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Studies on microbial sulfur cycling in marine sediment have primarily centered on the cycling of inorganic sulfur. The microbial diversity underlying the cycling of organosulfur compounds is largely unexplored. In this study, we present the first quantification of dissolved organic sulfur (DOS) microbial assimilation in marine surface sediments using 13C-DOS quantitative DNA stable isotope probing (qSIP). We sampled marine sediment from 493 m water depth on the Puerto Rico continental slope, measured 13C-assimilation from two DOS substrates (13C-taurine and 13C-methionine), and compared the 13C-DOS assimilation to 13C-glucose uptake. Taurine utilization was confined to bacteria, whereas methionine was degraded by bacteria and archaea, including methanogenic Methanococcoides. Globally widespread uncultivated clades of Gammaproteobacteria and Deltaproteobacteria were the main drivers of DOS cycling and exhibited increased assimilation of carbon from taurine and methionine, compared to glucose. Only one operational taxonomic unit (OTU) affiliated with Neptuniibacter was found to assimilate taurine and methionine, but not glucose, implying that microbes exclusively utilizing both DOS substrates as a carbon source in marine sediments are rare. Still, a substantial number of bacterial taxa exhibited a higher assimilation of 13C from taurine or methionine, compared to glucose, indicating their preference for both DOS substrates over glucose as a carbon source in the sediment. These results represent the first quantitative assessment of organosulfur cycling from taurine and methionine by uncultivated microbes in a marine benthic environment.
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Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux
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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- Award ID(s):
- 1656311
- PAR ID:
- 10485628
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 13
- Issue:
- 10
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 2536-2550
- Size(s):
- p. 2536-2550
- Sponsoring Org:
- National Science Foundation
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