Molecular mechanisms involved in prokaryotic cycling of labile dissolved organic matter in the sea

Abstract: Roughly half of the global primary production originates from microscopic phytoplankton in marine ecosystems, converting carbon dioxide into organic matter. This organic matter pool consists of a myriad of compounds that fuel heterotrophic bacterioplankton. However, knowledge of the molecular mechanisms – particularly the metabolic pathways involved in the degradation and utilization of dissolved organic matter (DOM) – and transcriptional dynamics over spatiotemporal gradients are still scarce. Therefore, we studied the molecular mechanisms of bacterioplankton communities, including archaea, involved in the cycling of DOM, over different spatiotemporal scales in experiments and through field observations.In seawater experiments, we found a divergence of bacterioplankton transcriptional responses to different organic matter compound classes (carbohydrates, nucleic acids, and proteins) and condensation states (monomers or polymers). These responses were associated with distinct bacterial taxa, suggesting pronounced functional partitioning of these compounds in the Sea. Baltic Proper mesocosms amended with two different river loadings (forest versus agriculture river water) revealed a divergence in gene expression patterns between treatments during bloom decay. This was particularly true for genes in phosphorus and nitrogen metabolism, highlighting the importance and sensitivity of interaction effects between river- and phytoplankton-derived DOM in regulating bacterial activity responses to changes in precipitation-induced riverine runoff.In shipboard mesocosms in an Atlantic coastal upwelling system, we found significant changes in bacterioplankton transcription of hydrolyzing enzymes and membrane transporters from phytoplankton bloom development to senescence, primarily driven by phytoplankton-derived DOM and dissolved organic carbon dynamics. These responses differed substantially between bacterial orders, suggesting that functional resource partitioning is dynamically structured by temporal changes in DOM quantity and quality. Further analysis of these gene systems in a stratified fjord revealed pronounced divergence in transcription with depth and between bacterial taxa; moreover, transcription was more variable in the surface waters. This highlights the interplay between functional and physical partitioning of biogeochemical cycles. Collectively, the findings in this thesis contribute novel insights into the interdependency between prokaryotes and DOM by shedding light on the mechanisms involved in DOM cycling over ecologically relevant spatiotemporal scales.

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