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Title: 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 » facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2]; ORCiD logo [3];  [2];  [4];  [2]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [5]; ORCiD logo [4];  [2];  [2];  [2];  [6]; ORCiD logo [2]
  1. Univ. of Vienna, Vienna (Austria); Univ. of Konstanz, Konstanz (Germany)
  2. Univ. of Vienna, Vienna (Austria)
  3. Aalborg Univ., Aalborg (Denmark)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Univ. of Florida, Davie, FL (United States)
  6. 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:
Journal Article: 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. 2018. "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},
url = {https://www.osti.gov/biblio/1543737}, journal = {The ISME Journal},
issn = {1751-7362},
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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Cited by: 71 works
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Microorganisms with Novel Dissimilatory (Bi)Sulfite Reductase Genes Are Widespread and Part of the Core Microbiota in Low-Sulfate Peatlands
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A Comparative Quantitative Proteomic Study Identifies New Proteins Relevant for Sulfur Oxidation in the Purple Sulfur Bacterium Allochromatium vinosum
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pH Gradient-Induced Heterogeneity of Fe(III)-Reducing Microorganisms in Coal Mining-Associated Lake Sediments
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A ‘rare biosphere’ microorganism contributes to sulfate reduction in a peatland
journal, June 2010


Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes
journal, June 2012


Measurement of bacterial replication rates in microbial communities
journal, November 2016


Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction
journal, October 2006


Erosion of functional independence early in the evolution of a microbial mutualism
journal, September 2014


Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging
journal, August 2015


MicroScope in 2017: an expanding and evolving integrated resource for community expertise of microbial genomes
journal, November 2016


Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer
journal, October 1999


Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium
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Thermoanaerobaculum aquaticum gen. nov., sp. nov., the first cultivated member of Acidobacteria subdivision 23, isolated from a hot spring
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Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils
journal, September 2013


The first representative of the globally widespread subdivision 6 Acidobacteria, Vicinamibacter silvestris gen. nov., sp. nov., isolated from subtropical savannah soil
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Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens
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High unique diversity of sulfate-reducing prokaryotes characterized in a depth gradient in an acidic fen
journal, May 2007


Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis
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pH Gradient-Induced Heterogeneity of Fe(III)-Reducing Microorganisms in Coal Mining-Associated Lake Sediments
journal, November 2008


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DsrL mediates electron transfer between NADH and rDsrAB in Allochromatium vinosum
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The Active Sulfate-Reducing Microbial Community in Littoral Sediment of Oligotrophic Lake Constance
journal, February 2019


Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O
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Beyond the tip of the iceberg; a new view of the diversity of sulfite- and sulfate-reducing microorganisms
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Glacial Runoff Promotes Deep Burial of Sulfur Cycling-Associated Microorganisms in Marine Sediments
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The Response of Microbial Communities to Peatland Drainage and Rewetting. A Review
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Formation of Large Native Sulfur Deposits Does Not Require Molecular Oxygen
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