Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Peatland Acidobacteria with a dissimilatory sulfur metabolism

Journal Article · · The ISME Journal
 [1];  [2];  [2];  [2];  [3];  [2];  [4];  [2];  [3];  [2];  [5];  [4];  [2];  [2];  [2];  [6];  [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)

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.

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, Journal Name: The ISME Journal Journal Issue: 7 Vol. 12; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (101)

Elemental sulfur as an intermediate of sulfide oxidation with oxygen byDesulfobulbus propionicus journal August 1995
Archaeoglobus fulgidus gen. nov., sp. nov.: a New Taxon of Extremely Thermophilic Archaebacteria journal March 1988
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 journal February 2015
Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs journal January 2010
Thermoanaerobaculum aquaticum gen. nov., sp. nov., the first cultivated member of Acidobacteria subdivision 23, isolated from a hot spring journal June 2013
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 journal August 2016
Racemase activity effected by two dehydrogenases in sulfolactate degradation by Chromohalobacter salexigens: purification of (S)-sulfolactate dehydrogenase journal December 2009
Membrane-bound oxygen reductases of the anaerobic sulfate-reducing Desulfovibrio vulgaris Hildenborough: roles in oxygen defence and electron link with periplasmic hydrogen oxidation journal October 2013
Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens journal September 2003
High unique diversity of sulfate-reducing prokaryotes characterized in a depth gradient in an acidic fen journal May 2007
Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a,c -diamide synthase, for sulphur oxidation journal August 2006
Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis journal September 2016
Microbial Diversity in Anaerobic Sediments at Río Tinto, a Naturally Acidic Environment with a High Heavy Metal Content journal July 2011
Microorganisms with Novel Dissimilatory (Bi)Sulfite Reductase Genes Are Widespread and Part of the Core Microbiota in Low-Sulfate Peatlands journal December 2010
pH Gradient-Induced Heterogeneity of Fe(III)-Reducing Microorganisms in Coal Mining-Associated Lake Sediments journal November 2008
Isolation and Characterization of Soil Bacteria That Define Terriglobus gen. nov., in the Phylum Acidobacteria journal February 2007
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils journal February 2009
Distinct Anaerobic Bacterial Consumers of Cellobiose-Derived Carbon in Boreal Fens with Different CO 2 /CH 4 Production Ratios journal December 2016
Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate journal July 2017
Accelerated Profile HMM Searches journal October 2011
A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea journal January 2011
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features text January 2013
Stable isotope probing of amino sugars - a promising tool to assess microbial interactions in soils: Stable isotope probing of amino sugars journal May 2013
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton journal September 2000
Sulfur Metabolism in Phototrophic Bacteria book February 2017
Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate-reducing bacteria journal July 1992
Fructose degradation byDesulfovibrio sp. in pure culture and in coculture withMethanospirillum hungatei journal September 1986
Elemental sulfur as an intermediate of sulfide oxidation with oxygen byDesulfobulbus propionicus journal August 1995
Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review journal October 2008
Thermotomaculum hydrothermale gen. nov., sp. nov., a novel heterotrophic thermophile within the phylum Acidobacteria from a deep-sea hydrothermal vent chimney in the Southern Okinawa Trough journal January 2012
Archaeoglobus fulgidus gen. nov., sp. nov.: a New Taxon of Extremely Thermophilic Archaebacteria journal March 1988
Crystal Structure of Dissimilatory Sulfite Reductase D (DsrD) Protein—Possible Interaction with B- and Z-DNA by Its Winged-Helix Motif journal September 2003
A Post-Genomic View of the Ecophysiology, Catabolism and Biotechnological Relevance of Sulphate-Reducing Prokaryotes book January 2015
Cytochrome bd oxidase and bacterial tolerance to oxidative and nitrosative stress journal July 2014
The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism journal July 2014
Microbial activity and community structure in two drained fen soils in the Ljubljana Marsh journal September 2006
Impact of experimental drought and rewetting on redox transformations and methanogenesis in mesocosms of a northern fen soil journal June 2009
Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms journal September 2012
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases journal October 2014
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival journal September 2015
Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms journal March 2016
Uncultivated microbes in need of their own taxonomy journal July 2017
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes journal May 2013
Three decades of global methane sources and sinks journal September 2013
Fast gapped-read alignment with Bowtie 2 journal March 2012
Identity of major sulfur-cycle prokaryotes in freshwater lake ecosystems revealed by a comprehensive phylogenetic study of the dissimilatory adenylylsulfate reductase journal November 2016
Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon journal July 2015
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features journal November 2013
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences journal November 2015
Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria journal August 2009
Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria, and emended description of Acidobacterium capsulatum Kishimoto et al. 1991
  • Pankratov, T. A.; Kirsanova, L. A.; Kaparullina, E. N.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 62, Issue 2, p. 430-437 https://doi.org/10.1099/ijs.0.029629-0
journal April 2011
Bryocella elongata gen. nov., sp. nov., a member of subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. 2008 journal May 2011
Aridibacter famidurans gen. nov., sp. nov. and Aridibacter kavangonensis sp. nov., two novel members of subdivision 4 of the Acidobacteria isolated from semiarid savannah soil journal February 2014
Paludibaculum fermentans gen. nov., sp. nov., a facultative anaerobe capable of dissimilatory iron reduction from subdivision 3 of the Acidobacteria journal May 2014
Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system journal January 2011
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
Temperature impacts differentially on the methanogenic food web of cellulose-supplemented peatland soil: Differential temperature effects on peat microbes journal June 2014
Identification of proteins capable of metal reduction from the proteome of the Gram-positive bacterium D esulfotomaculum reducens  MI-1 using an NADH-based activity assay : Metal reductases from Gram-positive metal reducer journal January 2015
Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface journal July 2015
Microbial community composition and in silico predicted metabolic potential reflect biogeochemical gradients between distinct peatland types journal September 2014
The life sulfuric: microbial ecology of sulfur cycling in marine sediments: Microbial sulfur cycling in marine sediments journal May 2017
Microbial diversity in alpine tundra wet meadow soil: novel Chloroflexi from a cold, water-saturated environment journal August 2006
Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria – evolution of the Sox sulfur oxidation enzyme system journal December 2007
Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat: Cellulose degradation in acidic peat journal May 2011
Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria: Candidatus Chloracidobacterium thermophilum genome journal September 2011
Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils journal April 2012
A common pathway of sulfide oxidation by sulfate-reducing bacteria journal November 1996
Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea journal November 2009
A protein trisulfide couples dissimilatory sulfate reduction to energy conservation journal December 2015
Microbial Diversity in Anaerobic Sediments at Río Tinto, a Naturally Acidic Environment with a High Heavy Metal Content journal July 2011
Influence of Plant Polymers on the Distribution and Cultivation of Bacteria in the Phylum Acidobacteria journal November 2010
pH Gradient-Induced Heterogeneity of Fe(III)-Reducing Microorganisms in Coal Mining-Associated Lake Sediments journal December 2007
Microorganisms with Novel Dissimilatory (Bi)Sulfite Reductase Genes Are Widespread and Part of the Core Microbiota in Low-Sulfate Peatlands journal December 2010
Comparison of the Levels of Bacterial Diversity in Freshwater, Intertidal Wetland, and Marine Sediments by Using Millions of Illumina Tags journal September 2012
Acidobacteria Phylum Sequences in Uranium-Contaminated Subsurface Sediments Greatly Expand the Known Diversity within the Phylum journal March 2007
Isolation and Characterization of Soil Bacteria That Define Terriglobus gen. nov., in the Phylum Acidobacteria journal February 2007
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils journal February 2009
A Comparative Quantitative Proteomic Study Identifies New Proteins Relevant for Sulfur Oxidation in the Purple Sulfur Bacterium Allochromatium vinosum journal January 2014
Microarray and Functional Gene Analyses of Sulfate-Reducing Prokaryotes in Low-Sulfate, Acidic Fens Reveal Cooccurrence of Recognized Genera and Novel Lineages journal December 2004
Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes journal March 2006
Phylogenetic Analysis and In Situ Identification of Bacteria Community Composition in an Acidic Sphagnum Peat Bog journal March 2006
Novel Genes of the dsr Gene Cluster and Evidence for Close Interaction of Dsr Proteins during Sulfur Oxidation in the Phototrophic Sulfur Bacterium Allochromatium vinosum journal February 2005
Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate journal July 2017
Bypassing Cultivation To Identify Bacterial Species: Culture-independent genomic approaches identify credibly distinct clusters, avoid cultivation bias, and provide true insights into microbial species journal March 2014
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Pyrosequencing-Based Assessment of the Bacteria Diversity in Surface and Subsurface Peat Layers of a Northern Wetland, with Focus on Poorly Studied Phyla and Candidate Divisions journal May 2013
Global Methane Budget 2000-2012 dataset January 2016
Cultivating Uncultured Bacteria from Northern Wetlands: Knowledge Gained and Remaining Gaps journal January 2011
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change journal January 2012
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences text January 2016
Microbial reduction of iron and porewater biogeochemistry in acidic peatlands journal January 2008

Cited By (13)

Long-Term Transcriptional Activity at Zero Growth of a Cosmopolitan Rare Biosphere Member journal February 2019
The Response of Microbial Communities to Peatland Drainage and Rewetting. A Review journal October 2020
Formation of Large Native Sulfur Deposits Does Not Require Molecular Oxygen text January 2019
Additional file 2 of Specialized metabolic functions of keystone taxa sustain soil microbiome stability dataset January 2021
Additional file 3 of Specialized metabolic functions of keystone taxa sustain soil microbiome stability dataset January 2021
Additional file 4 of Specialized metabolic functions of keystone taxa sustain soil microbiome stability dataset January 2021
Differential responses of the acidobacterial community in the topsoil and subsoil to fire disturbance in Pinus tabulaeformis stands journal December 2019
Beyond the tip of the iceberg; a new view of the diversity of sulfite- and sulfate-reducing microorganisms journal May 2018
Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O journal February 2019
DsrL mediates electron transfer between NADH and rDsrAB in Allochromatium vinosum journal December 2019
The Active Sulfate-Reducing Microbial Community in Littoral Sediment of Oligotrophic Lake Constance journal February 2019
Shotgun Metagenomics Reveals the Benthic Microbial Community Response to Plastic and Bioplastic in a Coastal Marine Environment journal June 2019
Glacial Runoff Promotes Deep Burial of Sulfur Cycling-Associated Microorganisms in Marine Sediments journal November 2019

Similar Records

Redox states of Desulfovibrio vulgaris DsrC, a key protein in dissimilatory sulfite reduction
Journal Article · Thu Nov 28 23:00:00 EST 2013 · Biochemical and Biophysical Research Communications · OSTI ID:22242203

Redox states of Desulfovibrio vulgaris DsrC, a key protein in dissimilatory sulfite reduction
Journal Article · Thu Nov 28 23:00:00 EST 2013 · Biochemical and Biophysical Research Communications, 441(4):731-736 · OSTI ID:1114105