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Significance of microscale interactions in bacterial ecology and carbon biogeochemistry in the ocean

Abstract

Marine bacteria are important players in regulating the pelagic ecosystem structure and functioning and in biogeochemical cycles of carbon, nitrogen, phosphorus and other bio-elements in the ocean. Although a major role of bacteria in ecosystem function and carbon cycle is well established we still know little about the underlying in situ mechanisms. A fundamental problem concerns the nature and the strength of coupling between bacteria and organic matter. Individual bacteria in seawater must exert their actions on organic matter--mostly polymeric and particulate--at the microscale, e.g. with cell-surface associated hydrolytic enzymes, to create hotspots of growth substrates. Microscale microbial ecology in the pelagic ocean is currently little explored. The general premise of this research is that microscale imaging of in situ interactions, along with ecosystem-level studies of bacteria-mediated carbon cycling, will help constrain hypotheses on the underlying mechanisms and their biogeochemical consequences. Atomic Force Microscopy, epifluorescence microscopy, radiotracers approaches and molecular techniques were used to generate an integrated basis to answer specific questions on nanoscale to microscale ecology of marine bacteria and their implications for ocean-basin-scale-carbon biogeochemistry. Field studies during the summer and winter in the Southern Ocean indicated that the degree of coupling between phytoplankton production and bacteria carbon demand is critically important for ecosystem functioning during the long austral winter when primary production is negligible. We discovered that in the austral winter, in the Drake Passage, a significant amount of dissolved organic carbon produced during the summer supports an active microbial loop with important consequences for ecosystem functioning, carbon cycling and climate. Atomic Force Microscopy combined with Epifluorescence Microscopy enabled us to discover bacteria-bacteria and bacteria-Synechococcus associations--putative symbioses-- in the pelagic ocean. This has implications for primary productivity and nutrient cycling. Further, at the nanometer to micrometer scale a substantial fraction of bacteria generally considered free-living were interconnected within organic matrixes forming bacterial networks suggesting potential for concerted metabolisms and biogeochemical activities as well as a role in marine aggregation. Finally, imaging of live pelagic bacteria by Atomic Force Microscopy provided insights on cell volumes based on measured height unbiased by fixation and drying. The new measurements provide a more reliable basis for quantifying bacteria-mediated carbon fluxes and the role of bacteria in pelagic marine ecosystems.

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