skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms

Journal Article · · BMC Genomics
 [1];  [2];  [3];  [3];  [3];  [3]
  1. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States); Technical Univ. of Denmark, Lyngby (Denmark)
  3. Univ. of California, Berkeley, CA (United States)

Bacteria of the genus Sulfobacillus are found worldwide as members of microbial communities that accelerate sulfide mineral dissolution in acid mine drainage environments (AMD), acid-rock drainage environments (ARD), as well as in industrial bioleaching operations. Despite their frequent identification in these environments, their role in biogeochemical cycling is poorly understood.Here we report draft genomes of five species of the Sulfobacillus genus (AMDSBA1-5) reconstructed by cultivation-independent sequencing of biofilms sampled from the Richmond Mine (Iron Mountain, CA). Three of these species (AMDSBA2, AMDSBA3, and AMDSBA4) have no cultured representatives while AMDSBA1 is a strain of S. benefaciens, and AMDSBA5 a strain of S. thermosulfidooxidans. We analyzed the diversity of energy conservation and central carbon metabolisms for these genomes and previously published Sulfobacillus genomes. Pathways of sulfur oxidation vary considerably across the genus, including the number and type of subunits of putative heterodisulfide reductase complexes likely involved in sulfur oxidation. The number and type of nickel-iron hydrogenase proteins varied across the genus, as does the presence of different central carbon pathways. Only the AMDSBA3 genome encodes a dissimilatory nitrate reducatase and only the AMDSBA5 and S. thermosulfidooxidans genomes encode assimilatory nitrate reductases. Within the genus, AMDSBA4 is unusual in that its electron transport chain includes a cytochrome bc type complex, a unique cytochrome c oxidase, and two distinct succinate dehydrogenase complexes.Overall, the results significantly expand our understanding of carbon, sulfur, nitrogen, and hydrogen metabolism within the Sulfobacillus genus.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; SC0004665
OSTI ID:
1257382
Alternate ID(s):
OSTI ID: 1579706
Journal Information:
BMC Genomics, Vol. 15, Issue 1; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 48 works
Citation information provided by
Web of Science

References (84)

Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs journal December 2007
UCHIME improves sensitivity and speed of chimera detection journal June 2011
Complete Genome Analysis of Sulfobacillus acidophilus Strain TPY, Isolated from a Hydrothermal Vent in the Pacific Ocean journal September 2011
X-ray Structure of a Self-Compartmentalizing Sulfur Cycle Metalloenzyme journal February 2006
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB journal July 2006
Archaeal complex II: ‘classical‘ and ‘non-classical’ succinate:quinone reductases with unusual features journal January 2002
Genome Data Mining and Soil Survey for the Novel Group 5 [NiFe]-Hydrogenase To Explore the Diversity and Ecological Importance of Presumptive High-Affinity H 2 -Oxidizing Bacteria journal July 2011
Production of Glycolic Acid by Chemolithotrophic Iron- and Sulfur-Oxidizing Bacteria and Its Role in Delineating and Sustaining Acidophilic Sulfide Mineral-Oxidizing Consortia journal November 2009
InterProScan: protein domains identifier journal July 2005
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis journal April 2000
PyNAST: a flexible tool for aligning sequences to a template alignment journal November 2009
Localization, purification and properties of a tetrathionate hydrolase from Acidithiobacillus caldus journal January 2004
Evidence that the potential for dissimilatory ferric iron reduction is widespread among acidophilic heterotrophic bacteria journal February 2008
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer journal November 2007
Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics journal July 2003
Identification of a gene encoding a tetrathionate hydrolase in Acidithiobacillus ferrooxidans journal October 2007
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
UniRef: comprehensive and non-redundant UniProt reference clusters journal March 2007
Thiosulfate Transfer Mediated by DsrE/TusA Homologs from Acidothermophilic Sulfur-oxidizing Archaeon Metallosphaera cuprina journal August 2014
Community-wide analysis of microbial genome sequence signatures journal January 2009
Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium journal May 2006
Identification and characterization of Rhodopseudomonas palustris TIE-1 hopanoid biosynthesis mutants: Hopanoid biosynthesis in R. palustris TIE-1 journal January 2012
Functional, biochemical and genetic diversity of prokaryotic nitrate reductases journal February 2001
Transaldolase/Glucose-6-phosphate Isomerase Bifunctional Enzyme and Ribulokinase as Factors to Increase Xylitol Production from D -Arabitol in Gluconobacter oxydans journal January 2003
Isolation of the Tetrathionate Hydrolase from Thiobacillus Acidophilus journal February 1997
Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations journal August 2008
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data journal May 2011
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation journal October 2006
Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases journal January 2005
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments journal August 2007
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria journal February 2007
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Structure and evolution of cytochrome oxidase journal January 1994
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
DECIPHER, a Search-Based Approach to Chimera Identification for 16S rRNA Sequences journal November 2011
ProtTest: selection of best-fit models of protein evolution journal January 2005
A Cysteine-Rich CCG Domain Contains a Novel [4Fe-4S] Cluster Binding Motif As Deduced from Studies with Subunit B of Heterodisulfide Reductase from Methanothermobacter marburgensis journal November 2007
Anaerobic Sulfur Metabolism Coupled to Dissimilatory Iron Reduction in the Extremophile Acidithiobacillus ferrooxidans journal January 2013
Copper A of Cytochrome c Oxidase, A Novel, Long-Embattled, Biological Electron-Transfer Site journal May 1997
Acidithiobacillus caldus Sulfur Oxidation Model Based on Transcriptome Analysis between the Wild Type and Sulfur Oxygenase Reductase Defective Mutant journal September 2012
Succinate:quinone oxidoreductases: an overview journal January 2002
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 1999
Identification of a New Class of 5'-Adenylylsulfate (APS) Reductases from Sulfate-Assimilating Bacteria journal January 2000
Search and clustering orders of magnitude faster than BLAST journal August 2010
How Signals Are Heard during Bacterial Chemotaxis: Protein-Protein Interactions in Sensory Signal Propagation journal December 2000
Thiol/Disulfide System Plays a Crucial Role in Redox Protection in the Acidophilic Iron-Oxidizing Bacterium Leptospirillum ferriphilum journal September 2012
Comparison of Acid Mine Drainage Microbial Communities in Physically and Geochemically Distinct Ecosystems journal November 2000
Crystal Structure of Sulfide:Quinone Oxidoreductase from Acidithiobacillus ferrooxidans: Insights into Sulfidotrophic Respiration and Detoxification journal April 2010
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth journal April 2012
Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview journal October 2007
New Proteins Involved in Sulfur Trafficking in the Cytoplasm of Allochromatium vinosum journal March 2014
The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. journal July 2003
Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms: Sulfur metabolizing acidophiles journal April 2012
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB journal November 2007
Comparative Genome Analysis Reveals Metabolic Versatility and Environmental Adaptations of Sulfobacillus thermosulfidooxidans Strain ST journal June 2014
Energy-Converting [NiFe] Hydrogenases: More than Just H<sub>2</sub> Activation journal January 2005
Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase journal March 2010
The prokaryotic complex iron–sulfur molybdoenzyme family journal September 2008
Draft Genome Sequence of the Sulfobacillus thermosulfidooxidans Cutipay Strain, an Indigenous Bacterium Isolated from a Naturally Extreme Mining Environment in Northern Chile journal October 2012
Extending the models for iron and sulfur oxidation in the extreme Acidophile Acidithiobacillus ferrooxidans journal January 2009
Microbial communities in acid mine drainage journal May 2003
Heterotrophic Archaea Contribute to Carbon Cycling in Low-pH, Suboxic Biofilm Communities journal September 2012
Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities journal February 2010
A Widely Conserved Gene Cluster Required for Lactate Utilization in Bacillus subtilis and Its Involvement in Biofilm Formation journal February 2009
A simple, fast, and accurate method of phylogenomic inference journal January 2008
Cytoplasmic Sulfurtransferases in the Purple Sulfur Bacterium Allochromatium vinosum: Evidence for Sulfur Transfer from DsrEFH to DsrC journal July 2012
Basic local alignment search tool journal October 1990
QIIME allows analysis of high-throughput community sequencing data journal April 2010
New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. MicroReview journal May 2000
Formation of Flat Lamellar Intramembrane Lipid Structures in Microorganisms journal March 2001
The Presence of an Iron-Sulfur Cluster in Adenosine 5′-Phosphosulfate Reductase Separates Organisms Utilizing Adenosine 5′-Phosphosulfate and Phosphoadenosine 5′-Phosphosulfate for Sulfate Assimilation journal April 2002
In Situ Evolutionary Rate Measurements Show Ecological Success of Recently Emerged Bacterial Hybrids journal April 2012
A Membrane-bound Multienzyme, Hydrogen-oxidizing, and Sulfur-reducing Complex from the Hyperthermophilic Bacterium Aquifex aeolicus journal October 2005
Clostridium neopropionicum sp. nov., a strict anaerobic bacterium fermenting ethanol to propionate through acrylate pathway journal February 1992
MUSCLE: multiple sequence alignment with high accuracy and high throughput journal March 2004
Swinging Arms and Swinging Domains in Multifunctional Enzymes: Catalytic Machines for Multistep Reactions journal June 2000
The Evolution of Respiratory Chain Complex I from a Smaller Last Common Ancestor Consisting of 11 Protein Subunits journal May 2011
Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H 2 Storage journal June 2010
Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide journal May 2009
Site-specific mutagenesis and functional analysis of active sites of sulfur oxygenase reductase from Gram-positive moderate thermophile Sulfobacillus acidophilus TPY journal December 2013
Purification and Characterization of Sulfide:Quinone Oxidoreductase from an Acidophilic Iron-Oxidizing Bacterium, Acidithiobacillus ferrooxidans journal November 2007
Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase: Thiosulphate oxidoreductase from Acidianus ambivalens journal July 2004
Anaerobic Respiration Using Fe3+, S0, and H2 in the Chemolithoautotrophic Bacterium Acidithiobacillus ferrooxidans journal April 2002

Cited By (1)

Structure and Diversity of the Bacterial Communities in the Acid and Thermophilic Crater-Lake of the Volcano “El Chichón”, Mexico journal October 2018