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  1. 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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  2. Dimethylsulfoniopropionate (DMSP) is produced by many species of marine phytoplankton and has been reported to provide a variety of beneficial functions including osmoregulation. Dinoflagellates are recognized as majorDMSPproducers; however, accumulation has been shown to be highly variable in this group. We explored the effect of hyposaline transfer inGambierdiscus belizeanusbetween ecologically relevant salinities (36 and 31) onDMSPaccumulation, Chla, cell growth, and cell volume, over 12 d. Our results showed thatG. belizeanusmaintained an intracellularDMSPcontent of 16.3 pmol cell−1and concentration of 139 mMin both salinities. Although this intracellular concentration was near the median reported for other dinoflagellates, the cellular content achieved byG. belizeanuswas the highest reported of any dinoflagellate thus far, owing mainly to its large size.DMSPlevels were not significantly affected by salinity treatment but did change over time during the experiment. Salinity, however, did have a significant effect on the ratio ofDMSP:Chla, suggesting that salinity transfer ofG. belizeanusinduced a physiological response other thanDMSPadjustment. A survey ofDMSPcontent in a variety ofGambierdiscusspecies and strains revealed relatively highDMSPconcentrations (1.0–16.4 pmol cell−1) as well as high intrageneric and intraspecific variation. We conclude that, althoughDMSPmay not be involved in long‐term (3–12 d) osmoregulation in this species,G. belizeanusand otherGambierdiscusspecies may be important contributors toDMSPproduction in tropical benthic microalgal communities due to their large size and high cellular content.

     
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  3. Abstract

    Metagenomic and metatranscriptomic time-series data covering a 52-day period in the fall of 2016 provide an inventory of bacterial and archaeal community genes, transcripts, and taxonomy during an intense dinoflagellate bloom in Monterey Bay, CA, USA. The dataset comprises 84 metagenomes (0.8 terabases), 82 metatranscriptomes (1.1 terabases), and 88 16S rRNA amplicon libraries from samples collected on 41 dates. The dataset also includes 88 18S rRNA amplicon libraries, characterizing the taxonomy of the eukaryotic community during the bloom. Accompanying the sequence data are chemical and biological measurements associated with each sample. These datasets will facilitate studies of the structure and function of marine bacterial communities during episodic phytoplankton blooms.

     
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  4. Abstract

    The organic sulfur compound dimethylsulfoniopropionate (DMSP) is synthesized by numerous species of marine phytoplankton, and its volatile degradation products are a major source of biogenic sulfur to the atmosphere. A massive bloom of the dinoflagellateAkashiwo sanguineaoccurred in Monterey Bay, CA, USA, in the fall of 2016 and led to exceptionally high seawater DMSP concentrations that peaked at 4,240 nM. Bacterial consumption rates showed that only a small fraction of the DMSP standing stock flowed through the dissolved DMSP pool per day, contributing to the high DMSP concentrations and creating conditions conducive to production of dimethylsulfide (DMS). Conservative calculations of DMS yield from this persistentA. sanguineabloom suggest substantial regional‐scale inputs of DMS‐sulfur to the atmosphere. Other recently reported major coastal blooms ofA. sanguinea, along with indications that this species may benefit from climate change conditions, reveal a mechanism that could alter oceanic contributions to atmospheric sulfur pools.

     
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  5. Summary

    Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur metabolite produced by many phytoplankton species and degraded by bacteria via two distinct pathways with climate‐relevant implications. We assessed the diversity and abundance of bacteria possessing these pathways in the context of phytoplankton community composition over a 3‐week time period spanning September–October, 2014 in Monterey Bay, CA. ThedmdAgene from the DMSP demethylation pathway dominated the DMSP gene pool and was harboured mostly by members of the alphaproteobacterial SAR11 clade and secondarily by the Roseobacter group, particularly during the second half of the study. Novel members of the DMSP‐degrading community emerged fromdmdAsequences recovered from metagenome assemblies and single‐cell sequencing, including largely uncharacterized gammaproteobacteria and alphaproteobacteria taxa. In the DMSP cleavage pathway, the SAR11 genedddKwas the most abundant early in the study, but was supplanted bydddPover time. SAR11 members, especially those harbouring genes for both DMSP degradation pathways, had a strong positive relationship with the abundance of dinoflagellates, and DMSP‐degrading gammaproteobacteria co‐occurred with haptophytes. Thisin situstudy of the drivers of DMSP fate in a coastal ecosystem demonstrates for the first time correlations between specific groups of bacterial DMSP degraders and phytoplankton taxa.

     
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