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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]
+ Show Author Affiliations
  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.
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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. https://doi.org/10.1128/aem.02015-17
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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. https://doi.org/10.1128/aem.02015-17. https://www.osti.gov/servlets/purl/1503628.
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@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 = {Fri Dec 08 00:00:00 EST 2017},
month = {Fri Dec 08 00:00:00 EST 2017}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/aem.02015-17
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Cited by: 4 works
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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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    Genomic Variations Underlying Speciation and Niche Specialization of Shewanella baltica
    journal, October 2019

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