Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux


Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N-acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.

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We appreciate assistance from C Smith and S Roth, and thank N Ivanova for help with IMG database access. Computing resources and technical expertise were provided by the Georgia Genomics and Bioinformatics Core. This work was funded by NSF grants OCE-1342694, OCE-1342699, IOS-1656311 and The Gordon and Betty Moore Foundation grant #5503. This research used resources of the Joint Genome Institute (JGI) and the National Energy Research Scientific Computing Center (NERSC), US Department of Energy Office of Science User Facilities operated under Contract No. DE-AC02-05CH11231.

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ML and MAM conceived of the study and wrote the paper with input from all authors. ML, ASB, BPD, KE, RPK, BN, and AV performed experiments or conducted analyses; TN and SS assembled and analyzed sequence data; ML, RPK, and MAM analyzed data and interpreted findings.

Correspondence to Mary Ann Moran.

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