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Title: Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, Desulfovibrio vulgaris

Abstract

ABSTRACT. Rapid genetic and phenotypic adaptation of the sulfate-reducing bacteriumDesulfovibrio vulgarisHildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES10 and allowed to experimentally evolve under salt stress for 5,000 generations, was analyzed and compared to clone ES9-11, which was isolated from population ES9 and had evolved under the same conditions for 1,200 generations. These two clones were chosen because they represented the best-adapted clones among six independently evolved populations. ES10-5 acquired new mutations in genes potentially involved in salt tolerance, in addition to the preexisting mutations and different mutations in the same genes as in ES9-11. Most basal abundance changes of metabolites and phospholipid fatty acids (PLFAs) were lower in ES10-5 than ES9-11, but an increase of glutamate and branched PLFA i17:1ω9c under high-salinity conditions was persistent. ES9-11 had decreased cell motility compared to the ancestor; in contrast, ES10-5 showed higher cell motility under both nonstress and high-salinity conditions. Both genotypes displayed better growth energy efficiencies than the ancestor under nonstress or high-salinity conditions. Consistently, ES10-5 did not display most of the basal transcriptional changes observed in ES9-11, but it showedmore » increased expression of genes involved in glutamate biosynthesis, cation efflux, and energy metabolism under high salinity. These results demonstrated the role of glutamate as a key osmolyte and i17:1ω9c as the major PLFA for salt tolerance inD. vulgaris. The mechanistic changes in evolved genotypes suggested that growth energy efficiency might be a key factor for selection. IMPORTANCE. High salinity (e.g., elevated NaCl) is a stressor that affects many organisms. Salt tolerance, a complex trait involving multiple cellular pathways, is attractive for experimental evolutionary studies.Desulfovibrio vulgarisHildenborough is a model sulfate-reducing bacterium (SRB) that is important in biogeochemical cycling of sulfur, carbon, and nitrogen, potentially for bio-corrosion, and for bioremediation of toxic heavy metals and radionuclides. The coexistence of SRB and high salinity in natural habitats and heavy metal-contaminated field sites laid the foundation for the study of salt adaptation ofD. vulgarisHildenborough with experimental evolution. Here in this paper, we analyzed a clone that evolved under salt stress for 5,000 generations and compared it to a clone evolved under the same condition for 1,200 generations. The results indicated the key roles of glutamate for osmoprotection and of i17:1ω9c for increasing membrane fluidity during salt adaptation. The findings provide valuable insights about the salt adaptation mechanism changes during long-term experimental evolution.« less

Authors:
 [1];  [2];  [2];  [1];  [3];  [1];  [3];  [1];  [1];  [1];  [1];  [4];  [1];  [2];  [2];  [5];  [3];  [4];  [6];  [7]
  1. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  3. Univ. of Washington, Seattle, WA (United States). Dept. of Earth and Space Sciences
  4. Univ. of Missouri, Columbia, MO (United States). Dept. of Biochemistry and Molecular Microbiology and Immunology
  5. Univ. of Washington Bothell, Bothell, WA (United States). School of Science, Technology, Engineering and Mathematics
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
  7. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Tsinghua Univ., Beijing (China). State Key Joint Lab. of Environment Simulation and Pollution Control, School of Environment
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:
1432221
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Desulfovibrio vulgaris; PLFA; cell motility; energy efficiency; genomic mutations; organic solutes; transcriptomics

Citation Formats

Zhou, Aifen, Lau, Rebecca, Baran, Richard, Ma, Jincai, von Netzer, Frederick, Shi, Weiling, Gorman-Lewis, Drew, Kempher, Megan L., He, Zhili, Qin, Yujia, Shi, Zhou, Zane, Grant M., Wu, Liyou, Bowen, Benjamin P., Northen, Trent R., Hillesland, Kristina L., Stahl, David A., Wall, Judy D., Arkin, Adam P., and Zhou, Jizhong. Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, Desulfovibrio vulgaris. United States: N. p., 2017. Web. doi:10.1128/mBio.01780-17.
Zhou, Aifen, Lau, Rebecca, Baran, Richard, Ma, Jincai, von Netzer, Frederick, Shi, Weiling, Gorman-Lewis, Drew, Kempher, Megan L., He, Zhili, Qin, Yujia, Shi, Zhou, Zane, Grant M., Wu, Liyou, Bowen, Benjamin P., Northen, Trent R., Hillesland, Kristina L., Stahl, David A., Wall, Judy D., Arkin, Adam P., & Zhou, Jizhong. Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, Desulfovibrio vulgaris. United States. doi:10.1128/mBio.01780-17.
Zhou, Aifen, Lau, Rebecca, Baran, Richard, Ma, Jincai, von Netzer, Frederick, Shi, Weiling, Gorman-Lewis, Drew, Kempher, Megan L., He, Zhili, Qin, Yujia, Shi, Zhou, Zane, Grant M., Wu, Liyou, Bowen, Benjamin P., Northen, Trent R., Hillesland, Kristina L., Stahl, David A., Wall, Judy D., Arkin, Adam P., and Zhou, Jizhong. Tue . "Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, Desulfovibrio vulgaris". United States. doi:10.1128/mBio.01780-17. https://www.osti.gov/servlets/purl/1432221.
@article{osti_1432221,
title = {Key Metabolites and Mechanistic Changes for Salt Tolerance in an Experimentally Evolved Sulfate-Reducing Bacterium, Desulfovibrio vulgaris},
author = {Zhou, Aifen and Lau, Rebecca and Baran, Richard and Ma, Jincai and von Netzer, Frederick and Shi, Weiling and Gorman-Lewis, Drew and Kempher, Megan L. and He, Zhili and Qin, Yujia and Shi, Zhou and Zane, Grant M. and Wu, Liyou and Bowen, Benjamin P. and Northen, Trent R. and Hillesland, Kristina L. and Stahl, David A. and Wall, Judy D. and Arkin, Adam P. and Zhou, Jizhong},
abstractNote = {ABSTRACT. Rapid genetic and phenotypic adaptation of the sulfate-reducing bacteriumDesulfovibrio vulgarisHildenborough to salt stress was observed during experimental evolution. In order to identify key metabolites important for salt tolerance, a clone, ES10-5, which was isolated from population ES10 and allowed to experimentally evolve under salt stress for 5,000 generations, was analyzed and compared to clone ES9-11, which was isolated from population ES9 and had evolved under the same conditions for 1,200 generations. These two clones were chosen because they represented the best-adapted clones among six independently evolved populations. ES10-5 acquired new mutations in genes potentially involved in salt tolerance, in addition to the preexisting mutations and different mutations in the same genes as in ES9-11. Most basal abundance changes of metabolites and phospholipid fatty acids (PLFAs) were lower in ES10-5 than ES9-11, but an increase of glutamate and branched PLFA i17:1ω9c under high-salinity conditions was persistent. ES9-11 had decreased cell motility compared to the ancestor; in contrast, ES10-5 showed higher cell motility under both nonstress and high-salinity conditions. Both genotypes displayed better growth energy efficiencies than the ancestor under nonstress or high-salinity conditions. Consistently, ES10-5 did not display most of the basal transcriptional changes observed in ES9-11, but it showed increased expression of genes involved in glutamate biosynthesis, cation efflux, and energy metabolism under high salinity. These results demonstrated the role of glutamate as a key osmolyte and i17:1ω9c as the major PLFA for salt tolerance inD. vulgaris. The mechanistic changes in evolved genotypes suggested that growth energy efficiency might be a key factor for selection. IMPORTANCE. High salinity (e.g., elevated NaCl) is a stressor that affects many organisms. Salt tolerance, a complex trait involving multiple cellular pathways, is attractive for experimental evolutionary studies.Desulfovibrio vulgarisHildenborough is a model sulfate-reducing bacterium (SRB) that is important in biogeochemical cycling of sulfur, carbon, and nitrogen, potentially for bio-corrosion, and for bioremediation of toxic heavy metals and radionuclides. The coexistence of SRB and high salinity in natural habitats and heavy metal-contaminated field sites laid the foundation for the study of salt adaptation ofD. vulgarisHildenborough with experimental evolution. Here in this paper, we analyzed a clone that evolved under salt stress for 5,000 generations and compared it to a clone evolved under the same condition for 1,200 generations. The results indicated the key roles of glutamate for osmoprotection and of i17:1ω9c for increasing membrane fluidity during salt adaptation. The findings provide valuable insights about the salt adaptation mechanism changes during long-term experimental evolution.},
doi = {10.1128/mBio.01780-17},
journal = {mBio (Online)},
number = 6,
volume = 8,
place = {United States},
year = {2017},
month = {11}
}

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