAN 016 to M.G.W.) and The Netherlands Organisation for Scientific Research–Earth and Life Sciences (grant to G.J.H.). We also thank the

three anonymous reviewers for their valuable comments. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Nianzhi Jiao and Tingwei Luo are at the State Key Laboratory of Marine Environmental

Sciences, Xiamen University, 361005, China., Nianzhi Jiao & Tingwei Luo * Gerhard J. Herndl is at the University of Vienna, Althanstrasse 14, 1090 Vienna, Austria., Gerhard J. Herndl *

Dennis A. Hansell is at the University of Miami's Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, Florida, 331249, USA., Dennis A. Hansell *

Ronald Benner is at the University of South Carolina, Columbia, South Carolina 29208, USA., Ronald Benner * Gerhard Kattner is at the Alfred Wegener Institute for Polar and Marine Research,

Am Handelshafen 12, D-27570 Bremerhaven, Germany., Gerhard Kattner * Steven W. Wilhelm is at The University of Tennessee, 1414 West Cumberland Avenue, Knoxville, Tennessee 37996, USA.,

Steven W. Wilhelm * David L. Kirchman is at the School of Marine Science and Policy, University of Delaware, 222 Cannon Lab, Lewes, Delaware 19958, USA., David L. Kirchman * Markus G.

Weinbauer is at the Laboratoire d'Océanographie de Villefranche, Université Pierre et Marie Curie–Paris 6 and Centre National de la Recherche Scientifique, 06230 Villefranche-sur-Mer,

France., Markus G. Weinbauer * Feng Chen is at the Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, 701 East Pratt Street,

Baltimore, Maryland 21012, USA., Feng Chen * Farooq Azam is at the Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, California 92093,

USA., Farooq Azam Authors * Nianzhi Jiao View author publications You can also search for this author inPubMed Google Scholar * Gerhard J. Herndl View author publications You can also search

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inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Nianzhi Jiao. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. RELATED LINKS

RELATED LINKS FURTHER INFORMATION Nianzhi Jiao's homepage The SCOR WG134 homepage GLOSSARY * Aerobic anoxygenic photoheterotrophic bacteria (AAPB). A group of bacteria that are

primarily heterotrophic but can utilize light energy through bacterial chlorophyll _a_. * Bathypelagic zone The water layer that extends from 1,000 metres to 4,000 metres below the ocean

surface. Sunlight does not reach this zone. * Dissolved organic matter (DOM). Marine organic matter that is less than 0.22 μm in diameter (or, sometimes, 0.7 μm, depending on the filter

used). DOM can be further classified on the basis of biological availability. * Downwelling The sinking of higher-density water beneath lower-density water, such as colder or more saline

water sinking below warmer or fresher surface water. * Euphotic zone The surface water layer of the ocean that is exposed to sufficient sunlight for photosynthesis to occur. This layer

extends from the atmosphere–water interface to a depth at which the light intensity falls to 0.1% of that at the surface. * f-ratio The fraction of total primary production that is fuelled

by new nitrogen (such as nitrate and N2) supplied from outside the euphotic zone, as opposed to that fuelled by regenerated nitrogen (such as ammonium) within the euphotic zone. *

Geobiomolecule A long-lived biologically produced molecule. * Heterotrophic osmotroph An organism requiring DOM for its carbon and energy sources. * Labile DOM (LDOM). A small fraction of

DOM that is present mainly in surface waters and is ready for biological utilization. * Mesopelagic zone Typically between 200 metres and 1,000 metres below the ocean surface. Although some

light penetrates this deep, it is insufficient for photosynthesis. * Microbial loop A pathway in the aquatic food web, whereby DOM is taken up by bacteria and archaea, which are in turn

eaten by protists, and so on up the food chain. * Ocean acidification The ongoing decrease in seawater pH that is caused by the uptake of anthropogenic CO2 by the ocean; CO2 uptake from the

atmosphere is controlled by the difference in partial pressure of CO2 between the air and the sea, as well as by the thermohaline circulation. * Particulate organic matter (POM).

Operationally defined as the material that is retained by a filter with a pore size of 0.22 μm (or, sometimes, 0.7 μm). * Recalcitrant DOM (RDOM). DOM that is resistant to microbial

utilization and that can persist in the ocean interior for up to thousands of years. This is the major fraction of DOM found throughout the entire water column, with an inventory of 624 Gt

C, accounting for more than 95% of the total dissolved organic carbon in the ocean. * Semi-labile DOM (SLDOM). DOM that can be used gradually, over months to years. SLDOM is a small fraction

of the total ocean DOM (∼50 Gt C) and is mainly present in surface waters. * Sloppy feeding Metazoan grazing on phytoplankton, entailing organic matter spill in the form of DOM. *

Solubility pump (SP). A physicochemical process that transports dissolved inorganic carbon from the ocean's surface to its interior. The SP is primarily driven by the solubility of CO2

and the thermohaline circulation. * Thermohaline circulation Also called the ocean conveyor belt, this is the part of the large-scale overturning circulation that is thought to be driven by

the global density gradients caused by temperature and salinity. * Viral shunt Viral lysis of microorganisms, which returns organic carbon from the POM form to the DOM form. RIGHTS AND

PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Jiao, N., Herndl, G., Hansell, D. _et al._ Microbial production of recalcitrant dissolved organic matter: long-term

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