Peatland Acidobacteria with a dissimilatory sulfur metabolism
Abstract
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 formore »
- Authors:
-
[1];
[3];
[3];
[2];
[5];
[4];
[2]
- Univ. of Vienna, Vienna (Austria); Univ. of Konstanz, Konstanz (Germany)
- Univ. of Vienna, Vienna (Austria)
- Aalborg Univ., Aalborg (Denmark)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Univ. of Florida, Davie, FL (United States)
- Univ. of Konstanz, Konstanz (Germany); Leibniz Inst. DSMZ, Braunschweig (Germany)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )
- OSTI Identifier:
- 1543737
- Alternate Identifier(s):
- OSTI ID: 1646840
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 12; Journal Issue: 7; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Environmental Sciences & Ecology; Microbiology
Citation Formats
Hausmann, Bela, Pelikan, Claus, Herbold, Craig W., Köstlbacher, Stephan, Albertsen, Mads, Eichorst, Stephanie A., Glavina del Rio, Tijana, Huemer, Martin, Nielsen, Per H., Rattei, Thomas, Stingl, Ulrich, Tringe, Susannah G., Trojan, Daniela, Wentrup, Cecilia, Woebken, Dagmar, Pester, Michael, and Loy, Alexander. Peatland Acidobacteria with a dissimilatory sulfur metabolism. United States: N. p., 2018.
Web. doi:10.1038/s41396-018-0077-1.
Hausmann, Bela, Pelikan, Claus, Herbold, Craig W., Köstlbacher, Stephan, Albertsen, Mads, Eichorst, Stephanie A., Glavina del Rio, Tijana, Huemer, Martin, Nielsen, Per H., Rattei, Thomas, Stingl, Ulrich, Tringe, Susannah G., Trojan, Daniela, Wentrup, Cecilia, Woebken, Dagmar, Pester, Michael, & Loy, Alexander. Peatland Acidobacteria with a dissimilatory sulfur metabolism. United States. https://doi.org/10.1038/s41396-018-0077-1
Hausmann, Bela, Pelikan, Claus, Herbold, Craig W., Köstlbacher, Stephan, Albertsen, Mads, Eichorst, Stephanie A., Glavina del Rio, Tijana, Huemer, Martin, Nielsen, Per H., Rattei, Thomas, Stingl, Ulrich, Tringe, Susannah G., Trojan, Daniela, Wentrup, Cecilia, Woebken, Dagmar, Pester, Michael, and Loy, Alexander. Fri .
"Peatland Acidobacteria with a dissimilatory sulfur metabolism". United States. https://doi.org/10.1038/s41396-018-0077-1. https://www.osti.gov/servlets/purl/1543737.
@article{osti_1543737,
title = {Peatland Acidobacteria with a dissimilatory sulfur metabolism},
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 Rattei, Thomas and Stingl, Ulrich and Tringe, Susannah G. and Trojan, Daniela and Wentrup, Cecilia and Woebken, Dagmar and Pester, Michael and Loy, Alexander},
abstractNote = {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.},
doi = {10.1038/s41396-018-0077-1},
journal = {The ISME Journal},
number = 7,
volume = 12,
place = {United States},
year = {Fri Feb 23 00:00:00 EST 2018},
month = {Fri Feb 23 00:00:00 EST 2018}
}
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