Genomic Variations Underlying Speciation and Niche Specialization of Shewanella baltica

Deng, Jie; Auchtung, Jennifer M.; Konstantinidis, Konstantinos T.; Brettar, Ingrid; Höfle, Manfred G.; Tiedje, James M.

doi:10.1128/msystems.00560-19

Genomic Variations Underlying Speciation and Niche Specialization of Shewanella baltica

Journal Article · Tue Oct 15 00:00:00 EDT 2019 · mSystems

DOI:https://doi.org/10.1128/msystems.00560-19· OSTI ID:1609945

Deng, Jie ^[1]; Auchtung, Jennifer M. ^[2]; Konstantinidis, Konstantinos T. ^[3]; Brettar, Ingrid ^[4]; Höfle, Manfred G. ^[4]; Tiedje, James M. ^[5]

East China Normal Univ. (ECNU), Shanghai (China); Michigan State Univ., East Lansing, MI (United States); DOE/OSTI
Univ. of Nebraska, Lincoln, NE (United States)
Georgia Inst. of Technology, Atlanta, GA (United States)
Helmholtz Centre for Infection Research, Braunschweig (Germany)
Michigan State Univ., East Lansing, MI (United States)

Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. The genomic structures of 46 of these isolates were investigated through comparative genomic hybridization (CGH), which revealed a gradient of genomic similarity, ranging from 65% to as high as 99%. The core genome of the S. baltica species was enriched in anaerobic respiration-associated genes. Auxiliary genes, most of which locate within a few genomic islands (GIs), were nonuniformly distributed among the isolates. Specifically, hypothetical and mobile genetic element (MGE)-associated genes dominated intraclade gene content differences, whereas gain/loss of functional genes drove gene content differences among less related strains. Among the major S. baltica clades, gene signatures related to specific redox-driven and spatial niches within the water column were identified. For instance, genes involved in anaerobic respiration of sulfur compounds may provide key adaptive advantages for clade A strains in anoxic waters where sulfur-containing electron acceptors are present. Genes involved in cell motility, in particular, a secondary flagellar biosynthesis system, may be associated with the free-living lifestyle by clade E strains. Collectively, this study revealed characteristics of genome variations present in the water column and active speciation of S. baltica strains, driven by niche partitioning and horizontal gene transfer (HGT).

View Accepted Manuscript (DOE)

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-07ER64389

OSTI ID:: 1609945

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 5 Vol. 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (47)

Phylogeny and Abundance of Novel Denitrifying Bacteria Isolated from the Water Column of the Central Baltic Sea Brettar, I.; Moore, E. R. B.; Höfle, M. G. Microbial Ecology, Vol. 42, Issue 3 https://doi.org/10.1007/s00248-001-0011-2	journal	October 2001
Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea Caro-Quintero, Alejandro; Deng, Jie; Auchtung, Jennifer The ISME Journal, Vol. 5, Issue 1 https://doi.org/10.1038/ismej.2010.93	journal	July 2010
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08656	journal	December 2009
Fifteen years of microbial genomics: meeting the challenges and fulfilling the dream Kyrpides, Nikos C. Nature Biotechnology, Vol. 27, Issue 7 https://doi.org/10.1038/nbt.1552	journal	July 2009
1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life Mukherjee, Supratim; Seshadri, Rekha; Varghese, Neha J. Nature Biotechnology, Vol. 35, Issue 7 https://doi.org/10.1038/nbt.3886	journal	June 2017
Horizontal gene transfer, genome innovation and evolution Gogarten, J. Peter; Townsend, Jeffrey P. Nature Reviews Microbiology, Vol. 3, Issue 9 https://doi.org/10.1038/nrmicro1204	journal	August 2005
Mobile genetic elements: the agents of open source evolution Frost, Laura S.; Leplae, Raphael; Summers, Anne O. Nature Reviews Microbiology, Vol. 3, Issue 9 https://doi.org/10.1038/nrmicro1235	journal	September 2005
CRISPR — a widespread system that provides acquired resistance against phages in bacteria and archaea Sorek, Rotem; Kunin, Victor; Hugenholtz, Philip Nature Reviews Microbiology, Vol. 6, Issue 3 https://doi.org/10.1038/nrmicro1793	journal	March 2008
Towards environmental systems biology of Shewanella Fredrickson, James K.; Romine, Margaret F.; Beliaev, Alexander S. Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1947	journal	July 2008
Genomic islands in pathogenic and environmental microorganisms Dobrindt, Ulrich; Hochhut, Bianca; Hentschel, Ute Nature Reviews Microbiology, Vol. 2, Issue 5 https://doi.org/10.1038/nrmicro884	journal	May 2004
Genomic insights that advance the species definition for prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409727102	journal	February 2005
Comparative systems biology across an evolutionary gradient within the Shewanella genus Konstantinidis, Konstantinos T.; Serres, Margrethe H.; Romine, Margaret F. Proceedings of the National Academy of Sciences, Vol. 106, Issue 37 https://doi.org/10.1073/pnas.0902000106	journal	September 2009
Complete genome sequence and analysis of Wolinella succinogenes Baar, C.; Eppinger, M.; Raddatz, G. Proceedings of the National Academy of Sciences, Vol. 100, Issue 20 https://doi.org/10.1073/pnas.1932838100	journal	September 2003
Complete Genome Structure of the Nitrogen-fixing Symbiotic Bacterium Mesorhizobium loti Kaneko, T. DNA Research, Vol. 7, Issue 6 https://doi.org/10.1093/dnares/7.6.331	journal	January 2000
Application of Phylogenetic Networks in Evolutionary Studies Huson, Daniel H.; Bryant, David Molecular Biology and Evolution, Vol. 23, Issue 2 https://doi.org/10.1093/molbev/msj030	journal	October 2005
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level Rodriguez-R, Luis M.; Gunturu, Santosh; Harvey, William T. Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky467	journal	June 2018
Sequences, sequence clusters and bacterial species Hanage, William P.; Fraser, Christophe; Spratt, Brian G. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475 https://doi.org/10.1098/rstb.2006.1917	journal	October 2006
Reclassification of Shewanella putrefaciens Owen's genomic group II as Shewanella baltica sp. nov. Ziemke, F.; Hofle, M. G.; Lalucat, J. International Journal of Systematic Bacteriology, Vol. 48, Issue 1 https://doi.org/10.1099/00207713-48-1-179	journal	January 1998
The mercury resistance operon of the IncJ plasmid pMERPH exhibits structural and regulatory divergence from other Gramnegative mer operons Osborn, A. M.; Bruce, K. D.; Ritchie, D. A. Microbiology, Vol. 142, Issue 2 https://doi.org/10.1099/13500872-142-2-337	journal	February 1996
Specificity of motor components in the dual flagellar system of Shewanella putrefaciens CN-32: Specificity in dual flagellar systems Bubendorfer, Sebastian; Held, Susanne; Windel, Natalie Molecular Microbiology, Vol. 83, Issue 2 https://doi.org/10.1111/j.1365-2958.2011.07934.x	journal	December 2011
Pathogenicity islands: a molecular toolbox for bacterial virulence Gal-Mor, Ohad; Finlay, B. Brett Cellular Microbiology, Vol. 8, Issue 11 https://doi.org/10.1111/j.1462-5822.2006.00794.x	journal	November 2006
Phylogenomics: Intersection of Evolution and Genomics Eisen, J. A. Science, Vol. 300, Issue 5626 https://doi.org/10.1126/science.1086292	journal	June 2003
Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains Deng, Jie; Auchtung, Jennifer M.; Konstantinidis, Konstantinos T. Applied and Environmental Microbiology, Vol. 84, Issue 4 https://doi.org/10.1128/aem.02015-17	journal	December 2017
Genotyping of heterotrophic bacteria from the central baltic sea by use of low-molecular-weight RNA profiles Hofle, M. G.; Brettar, I. Applied and Environmental Microbiology, Vol. 62, Issue 4 https://doi.org/10.1128/aem.62.4.1383-1390.1996	journal	April 1996
Characterization of the cciIR Quorum-Sensing System in Burkholderia cenocepacia Malott, Rebecca J.; Baldwin, Adam; Mahenthiralingam, Eshwar Infection and Immunity, Vol. 73, Issue 8 https://doi.org/10.1128/iai.73.8.4982-4992.2005	journal	August 2005
Genome Sequencing of Five Shewanella baltica Strains Recovered from the Oxic-Anoxic Interface of the Baltic Sea Caro-Quintero, A.; Auchtung, J.; Deng, J. Journal of Bacteriology, Vol. 194, Issue 5 https://doi.org/10.1128/jb.06468-11	journal	February 2012
Nested Deletions of the SRL Pathogenicity Island ofShigella flexneri 2a Turner, Sally A.; Luck, Shelley N.; Sakellaris, Harry Journal of Bacteriology, Vol. 183, Issue 19 https://doi.org/10.1128/jb.183.19.5535-5543.2001	journal	October 2001
Global Transcriptome Analysis of Shewanella oneidensis MR-1 Exposed to Different Terminal Electron Acceptors Beliaev, A. S.; Klingeman, D. M.; Klappenbach, J. A. Journal of Bacteriology, Vol. 187, Issue 20 https://doi.org/10.1128/jb.187.20.7138-7145.2005	journal	September 2005
Ecology and Biotechnology of the Genus Shewanella Hau, Heidi H.; Gralnick, Jeffrey A. Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093257	journal	October 2007
Stability and diversity of the genetic structure of a Shewanella putrefaciens population in the water column of the central Baltic Ziemke, F.; Brettar, I.; Höfle, Mg Aquatic Microbial Ecology, Vol. 13 https://doi.org/10.3354/ame013063	journal	January 1997
Nitrous oxide producing heterotrophic bacteria from the water column of the central Baltic: abundance and molecular identification Brettar, I.; Hofle, Mg Marine Ecology Progress Series, Vol. 94 https://doi.org/10.3354/meps094253	journal	January 1993
Interaction of enteropathogenicEscherichia coli with host epithelial cells Nisan, I.; Wolff, C.; Hanski, E. Folia Microbiologica, Vol. 43, Issue 3 https://doi.org/10.1007/bf02818609	journal	June 1998
The Repetitive DNA Elements Called CRISPRs and Their Associated Genes: Evidence of Horizontal Transfer Among Prokaryotes Godde, James S.; Bickerton, Amanda Journal of Molecular Evolution, Vol. 62, Issue 6 https://doi.org/10.1007/s00239-005-0223-z	journal	April 2006
Mechanism of Cobyrinic Acid a , c -Diamide Synthetase from Salmonella typhimurium LT2 ^† Fresquet, Vicente; Williams, LaKenya; Raushel, Frank M. Biochemistry, Vol. 43, Issue 33 https://doi.org/10.1021/bi048972x	journal	August 2004
Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species Luo, C.; Walk, S. T.; Gordon, D. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1015622108	journal	April 2011
Secondary bacterial flagellar system improves bacterial spreading by increasing the directional persistence of swimming Bubendorfer, S.; Koltai, M.; Rossmann, F. Proceedings of the National Academy of Sciences, Vol. 111, Issue 31 https://doi.org/10.1073/pnas.1405820111	journal	July 2014
Complete Genomic Sequence of Nitrogen-fixing Symbiotic Bacterium Bradyrhizobium japonicum USDA110 Kaneko, T. DNA Research, Vol. 9, Issue 6 https://doi.org/10.1093/dnares/9.6.189	journal	January 2002
Stability, genotypic and phenotypic diversity of S hewanella baltica in the redox transition zone of the Baltic Sea Deng, Jie; Brettar, Ingrid; Luo, Chengwei Environmental Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/1462-2920.12344	journal	January 2014
How organic carbon derived from multiple sources contributes to carbon sequestration processes in a shallow coastal system? Watanabe, Kenta; Kuwae, Tomohiro Global Change Biology, Vol. 21, Issue 7 https://doi.org/10.1111/gcb.12924	journal	April 2015
Diversity and occurrence of Burkholderia spp. in the natural environment Compant, Stéphane; Nowak, Jerzy; Coenye, Tom FEMS Microbiology Reviews, Vol. 32, Issue 4 https://doi.org/10.1111/j.1574-6976.2008.00113.x	journal	July 2008
Involvement of the Shewanella oneidensis Decaheme Cytochrome MtrA in the Periplasmic Stability of the β-Barrel Protein MtrB Schicklberger, Marcus; Bücking, Clemens; Schuetz, Bjoern Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.01201-10	journal	December 2010
Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains Deng, Jie; Auchtung, Jennifer M.; Konstantinidis, Konstantinos T. Applied and Environmental Microbiology, Vol. 84, Issue 4 https://doi.org/10.1128/AEM.02015-17	journal	December 2017
Characterization of the cciIR Quorum-Sensing System in Burkholderia cenocepacia Malott, Rebecca J.; Baldwin, Adam; Mahenthiralingam, Eshwar Infection and Immunity, Vol. 73, Issue 8 https://doi.org/10.1128/IAI.73.8.4982-4992.2005	journal	August 2005
Genome Sequencing of Five Shewanella baltica Strains Recovered from the Oxic-Anoxic Interface of the Baltic Sea Caro-Quintero, A.; Auchtung, J.; Deng, J. Journal of Bacteriology, Vol. 194, Issue 5 https://doi.org/10.1128/JB.06468-11	journal	February 2012
Nested Deletions of the SRL Pathogenicity Island ofShigella flexneri 2a Turner, Sally A.; Luck, Shelley N.; Sakellaris, Harry Journal of Bacteriology, Vol. 183, Issue 19 https://doi.org/10.1128/JB.183.19.5535-5543.2001	journal	October 2001
Global Transcriptome Analysis of Shewanella oneidensis MR-1 Exposed to Different Terminal Electron Acceptors Beliaev, A. S.; Klingeman, D. M.; Klappenbach, J. A. Journal of Bacteriology, Vol. 187, Issue 20 https://doi.org/10.1128/JB.187.20.7138-7145.2005	journal	September 2005

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