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Title: Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains

Abstract

Niche partitioning and sequence evolution drive genomic and phenotypic divergence, which ultimately leads to bacterial diversification. This study investigated the genomic composition of two Shewanella baltica clades previously identified through multilocus sequencing typing and recovered from the redox transition zone in the central Baltic Sea. Comparative genomic analysis revealed significantly higher interclade than intraclade genomic dissimilarity and that a subset of genes present in clade A were associated with potential adaptation to respiration of sulfur compounds present in the redox transition zone. The transcriptomic divergence between two representative strains of clades A and D, OS185 and OS195, was also characterized and revealed marked regulatory differences. We found that both the transcriptional divergence of shared genes and expression of strain-specific genes led to differences in regulatory patterns between strains that correlate with environmental redox niches. For example, under anoxic conditions of respiratory nitrate ammonification, OS185—the strain isolated from a nitrate-rich environment—upregulated nearly twice the number of shared genes upregulated by OS195—the strain isolated from an H2S-containing anoxic environment. On the other hand, OS195 showed stronger induction of strain-specific genes, especially those associated with sulfur compound respiration, under thiosulfate-reducing conditions. A positive association between the level of transcriptional divergence and the levelmore » of sequence divergence for shared genes was also noted. Our results provide further support for the hypothesis that genomic changes impacting transcriptional regulation play an important role in the diversification of ecologically distinct populations. IMPORTANCE: This study examined potential mechanisms through which co-occurring Shewanella baltica strains diversified to form ecologically distinct populations. At the time of isolation, the strains studied composed the major fraction of culturable nitrate-reducing communities in the Baltica Sea. Analysis of genomic content of 13 S. baltica strains from two clades representing different ecotypes demonstrated that one clade specifically possesses a number of genes that could favor successful adaptation to respire sulfur compounds in the portion of the water column from which these strains were isolated. In addition, transcriptional profiling of fully sequenced strains representative of these two clades, OS185 and OS195, under oxygen-, nitrate-, and thiosulfate-respiring conditions demonstrated that the strains exhibit relatively similar transcriptional responses during aerobic growth but more-distinct transcriptional responses under nitrate- and thiosulfate-respiring conditions. Results from this study provide insights into how genomic and gene regulatory diversification together impacted the redox specialization of the S. baltica strains.« less

Authors:
 [1];  [2];  [3];  [3];  [4];  [4];  [5];  [6]
  1. East China Normal Univ. (ECNU), Shanghai (China); Shanghai Inst. of Eco-Chongming, Shanghai (China); Michigan State Univ., East Lansing, MI (United States)
  2. Baylor College of Medicine, Houston, TX (United States)
  3. Georgia Inst. of Technology, Atlanta, GA (United States)
  4. Helmholtz Centre for Infection Research, Braunschweig (Germany)
  5. Michigan State Univ., East Lansing, MI (United States)
  6. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1503628
Grant/Contract Number:  
FG02-07ER64389
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: 4; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Shewanella baltica; comparative transcriptomics; comparative genomics; adaptation

Citation Formats

Deng, Jie, Auchtung, Jennifer M., Konstantinidis, Konstantinos T., Caro-Quintero, Alejandro, Brettar, Ingrid, Höfle, Manfred, Tiedje, James M., and Löffler, Frank E. Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains. United States: N. p., 2017. Web. doi:10.1128/aem.02015-17.
Deng, Jie, Auchtung, Jennifer M., Konstantinidis, Konstantinos T., Caro-Quintero, Alejandro, Brettar, Ingrid, Höfle, Manfred, Tiedje, James M., & Löffler, Frank E. Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains. United States. doi:10.1128/aem.02015-17.
Deng, Jie, Auchtung, Jennifer M., Konstantinidis, Konstantinos T., Caro-Quintero, Alejandro, Brettar, Ingrid, Höfle, Manfred, Tiedje, James M., and Löffler, Frank E. Fri . "Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains". United States. doi:10.1128/aem.02015-17. https://www.osti.gov/servlets/purl/1503628.
@article{osti_1503628,
title = {Divergence in Gene Regulation Contributes to Sympatric Speciation of Shewanella baltica Strains},
author = {Deng, Jie and Auchtung, Jennifer M. and Konstantinidis, Konstantinos T. and Caro-Quintero, Alejandro and Brettar, Ingrid and Höfle, Manfred and Tiedje, James M. and Löffler, Frank E.},
abstractNote = {Niche partitioning and sequence evolution drive genomic and phenotypic divergence, which ultimately leads to bacterial diversification. This study investigated the genomic composition of two Shewanella baltica clades previously identified through multilocus sequencing typing and recovered from the redox transition zone in the central Baltic Sea. Comparative genomic analysis revealed significantly higher interclade than intraclade genomic dissimilarity and that a subset of genes present in clade A were associated with potential adaptation to respiration of sulfur compounds present in the redox transition zone. The transcriptomic divergence between two representative strains of clades A and D, OS185 and OS195, was also characterized and revealed marked regulatory differences. We found that both the transcriptional divergence of shared genes and expression of strain-specific genes led to differences in regulatory patterns between strains that correlate with environmental redox niches. For example, under anoxic conditions of respiratory nitrate ammonification, OS185—the strain isolated from a nitrate-rich environment—upregulated nearly twice the number of shared genes upregulated by OS195—the strain isolated from an H2S-containing anoxic environment. On the other hand, OS195 showed stronger induction of strain-specific genes, especially those associated with sulfur compound respiration, under thiosulfate-reducing conditions. A positive association between the level of transcriptional divergence and the level of sequence divergence for shared genes was also noted. Our results provide further support for the hypothesis that genomic changes impacting transcriptional regulation play an important role in the diversification of ecologically distinct populations. IMPORTANCE: This study examined potential mechanisms through which co-occurring Shewanella baltica strains diversified to form ecologically distinct populations. At the time of isolation, the strains studied composed the major fraction of culturable nitrate-reducing communities in the Baltica Sea. Analysis of genomic content of 13 S. baltica strains from two clades representing different ecotypes demonstrated that one clade specifically possesses a number of genes that could favor successful adaptation to respire sulfur compounds in the portion of the water column from which these strains were isolated. In addition, transcriptional profiling of fully sequenced strains representative of these two clades, OS185 and OS195, under oxygen-, nitrate-, and thiosulfate-respiring conditions demonstrated that the strains exhibit relatively similar transcriptional responses during aerobic growth but more-distinct transcriptional responses under nitrate- and thiosulfate-respiring conditions. Results from this study provide insights into how genomic and gene regulatory diversification together impacted the redox specialization of the S. baltica strains.},
doi = {10.1128/aem.02015-17},
journal = {Applied and Environmental Microbiology},
number = 4,
volume = 84,
place = {United States},
year = {2017},
month = {12}
}

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Figures / Tables:

FIG 1 FIG 1: Principal-component analysis (PCA) of genes differentially expressed by OS185 and OS195 grown under oxygen (O), thiosulfate (T) and nitrate (N)-respiring conditions. Analysis was done on (a) genes shared by OS185 and OS195 and (b) all differentially expressed genes.

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Works referenced in this record:

Denitrification in the Central Baltic: evidence for H2S-oxidation as motor of denitrification at the oxic-anoxic interface
journal, January 1991

  • Brettar, I.; Rheinheimer, G.
  • Marine Ecology Progress Series, Vol. 77
  • DOI: 10.3354/meps077157

Shewanella baltica Ecotypes Have Wide Transcriptional Variation under the Same Growth Conditions
journal, October 2016


Global Transcriptome Analysis of Shewanella oneidensis MR-1 Exposed to Different Terminal Electron Acceptors
journal, September 2005


Gene expression analysis of E. coli strains provides insights into the role of gene regulation in diversification
journal, October 2014


Characterization of cytochrome mutants for pellicle formation in Shewanella onedensis MR-1
journal, June 2009

  • Liang, Yi-li; He, Zhi-li; Gao, Hai-chun
  • Transactions of Nonferrous Metals Society of China, Vol. 19, Issue 3
  • DOI: 10.1016/S1003-6326(08)60336-2

Evolution of global regulatory networks during a long-term experiment withEscherichia coli
journal, January 2007

  • Philippe, Nadège; Crozat, Estelle; Lenski, Richard E.
  • BioEssays, Vol. 29, Issue 9
  • DOI: 10.1002/bies.20629

The bacterial species definition in the genomic era
journal, October 2006

  • Konstantinidis, Konstantinos T.; Ramette, Alban; Tiedje, James M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475
  • DOI: 10.1098/rstb.2006.1920

The landscape of genetic complexity across 5,700 gene expression traits in yeast
journal, January 2005

  • Brem, R. B.; Kruglyak, L.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 5
  • DOI: 10.1073/pnas.0408709102

The Protonmotive Q Cycle in Mitochondria and Bacteria
journal, January 1994

  • Brandt, Ulrich; Trumpower, Bernard
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 29, Issue 3
  • DOI: 10.3109/10409239409086800

The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1 : Dissimilatory sulfite reduction by the octahaem SirA
journal, August 2010


Significance analysis of microarrays applied to the ionizing radiation response
journal, April 2001

  • Tusher, V. G.; Tibshirani, R.; Chu, G.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 9, p. 5116-5121
  • DOI: 10.1073/pnas.091062498

The species concept for prokaryotes
journal, January 2001


Respiratory Nitrate Ammonification by Shewanella oneidensis MR-1
journal, November 2006

  • Cruz-Garcia, C.; Murray, A. E.; Klappenbach, J. A.
  • Journal of Bacteriology, Vol. 189, Issue 2
  • DOI: 10.1128/JB.01194-06

Expression variability of co-regulated genes differentiates Saccharomyces cerevisiae strains
journal, April 2011


Analysis of Genome Plasticity in Pathogenic and Commensal Escherichia coli Isolates by Use of DNA Arrays
journal, March 2003


Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration: c-type cytochromes of S. oneidensis
journal, June 2010


Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing
journal, February 2009

  • Yoder-Himes, D. R.; Chain, P. S. G.; Zhu, Y.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 10
  • DOI: 10.1073/pnas.0813403106

Genomic insights that advance the species definition for prokaryotes
journal, February 2005

  • Konstantinidis, K. T.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
  • DOI: 10.1073/pnas.0409727102

Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium
journal, February 2016

  • Parkinson, John E.; Baumgarten, Sebastian; Michell, Craig T.
  • Genome Biology and Evolution, Vol. 8, Issue 3
  • DOI: 10.1093/gbe/evw019

Microbial Genomics: E. coli Relatives Out of Doors and Out of Body
journal, August 2011


Stability, genotypic and phenotypic diversity of S hewanella baltica in the redox transition zone of the Baltic Sea
journal, January 2014

  • Deng, Jie; Brettar, Ingrid; Luo, Chengwei
  • Environmental Microbiology, Vol. 16, Issue 6
  • DOI: 10.1111/1462-2920.12344

Stability and diversity of the genetic structure of a Shewanella putrefaciens population in the water column of the central Baltic
journal, January 1997

  • Ziemke, F.; Brettar, I.; Höfle, Mg
  • Aquatic Microbial Ecology, Vol. 13
  • DOI: 10.3354/ame013063

Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species
journal, April 2011

  • Luo, C.; Walk, S. T.; Gordon, D. M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 17
  • DOI: 10.1073/pnas.1015622108

Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea
journal, July 2010

  • Caro-Quintero, Alejandro; Deng, Jie; Auchtung, Jennifer
  • The ISME Journal, Vol. 5, Issue 1
  • DOI: 10.1038/ismej.2010.93

The loci of Evolution: how Predictable is Genetic Evolution?
journal, September 2008


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