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      Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux

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          Abstract

          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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          Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage

          Bacteria in the 16S rRNA clade SAR86 are among the most abundant uncultivated constituents of microbial assemblages in the surface ocean for which little genomic information is currently available. Bioinformatic techniques were used to assemble two nearly complete genomes from marine metagenomes and single-cell sequencing provided two more partial genomes. Recruitment of metagenomic data shows that these SAR86 genomes substantially increase our knowledge of non-photosynthetic bacteria in the surface ocean. Phylogenomic analyses establish SAR86 as a basal and divergent lineage of γ-proteobacteria, and the individual genomes display a temperature-dependent distribution. Modestly sized at 1.25–1.7 Mbp, the SAR86 genomes lack several pathways for amino-acid and vitamin synthesis as well as sulfate reduction, trends commonly observed in other abundant marine microbes. SAR86 appears to be an aerobic chemoheterotroph with the potential for proteorhodopsin-based ATP generation, though the apparent lack of a retinal biosynthesis pathway may require it to scavenge exogenously-derived pigments to utilize proteorhodopsin. The genomes contain an expanded capacity for the degradation of lipids and carbohydrates acquired using a wealth of tonB-dependent outer membrane receptors. Like the abundant planktonic marine bacterial clade SAR11, SAR86 exhibits metabolic streamlining, but also a distinct carbon compound specialization, possibly avoiding competition.
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            Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea.

            Marine dissolved organic matter (DOM) contains as much carbon as the Earth's atmosphere, and represents a critical component of the global carbon cycle. To better define microbial processes and activities associated with marine DOM cycling, we analyzed genomic and transcriptional responses of microbial communities to high-molecular-weight DOM (HMWDOM) addition. The cell density in the unamended control remained constant, with very few transcript categories exhibiting significant differences over time. In contrast, the DOM-amended microcosm doubled in cell numbers over 27 h, and a variety of HMWDOM-stimulated transcripts from different taxa were observed at all time points measured relative to the control. Transcripts significantly enriched in the HMWDOM treatment included those associated with two-component sensor systems, phosphate and nitrogen assimilation, chemotaxis, and motility. Transcripts from Idiomarina and Alteromonas spp., the most highly represented taxa at the early time points, included those encoding TonB-associated transporters, nitrogen assimilation genes, fatty acid catabolism genes, and TCA cycle enzymes. At the final time point, Methylophaga rRNA and non-rRNA transcripts dominated the HMWDOM-amended microcosm, and included gene transcripts associated with both assimilatory and dissimilatory single-carbon compound utilization. The data indicated specific resource partitioning of DOM by different bacterial species, which results in a temporal succession of taxa, metabolic pathways, and chemical transformations associated with HMWDOM turnover. These findings suggest that coordinated, cooperative activities of a variety of bacterial "specialists" may be critical in the cycling of marine DOM, emphasizing the importance of microbial community dynamics in the global carbon cycle.
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              SAR11 marine bacteria require exogenous reduced sulphur for growth.

              Sulphur is a universally required cell nutrient found in two amino acids and other small organic molecules. All aerobic marine bacteria are known to use assimilatory sulphate reduction to supply sulphur for biosynthesis, although many can assimilate sulphur from organic compounds that contain reduced sulphur atoms. An analysis of three complete 'Candidatus Pelagibacter ubique' genomes, and public ocean metagenomic data sets, suggested that members of the ubiquitous and abundant SAR11 alphaproteobacterial clade are deficient in assimilatory sulphate reduction genes. Here we show that SAR11 requires exogenous sources of reduced sulphur, such as methionine or 3-dimethylsulphoniopropionate (DMSP) for growth. Titrations of the algal osmolyte DMSP in seawater medium containing all other macronutrients in excess showed that 1.5 x 10(8) SAR11 cells are produced per nanomole of DMSP. Although it has been shown that other marine alphaproteobacteria use sulphur from DMSP in preference to sulphate, our results indicate that 'Cand. P. ubique' relies exclusively on reduced sulphur compounds that originate from other plankton.
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                Author and article information

                Journal
                The ISME Journal
                ISME J
                Springer Science and Business Media LLC
                1751-7362
                1751-7370
                June 21 2019
                Article
                10.1038/s41396-019-0455-3
                6776065
                31227817
                1d39cde5-df69-4711-b8e8-609d7c4a77ec
                © 2019

                http://www.springer.com/tdm

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