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Title: Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle

Journal Article · · The ISME Journal
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [6];  [7];  [8]; ORCiD logo [2];  [5]; ORCiD logo [9]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  2. Univ. of Vienna (Austria). Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry meets Microbiology
  3. Univ. of Southern California, Los Angeles, CA (United States). Center for Dark Energy Biosphere Investigations; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  5. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States)
  6. Univ. of Toronto, ON (Canada). Dept. of Civil Engineering
  7. Univ. of Hawaii, Manoa, Kaneohe, HI (United States). Hawaii Inst. of Marine Biology
  8. Leibniz Inst. DSMZ, Braunschweig (Germany). Dept. of Microorganisms, and German Collection of Microorganisms and Cell Cultures
  9. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States), and Dept. of Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences

A critical step in the biogeochemical cycle of sulfur on Earth is microbial sulfate reduction, yet organisms from relatively few lineages have been implicated in this process. Previous studies using functional marker genes have detected abundant, novel dissimilatory sulfite reductases (DsrAB) that could confer the capacity for microbial sulfite/sulfate reduction but were not affiliated with known organisms. Thus, the identity of a significant fraction of sulfate/sulfite-reducing microbes has remained elusive. Here we report the discovery of the capacity for sulfate/sulfite reduction in the genomes of organisms from 13 bacterial and archaeal phyla, thereby more than doubling the number of microbial phyla associated with this process. Eight of the 13 newly identified groups are candidate phyla that lack isolated representatives, a finding only possible given genomes from metagenomes. Organisms from Verrucomicrobia and two candidate phyla, Candidatus Rokubacteria and Candidatus Hydrothermarchaeota, contain some of the earliest evolved dsrAB genes. The capacity for sulfite reduction has been laterally transferred in multiple events within some phyla, and a key gene potentially capable of modulating sulfur metabolism in associated cells has been acquired by putatively symbiotic bacteria. We conclude that current functional predictions based on phylogeny significantly underestimate the extent of sulfate/sulfite reduction across Earth's ecosystems. Understanding the prevalence of this capacity is integral to interpreting the carbon cycle because sulfate reduction is often coupled to turnover of buried organic carbon. Our findings expand the diversity of microbial groups associated with sulfur transformations in the environment and motivate revision of biogeochemical process models based on microbial community composition.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1478346
Journal Information:
The ISME Journal, Vol. 12, Issue 7; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 203 works
Citation information provided by
Web of Science

References (75)

Sulfur Oxidation Genes in Diverse Deep-Sea Viruses journal May 2014
Domain Evolution and Functional Diversification of Sulfite Reductases journal February 2005
The CIPRES science gateway: a community resource for phylogenetic analyses conference January 2011
The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism journal July 2014
Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum journal January 2016
Syntrophism Among Prokaryotes book January 2013
Corrosion by the Sulphate-reducing Bacteria journal October 1971
Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes journal February 2009
The I-TASSER Suite: protein structure and function prediction journal December 2014
Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids journal March 2017
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes journal May 2012
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
The TIGRFAMs database of protein families journal January 2003
The Archean Sulfur Cycle and the Early History of Atmospheric Oxygen journal April 2000
A Multicomponent Protein Complex Mediates Environmental Stress Signaling in Bacillus subtilis journal July 2004
Ocean biogeochemistry modeled with emergent trait-based genomics journal November 2017
Unusual biology across a group comprising more than 15% of domain Bacteria journal June 2015
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
Noisy: Identification of problematic columns in multiple sequence alignments journal January 2008
The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1 : Dissimilatory sulfite reduction by the octahaem SirA journal August 2010
A new view of the tree of life journal April 2016
Cytoplasmic Sulfurtransferases in the Purple Sulfur Bacterium Allochromatium vinosum: Evidence for Sulfur Transfer from DsrEFH to DsrC journal July 2012
The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough journal April 2004
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
Revisiting the dissimilatory sulfate reduction pathway: Revisiting the dissimilatory sulfate reduction pathway journal August 2011
Dissimilatory ATP sulfurylase from the hyperthermophilic sulfate reducer Archaeoglobus fulgidus belongs to the group of homo-oligomeric ATP sulfurylases journal May 1998
Regulation of Dissimilatory Sulfur Oxidation in the Purple Sulfur Bacterium Allochromatium Vinosum journal January 2011
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Pfam: the protein families database journal November 2013
UniProt: a hub for protein information journal October 2014
Mineralization of organic matter in the sea bed—the role of sulphate reduction journal April 1982
A Genomic Perspective on Protein Families journal October 1997
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases journal October 2014
Multiple Lateral Transfers of Dissimilatory Sulfite Reductase Genes between Major Lineages of Sulfate-Reducing Prokaryotes journal October 2001
Characterization of anaerobic sulfite reduction by Salmonella typhimurium and purification of the anaerobically induced sulfite reductase. journal June 1989
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge? journal August 2002
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating journal June 2009
Isotopic evidence for microbial sulphate reduction in the early Archaean era journal March 2001
Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO 2 concentrations : Genomic resolution of a high-CO journal July 2016
Disguised as a Sulfate Reducer: Growth of the Deltaproteobacterium Desulfurivibrio alkaliphilus by Sulfide Oxidation with Nitrate journal July 2017
Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments journal March 2017
The life sulfuric: microbial ecology of sulfur cycling in marine sediments: Microbial sulfur cycling in marine sediments journal May 2017
The octahaem MccA is a haem c–copper sulfite reductase journal February 2015
Sulfur Isotope Effects of Dissimilatory Sulfite Reductase journal December 2015
Crystal Structure of Dissimilatory Sulfite Reductase D (DsrD) Protein—Possible Interaction with B- and Z-DNA by Its Winged-Helix Motif journal September 2003
Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes journal August 2006
Search and clustering orders of magnitude faster than BLAST journal August 2010
Commensal Bacteria, Redox Stress, and Colorectal Cancer: Mechanisms and Models journal July 2004
Accelerated Profile HMM Searches journal October 2011
Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5'-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes - origin and evolution of the dissimilatory sulfate-reduction pathway journal July 2007
Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms journal March 2016
Evolutionary timing of the origins of mesophilic sulphate reduction and oxygenic photosynthesis: a phylogenomic dating approach journal January 2004
Structural Insights into Inhibition of Bacillus anthracis Sporulation by a Novel Class of Non-heme Globin Sensor Domains journal January 2011
Sulfur globule oxidation in green sulfur bacteria is dependent on the dissimilatory sulfite reductase system journal January 2011
Identification and characterization of a bacterial hydrosulphide ion channel journal March 2012
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center journal June 2015
Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities journal May 2014
Microbiological disproportionation of inorganic sulfur compounds journal August 2008
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change journal January 2012
Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulfate-reducing, fermentative, and sulfide-oxidizing bacteria. journal January 1996
Phylogeny of Dissimilatory Sulfite Reductases Supports an Early Origin of Sulfate Respiration journal June 1998
The CIPRES science gateway: enabling high-impact science for phylogenetics researchers with limited resources
  • Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
  • Proceedings of the 1st Conference of the Extreme Science and Engineering Discovery Environment on Bridging from the eXtreme to the campus and beyond - XSEDE '12 https://doi.org/10.1145/2335755.2335836
conference January 2012
Occurrence, Classification, and Biological Function of Hydrogenases: An Overview journal December 2007
Syntrophism among Prokaryotes book January 2006
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis journal September 2020
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies text January 2014
A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774 journal August 2003
Metaproteomics reveal that rapid perturbations in organic matter prioritize functional restructuring over taxonomy in western Arctic Ocean microbiomes journal September 2019
Mating pair stabilization mediates bacterial conjugation species specificity journal June 2022
New Family of Regulators in the Environmental Signaling Pathway Which Activates the General Stress Transcription Factor  B of Bacillus subtilis journal February 2001
Clustered Genes Related to Sulfate Respiration in Uncultured Prokaryotes Support the Theory of Their Concomitant Horizontal Transfer journal September 2005
A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea journal January 2011

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The Active Sulfate-Reducing Microbial Community in Littoral Sediment of Oligotrophic Lake Constance journal February 2019
The Biogeochemical Sulfur Cycle of Marine Sediments journal April 2019
Shotgun Metagenomics Reveals the Benthic Microbial Community Response to Plastic and Bioplastic in a Coastal Marine Environment journal June 2019
Dietary Factors in Sulfur Metabolism and Pathogenesis of Ulcerative Colitis journal April 2019
Accurate and complete genomes from metagenomes journal March 2020
Glacial Runoff Promotes Deep Burial of Sulfur Cycling-Associated Microorganisms in Marine Sediments journal November 2019
Highlight: Contribution of Ultra-Small Microbes to Global Carbon Cycles journal May 2019
Shotgun metagenomic sequencing from Manao-Pee cave, Thailand, reveals insight into the microbial community structure and its metabolic potential journal June 2019
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Formation of Large Native Sulfur Deposits Does Not Require Molecular Oxygen text January 2019