Microbial control of the dark end of the biological pump

Abstract

A fraction of the carbon captured by phytoplankton in the sunlit surface ocean sinks to depth as dead organic matter and faecal material. The microbial breakdown of this material in the subsurface ocean generates carbon dioxide. Collectively, this microbially mediated flux of carbon from the atmosphere to the ocean interior is termed the biological pump. In recent decades it has become clear that the composition of the phytoplankton community in the surface ocean largely determines the quantity and quality of organic matter that sinks to depth. This settling organic matter, however, is not sufficient to meet the energy demands of microbes in the dark ocean. Two additional sources of organic matter have been identified: non-sinking organic particles of debated origin that escape capture by sediment traps and exhibit stable concentrations throughout the dark ocean, and microbes that convert inorganic carbon into organic matter. Whether these two sources can together account for the significant mismatch between organic matter consumption and supply in the dark ocean remains to be seen. It is clear, however, that the microbial community of the deep ocean works in a fundamentally different way from surface water communities.In the sunlit surface waters of the ocean, phytoplankton convert carbon dioxide into particulate organic carbon. A significant fraction of this newly produced particulate organic carbon is remineralized-that is, respired back to carbon dioxide-in these surface waters. However, about 1 to 40% of the photosynthetically fixed carbon is exported into the dark realm of the ocean where it is remineralized at substantially slower rates than in surface waters 1 . The resultant increase in dissolved inorganic carbon concentrations towards the interior of the ocean, coined the biological pump, is regulated by food web processes such as grazing.Non-living particles, termed 'marine snow' 2-4 , transport organic matter to depth in the ocean. These particles comprise decaying phytoplankton, faecal matter generated by zooplankton, the most abundant multicellular organisms in the oceanic water column, and aggregates of high-molecular-weight dissolved organic matter released by phytoplankton in the senescent stage of blooms, or as a result of an imbalance in nutrient supply ratios 5,6 . The aggregation of high-molecular-weight dissolved organic matter, largely in the form of © 2013 Macmillan Publishers Limited. All rights reserved * Correspondence and requests for materials should be addressed to G.J.H. gerhard.herndl@univie.ac.at. Competing financial interestsThe authors declare no competing financial interests. Additional informationReprints and permissions information is available online at www.nature.com/reprints. Europe PMC Funders GroupAuthor Manuscript Nat Geosci. Author manuscript; available in PMC 2014 April 02. Published in final edited form as:Nat Geosci. 2013 September 1; 6(9): 718-724. doi:10.1038/ngeo1921. Europe PMC Funders Author ManuscriptsEurope PMC Funders Author Manuscripts polysacchari...

Deciphering associations between dissolved organic molecules and bacterial communities in a pelagic marine system

“…Water at depths between 100 and 350 m was enriched in TDN presumably due to the lack of active autotrophs and dominance of remineralization processes of sinking particles at these depths (Shaffer, 1996;Herndl and Reinthaler, 2013). During our sampling campaign, however, no extensive phytoplankton blooms were detected.…”

Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years

“…Particle flux, which varies seasonally in magnitude and composition (Collins et al, 2011), likely contributes to the observed seasonality at 890 m, which is at the bottom of the water column. Particles are believed to be the source of key substrates for bacteria in the deep ocean and likely transport organic nutrients from the surface to the bottom, where they may become entrained in the nepheloid layer or land on the sea floor, degrade and affect nearby overlying waters (Francois et al, 2002;Herndl and Reinthaler, 2013). Therefore, the longer residence time of particles and their associated organic matter at or near the sea floor, compared with mid-water, likely leads to stronger seasonality there.…”

“…However, relatively little is known about whether these characteristics are consistent with or influence subsurface microbial communities, especially those below the euphotic zone. The mesopelagic region is of great biogeochemical interest, as it is the site of much of the Earth's carbon remineralization (Aristegui et al, 2009;Herndl and Reinthaler, 2013), as well as the nitrogen (Zehr and Ward, 2002) and sulfur cycles (Canfield et al, 2010), particularly in oxygen minimum zones that are found in association with coastal upwelling (Wright et al, 2012). The San Pedro Ocean Time Series (SPOT) provides an opportunity to study the entire water column, from surface to mesopelagic, in a coastal seasonal upwelling system that includes an oxygen minimum at the bottom of the water column.…”

Hadal biosphere: Insight into the microbial ecosystem in the deepest ocean on Earth

“…However, it has recently been revealed that the deep-sea biogeochemical cycles are more complex than previously expected and that the mismatch between the organic carbon supply and microbial heterotrophic demand has led to imbalances in some oceans (1-4). Currently, the contribution of chemolithoautotrophy and mixotrophy to the biogeochemical cycle (e.g., dark carbon fixation coupled with nitrification and sulfur oxidations) is also recognized as another significant organic carbon source in the dark ocean (3,5,6). It has been estimated that the dissolved inorganic carbon fixation in the dark ocean by these organisms could be on the same order-of-magnitude as heterotrophic biomass production (3,5).…”