DOE PAGES 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

Abstract

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 electronmore » 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.« less

Authors:
 [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)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1257382
Alternate Identifier(s):
OSTI ID: 1579706
Grant/Contract Number:  
AC02-05CH11231; SC0004665
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Justice, Nicholas B., Norman, Anders, Brown, Christopher T., Singh, Andrea, Thomas, Brian C., and Banfield, Jillian F. Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. United States: N. p., 2014. Web. doi:10.1186/1471-2164-15-1107.
Justice, Nicholas B., Norman, Anders, Brown, Christopher T., Singh, Andrea, Thomas, Brian C., & Banfield, Jillian F. Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. United States. https://doi.org/10.1186/1471-2164-15-1107
Justice, Nicholas B., Norman, Anders, Brown, Christopher T., Singh, Andrea, Thomas, Brian C., and Banfield, Jillian F. Mon . "Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms". United States. https://doi.org/10.1186/1471-2164-15-1107. https://www.osti.gov/servlets/purl/1257382.
@article{osti_1257382,
title = {Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms},
author = {Justice, Nicholas B. and Norman, Anders and Brown, Christopher T. and Singh, Andrea and Thomas, Brian C. and Banfield, Jillian F.},
abstractNote = {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.},
doi = {10.1186/1471-2164-15-1107},
journal = {BMC Genomics},
number = 1,
volume = 15,
place = {United States},
year = {Mon Dec 15 00:00:00 EST 2014},
month = {Mon Dec 15 00:00:00 EST 2014}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 48 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs
journal, December 2007

  • Tabita, F. R.; Hanson, T. E.; Li, H.
  • Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4
  • DOI: 10.1128/MMBR.00015-07

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

  • Li, B.; Chen, Y.; Liu, Q.
  • Journal of Bacteriology, Vol. 193, Issue 19
  • DOI: 10.1128/JB.05684-11

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

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Archaeal complex II: ‘classical‘ and ‘non-classical’ succinate:quinone reductases with unusual features
journal, January 2002

  • Schäfer, Günter; Anemüller, Stefan; Moll, Ralf
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1553, Issue 1-2
  • DOI: 10.1016/S0005-2728(01)00232-8

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

  • Constant, Philippe; Chowdhury, Soumitra Paul; Hesse, Laura
  • Applied and Environmental Microbiology, Vol. 77, Issue 17
  • DOI: 10.1128/AEM.00673-11

InterProScan: protein domains identifier
journal, July 2005

  • Quevillon, E.; Silventoinen, V.; Pillai, S.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki442

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

  • Johnson, D. Barrie; Okibe, Naoko; Roberto, Francisco F.
  • Archives of Microbiology, Vol. 180, Issue 1
  • DOI: 10.1007/s00203-003-0562-3

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

  • Liu, Li-Jun; Stockdreher, Yvonne; Koch, Tobias
  • Journal of Biological Chemistry, Vol. 289, Issue 39
  • DOI: 10.1074/jbc.M114.591669

Community-wide analysis of microbial genome sequence signatures
journal, January 2009

  • Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J.
  • Genome Biology, Vol. 10, Issue 8
  • DOI: 10.1186/gb-2009-10-8-r85

Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium
journal, May 2006

  • Bogdanova, T. I.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 5
  • DOI: 10.1099/ijs.0.64106-0

Functional, biochemical and genetic diversity of prokaryotic nitrate reductases
journal, February 2001

  • Richardson*, D. J.; Berks, B. C.; Russell, D. A.
  • Cellular and Molecular Life Sciences, Vol. 58, Issue 2
  • DOI: 10.1007/PL00000845

Transaldolase/Glucose-6-phosphate Isomerase Bifunctional Enzyme and Ribulokinase as Factors to Increase Xylitol Production from D -Arabitol in Gluconobacter oxydans
journal, January 2003

  • Sugiyama, Masakazu; Suzuki, Shun-ichi; Tonouchi, Naoto
  • Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 12
  • DOI: 10.1271/bbb.67.2524

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

  • Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
  • Genome Biology, Vol. 12, Issue 5
  • DOI: 10.1186/gb-2011-12-5-r44

Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation
journal, October 2006


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

  • King, Gary M.; Weber, Carolyn F.
  • Nature Reviews Microbiology, Vol. 5, Issue 2
  • DOI: 10.1038/nrmicro1595

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

  • Wright, Erik S.; Yilmaz, L. Safak; Noguera, Daniel R.
  • Applied and Environmental Microbiology, Vol. 78, Issue 3
  • DOI: 10.1128/AEM.06516-11

ProtTest: selection of best-fit models of protein evolution
journal, January 2005


Anaerobic Sulfur Metabolism Coupled to Dissimilatory Iron Reduction in the Extremophile Acidithiobacillus ferrooxidans
journal, January 2013

  • Osorio, Héctor; Mangold, Stefanie; Denis, Yann
  • Applied and Environmental Microbiology, Vol. 79, Issue 7
  • DOI: 10.1128/AEM.03057-12

Copper A of Cytochrome c Oxidase, A Novel, Long-Embattled, Biological Electron-Transfer Site
journal, May 1997


Succinate:quinone oxidoreductases: an overview
journal, January 2002


KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 1999

  • Ogata, H.; Goto, S.; Sato, K.
  • Nucleic Acids Research, Vol. 27, Issue 1
  • DOI: 10.1093/nar/27.1.29

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

  • Cherney, Maia M.; Zhang, Yanfei; Solomonson, Matthew
  • Journal of Molecular Biology, Vol. 398, Issue 2
  • DOI: 10.1016/j.jmb.2010.03.018

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

  • Vignais, Paulette M.; Billoud, Bernard
  • Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272
  • DOI: 10.1021/cr050196r

New Proteins Involved in Sulfur Trafficking in the Cytoplasm of Allochromatium vinosum
journal, March 2014

  • Stockdreher, Yvonne; Sturm, Marga; Josten, Michaele
  • Journal of Biological Chemistry, Vol. 289, Issue 18
  • DOI: 10.1074/jbc.M113.536425

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

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

Energy-Converting [NiFe] Hydrogenases: More than Just H<sub>2</sub> Activation
journal, January 2005

  • Hedderich, Reiner; Forzi, Lucia
  • Journal of Molecular Microbiology and Biotechnology, Vol. 10, Issue 2-4
  • DOI: 10.1159/000091557

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

  • Rothery, Richard A.; Workun, Gregory J.; Weiner, Joel H.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9
  • DOI: 10.1016/j.bbamem.2007.09.002

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

  • Justice, Nicholas B.; Pan, Chongle; Mueller, Ryan
  • Applied and Environmental Microbiology, Vol. 78, Issue 23
  • DOI: 10.1128/AEM.01938-12

Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities
journal, February 2010

  • Denef, V. J.; Kalnejais, L. H.; Mueller, R. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 6
  • DOI: 10.1073/pnas.0907041107

A Widely Conserved Gene Cluster Required for Lactate Utilization in Bacillus subtilis and Its Involvement in Biofilm Formation
journal, February 2009

  • Chai, Y.; Kolter, R.; Losick, R.
  • Journal of Bacteriology, Vol. 191, Issue 8
  • DOI: 10.1128/JB.01464-08

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

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

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

  • Duda, V. I.; Suzina, N. E.; Severina, L. O.
  • Journal of Membrane Biology, Vol. 180, Issue 1
  • DOI: 10.1007/s002320010057

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

  • Guiral, Marianne; Tron, Pascale; Aubert, Corinne
  • Journal of Biological Chemistry, Vol. 280, Issue 51, p. 42004-42015
  • DOI: 10.1074/jbc.M508034200

Clostridium neopropionicum sp. nov., a strict anaerobic bacterium fermenting ethanol to propionate through acrylate pathway
journal, February 1992

  • Tholozan, J. L.; Touzel, J. P.; Samain, E.
  • Archives of Microbiology, Vol. 157, Issue 3
  • DOI: 10.1007/BF00245158

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

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


Purification and Characterization of Sulfide:Quinone Oxidoreductase from an Acidophilic Iron-Oxidizing Bacterium, Acidithiobacillus ferrooxidans
journal, November 2007

  • Wakai, Satoshi; Tsujita, Mizuho; Kikumoto, Mei
  • Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 11
  • DOI: 10.1271/bbb.70332

Anaerobic Respiration Using Fe3+, S0, and H2 in the Chemolithoautotrophic Bacterium Acidithiobacillus ferrooxidans
journal, April 2002


Works referencing / citing this record:

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

  • Rincón-Molina, Clara Ivette; Hernández-García, Juan Alfredo; Rincón-Rosales, Reiner
  • Geomicrobiology Journal, Vol. 36, Issue 2
  • DOI: 10.1080/01490451.2018.1509158