Abstract
The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry and nuclear magnetic resonance using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N-acetyl-d-glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate.
Highlights
The marine dissolved organic carbon (DOC) reservoir plays two critical roles in the global carbon cycle
Identification of ecologically relevant exometabolites was carried out in co-culture systems in which marine phytoplankter T. pseudonana CCMP1335 served as the sole carbon source for three bacterial strains
SKA14, and P. dokdonensis MED152 were individually inoculated into a T. pseudonana culture that had accumulated exometabolites over 7 days
Summary
The marine dissolved organic carbon (DOC) reservoir plays two critical roles in the global carbon cycle. Three marine bacterial taxa have consistently been found associated with microphytoplankton in natural marine environments and phytoplankton cultures, and are thought to dominate processing of recently-fixed carbon using genes that allow them to quickly respond to transient nutrient pulses [23]. Members of these three groups, the Rhodobacterales, Gammaproteobacteria, and Flavobacteriales, appear to specialize on different components of bioreactive DOC [11, 23,24,25]. Both biological vetting strategies relied on bacterial activity to spotlight compounds within a complex pool of dilute metabolites that were likely supporting bacterial heterotrophy
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