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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.

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Figure 1: Major biological processes involved in carbon cycling in the ocean.
Figure 2: The effects of the microbial carbon pump.
Figure 3: Dynamic interactions between rapid and slow cycles of organic carbon in the ocean.
Figure 4: The major mechanisms for formation of oceanic carbon reservoirs.

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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.

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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.

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Jiao, N., Herndl, G., Hansell, D. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8, 593–599 (2010). https://doi.org/10.1038/nrmicro2386

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