Peatland Acidobacteria with a dissimilatory sulfur metabolism

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

doi:10.1038/s41396-018-0077-1

Title: Peatland Acidobacteria with a dissimilatory sulfur metabolism

Journal Article · Fri Feb 23 00:00:00 EST 2018 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-018-0077-1· OSTI ID:1543737

^[1]; Pelikan, Claus ^[2]; Herbold, Craig W. ^[2]; Köstlbacher, Stephan ^[2];

^[3]; Eichorst, Stephanie A. ^[2]; Glavina del Rio, Tijana ^[4]; Huemer, Martin ^[2];

^[3];

^[2];

^[5];

^[4]; Trojan, Daniela ^[2]; Wentrup, Cecilia ^[2]; Woebken, Dagmar ^[2]; Pester, Michael ^[6];

^[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)

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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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1543737

Alternate ID(s):: OSTI ID: 1646840

Journal Information:: The ISME Journal, Vol. 12, Issue 7; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 71 works

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eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Jaime, Huerta-Cepas,; Damian, Szklarczyk,; Kristoffer, Forslund, Oxford University Press https://doi.org/10.5167/uzh-120037	text	January 2016
Elemental sulfur as an intermediate of sulfide oxidation with oxygen byDesulfobulbus propionicus Fuseler, Knut; Cypionka, Heribert Archives of Microbiology, Vol. 164, Issue 2 https://doi.org/10.1007/bf02525315	journal	August 1995
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A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00069	journal	January 2011

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The Active Sulfate-Reducing Microbial Community in Littoral Sediment of Oligotrophic Lake Constance Wörner, Susanne; Pester, Michael Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00247	journal	February 2019
Shotgun Metagenomics Reveals the Benthic Microbial Community Response to Plastic and Bioplastic in a Coastal Marine Environment Pinnell, Lee J.; Turner, Jeffrey W. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01252	journal	June 2019
Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O Coskun, Ömer K.; Özen, Volkan; Wankel, Scott D. The ISME Journal, Vol. 13, Issue 6 https://doi.org/10.1038/s41396-019-0373-4	journal	February 2019
Beyond the tip of the iceberg; a new view of the diversity of sulfite- and sulfate-reducing microorganisms Vigneron, Adrien; Cruaud, Perrine; Alsop, Eric The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-018-0155-4	journal	May 2018
Glacial Runoff Promotes Deep Burial of Sulfur Cycling-Associated Microorganisms in Marine Sediments Pelikan, Claus; Jaussi, Marion; Wasmund, Kenneth Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02558	journal	November 2019
The Response of Microbial Communities to Peatland Drainage and Rewetting. A Review Kitson, Ezra; Bell, Nicholle G. A. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.582812	journal	October 2020
Formation of Large Native Sulfur Deposits Does Not Require Molecular Oxygen L., Labrado, Amanda; Benjamin, Brunner,; M., Bernasconi, Stefano ETH Zurich https://doi.org/10.3929/ethz-b-000323373	text	January 2019
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