Peatland Acidobacteria with a dissimilatory sulfur metabolism

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2018
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Hausmann, Bela
Pelikan, Claus
Herbold, Craig W.
Köstlbacher, Stephan
Albertsen, Mads
Eichorst, Stephanie A.
Glavina del Rio, Tijana
Huemer, Martin
Nielsen, Per H.
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The ISME Journal. 2018, 12(7), pp. 1729-1742. ISSN 1751-7362. eISSN 1751-7370. Available under: doi: 10.1038/s41396-018-0077-1
Zusammenfassung

Sulfur-cycling microorganisms impact organic matter decomposition in wetlands and consequently greenhouse gas emissions from these globally relevant environments. However, their identities and physiological properties are largely unknown. By applying a functional metagenomics approach to an acidic peatland, we recovered draft genomes of seven novel Acidobacteria species with the potential for dissimilatory sulfite (dsrAB, dsrC, dsrD, dsrN, dsrT, dsrMKJOP) or sulfate respiration (sat, aprBA, qmoABC plus dsr genes). Surprisingly, the genomes also encoded DsrL, which so far was only found in sulfur-oxidizing microorganisms. Metatranscriptome analysis demonstrated expression of acidobacterial sulfur-metabolism genes in native peat soil and their upregulation in diverse anoxic microcosms. This indicated an active sulfate respiration pathway, which, however, might also operate in reverse for dissimilatory sulfur oxidation or disproportionation as proposed for the sulfur-oxidizing Desulfurivibrio alkaliphilus. Acidobacteria that only harbored genes for sulfite reduction additionally encoded enzymes that liberate sulfite from organosulfonates, which suggested organic sulfur compounds as complementary energy sources. Further metabolic potentials included polysaccharide hydrolysis and sugar utilization, aerobic respiration, several fermentative capabilities, and hydrogen oxidation. Our findings extend both, the known physiological and genetic properties of Acidobacteria and the known taxonomic diversity of microorganisms with a DsrAB-based sulfur metabolism, and highlight new fundamental niches for facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.

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ISO 690HAUSMANN, Bela, Claus PELIKAN, Craig W. HERBOLD, Stephan KÖSTLBACHER, Mads ALBERTSEN, Stephanie A. EICHORST, Tijana GLAVINA DEL RIO, Martin HUEMER, Per H. NIELSEN, Michael PESTER, 2018. Peatland Acidobacteria with a dissimilatory sulfur metabolism. In: The ISME Journal. 2018, 12(7), pp. 1729-1742. ISSN 1751-7362. eISSN 1751-7370. Available under: doi: 10.1038/s41396-018-0077-1
BibTex
@article{Hausmann2018-06Peatl-45136,
  year={2018},
  doi={10.1038/s41396-018-0077-1},
  title={Peatland Acidobacteria with a dissimilatory sulfur metabolism},
  number={7},
  volume={12},
  issn={1751-7362},
  journal={The ISME Journal},
  pages={1729--1742},
  author={Hausmann, Bela and Pelikan, Claus and Herbold, Craig W. and Köstlbacher, Stephan and Albertsen, Mads and Eichorst, Stephanie A. and Glavina del Rio, Tijana and Huemer, Martin and Nielsen, Per H. and Pester, Michael}
}
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    <dcterms:abstract xml:lang="eng">Sulfur-cycling microorganisms impact organic matter decomposition in wetlands and consequently greenhouse gas emissions from these globally relevant environments. However, their identities and physiological properties are largely unknown. By applying a functional metagenomics approach to an acidic peatland, we recovered draft genomes of seven novel Acidobacteria species with the potential for dissimilatory sulfite (dsrAB, dsrC, dsrD, dsrN, dsrT, dsrMKJOP) or sulfate respiration (sat, aprBA, qmoABC plus dsr genes). Surprisingly, the genomes also encoded DsrL, which so far was only found in sulfur-oxidizing microorganisms. Metatranscriptome analysis demonstrated expression of acidobacterial sulfur-metabolism genes in native peat soil and their upregulation in diverse anoxic microcosms. This indicated an active sulfate respiration pathway, which, however, might also operate in reverse for dissimilatory sulfur oxidation or disproportionation as proposed for the sulfur-oxidizing Desulfurivibrio alkaliphilus. Acidobacteria that only harbored genes for sulfite reduction additionally encoded enzymes that liberate sulfite from organosulfonates, which suggested organic sulfur compounds as complementary energy sources. Further metabolic potentials included polysaccharide hydrolysis and sugar utilization, aerobic respiration, several fermentative capabilities, and hydrogen oxidation. Our findings extend both, the known physiological and genetic properties of Acidobacteria and the known taxonomic diversity of microorganisms with a DsrAB-based sulfur metabolism, and highlight new fundamental niches for facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.</dcterms:abstract>
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