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Microbial Production of Recalcitrant Dissolved Organic Matter

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Microbial Production of Recalcitrant Dissolved Organic Matter View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Xiamen University Institutional Repository PERSPECTIVES as the dominant heterotrophic osmotrophs, OPINION they essentially monopolize the utilization of DOM. The diverse adaptive strategies of Microbial production of recalcitrant microorganisms for using newly fixed carbon are well known. However, there are dissolved organic matter: long-term large gaps in our knowledge of how these microorganisms interact with the large pool of DOM that seems to be recalcitrant. The carbon storage in the global ocean relationship of microorganisms with this RDOM pool is not well explored, despite Nianzhi Jiao, Gerhard J. Herndl, Dennis A. Hansell, Ronald Benner, great progress in our understanding of Gerhard Kattner, Steven W. Wilhelm, David L. Kirchman, Markus G. Weinbauer, the genomic diversity of marine microor- Tingwei Luo, Feng Chen and Farooq Azam ganisms and their in situ processes. The interaction between this RDOM pool and microorganisms is important, as DOM mol- 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 ecules that are not degraded for extended particles or as dissolved organic matter. The fate of most of this exported material periods of time constitute carbon storage. In this Opinion article, we propose the is remineralization to CO , which accumulates in deep waters until it is eventually 2 microbial carbon pump as a conceptual ventilated again at the sea surface. However, a proportion of the fixed carbon is not framework to address the role of microbial mineralized but is instead stored for millennia as recalcitrant dissolved organic generation of RDOM and relevant carbon matter. The processes and mechanisms involved in the generation of this large storage, with the aim of improving our carbon reservoir are poorly understood. Here, we propose the microbial carbon understanding of oceanic carbon cycling pump as a conceptual framework to address this important, multifaceted and global climate change. biogeochemical problem. Marine organic matter Although organic matter in marine envi- The biogeochemical fate of organic matter in thermohaline circulation2. A small fraction of ronments occupies a molecular-size the ocean is an important issue that must be POM escapes mineralization and reaches continuum10,11, in research practice it is considered in order to understand the role of the sediment, where organic carbon can be operationally divided into POM and DOM. the ocean in climate change. The biological buried and stored for thousands and even POM is initially formed as autotrophic pump involves a series of processes through millions of years1–3. The long-term storage of biomass and is then transformed through which CO2 is fixed as organic matter by carbon by the biological pump is the primary multiple trophic pathways at each level of photosynthesis and then transferred to the concern regarding the role of the ocean in cli- the marine food web12,13. There are many ocean interior, resulting in the temporary or mate change. The efficiency of the biological mechanisms of DOM production in the permanent storage of carbon1–3. The known pump is currently regarded as a basic measure upper ocean, and they vary spatially and mechanisms involved in the biological of the ocean’s ability to store biologically fixed temporally. It is difficult to specify or predict pump include the sedimentation of carbon. However, in our opinion the produc- the dominant sources of DOM in a given particulate organic matter (POM) from surface tion and fate of the large pool of recalcitrant ecological scenario. Phytoplankton release a waters towards the seabed1 and the export DOM (RDOM) in the oceanic water column highly variable, but at times substantial, frac- of dissolved organic matter (DOM) from the has not been adequately considered in the tion of primary production into seawater as euphotic zone to deeper waters2,3 by mixing biological pump concept. DOM14–16. Another notable mechanism is the and downwelling of water parcels. Both POM Marine bacteria and archaea are respon- release of DOM resulting from viral lysis8. and DOM are subject to microbial minerali- sible for the respiration of most of the ‘Sloppy feeding’ by metazoan grazers might zation, and most of the organic carbon will carbon that sinks into the ocean’s depths5. also release phytoplankton cytosol as DOM, be returned to dissolved inorganic carbon Consequently, these microorganisms and and the egesta of protists and metazoa can (DIC) within a few decades4. Together, these their interactions with organic matter have contain DOM. Further, a major mechanism processes remove organic-form carbon from received much attention recently, and sev- of DOM production is POM solubilization the surface waters and convert it to DIC at eral excellent reviews have been published by bacterial and archaeal ectohydrolases17. greater depths, maintaining the surface-to- on this topic6–9. One fundamental aspect deep-ocean gradient of DIC and resulting of the interaction between these bacterial The lability of DOM in the temporary storage of carbon until and archaeal species and organic matter It has been difficult to elucidate the it is ventilated to the surface again by the sets them apart from other ocean biota: biochemical interactions between NATURE REVIEWS | MICROBIOLOGY VOLUME 8 | AUGUST 2010 | 593 © 2010 Macmillan Publishers Limited. All rights reserved PERSPECTIVES Generation of RDOM Biological Phytoplankton Determining the sources, mechanisms and pump rates of RDOM generation are intriguing Zooplankton problems. Empirical tests of RDOM genera- M tion from a particular source (for example, a DO Viral Microbial shunt pool of LDOM or SLDOM) become logisti- loop cally impractical if RDOM is defined only in acter B ia terms of its extremely long half-life. In fact, A the half-life of RDOM varies over a con- s r Metabolism c e POM h s tinuum; carbon storage in RDOM molecules flux a ru ea Vi with a half-life of 50–100 years is a shorter storage period than average but is still rel- 1 2 3 evant to climate models, and measuring the M Microbial production of such molecules in experimen- RDO carbon pump tal systems would be more tractable than for molecules with a half-life of 1,000 years. A promising approach is to experimentally demonstrate the production of molecular species that are known to persist as DOM for long periods29. In a 36-day incubation, Pseudomonas chlororaphis depleted the sole carbon source, d-glucose, within 2 days and generated >100 DOM compounds that contained carbon from this glucose. Approximately 3–5% of the glucose-derived carbon persisted until the end of the experi- Figure 1 | Major biological processes involved in carbon cycling in the ocean. The main biologi- 30 cal processes are shown. The biological pump is a process whereby CO in the upper ocean is fixed by ment . Year-long experiments exposing 2 Nature Reviews | Microbiology primary producers and transported to the deep ocean as sinking biogenic particles (particulate DOM to natural assemblages of pelagic organic matter; POM) or as dissolved organic matter (DOM). The microbial loop is a pathway in the bacteria might minimize the LDOM and aquatic food web whereby DOM is taken up by bacteria and archaea, which are consumed by protists, SLDOM ‘noise’ sufficiently to allow identi- which are in turn consumed by metazoans (not shown). The viral shunt reflects virus-mediated lysis of fication of the sources and mechanisms of microorganisms, which returns the POM to the DOM pool. The proposed microbial carbon pump is a RDOM production. In a 1-year incubation conceptual framework for understanding the role of microbial processes in the production of recalci- with pelagic marine bacteria assemblages trant DOM (RDOM). RDOM can persist in the ocean for millennia and is therefore a reservoir for car- and either d-glucose or l-glutamate, bon storage in the ocean. Three major pathways have been identified in the microbial carbon pump: direct exudation of microbial cells during production and proliferation (path 1); viral lysis of microbial ~37% and ~50%, respectively, of the gener- cells to release microbial cell wall and cell surface macromolecules (path 2); and POM degradation ated DOM persisted until the end of the 31 (path 3). The grey shading roughly indicates the total flux of carbon metabolism in the water column. incubation , indicating that bacteria can generate long-lived DOM efficiently. In the deep sea, the fact that microbial RDOM microorganisms and DOM. For the present photoheterotrophic bacteria (AAPB), which generation occurs can be inferred from the discussion, it is useful to recognize the mainly inhabit the euphotic zone, were increase in fluorescent DOM as a function operational classification of DOM into found to be less versatile in utilizing diverse of increasing oxygen consumption32. three categories according to biological organic matter25 than most other bacterial Although <10% of marine DOM has been availability: labile DOM (LDOM), semi-labile groups. By contrast, microorganisms in the chemically characterized to date, thousands DOM (SLDOM) and recalcitrant DOM bathypelagic zone have developed metabolic of organic molecules (that is, their mass (RDOM)18–20. LDOM can be used by het- strategies to adapt to the low reactivity of formulas) have been identified33,34. Several erotrophic microorganisms within days or deep-sea DOM19. For instance, high ectoen- molecular species derived from bacteria, even hours21,22, whereas SLDOM can persist zymatic activity in deep waters26 has been such as porins35, d-amino acids (specifically, for months to years and accounts for most of suggested to enable deep-sea microorgan- d-alanine, d-serine, d-aspartate and d-gluta- the DOM that is exported from the euphotic isms to utilize organic moieties from resist- mate36,37), muramic acid36,38 and lipopoly- zone to greater depths.
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