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Title: Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris

Abstract

To investigate the genetic basis of microbial evolutionary adaptation to salt (NaCl) stress, populations of Desulfovibrio vulgaris Hildenborough (DvH), a sulfate-reducing bacterium important for the biogeochemical cycling of sulfur, carbon and nitrogen, and potentially the bioremediation of toxic heavy metals and radionuclides, were propagated under salt stress or non-stress conditions for 1200 generations. Whole-genome sequencing revealed 11 mutations in salt stress-evolved clone ES9-11 and 14 mutations in non-stress-evolved clone EC3-10. Whole-population sequencing data suggested the rapid selective sweep of the pre-existing polymorphisms under salt stress within the first 100 generations and the slow fixation of new mutations. Population genotyping data demonstrated that the rapid selective sweep of pre-existing polymorphisms was common in salt stress-evolved populations. In contrast, the selection of pre-existing polymorphisms was largely random in EC populations. Consistently, at 100 generations, stress-evolved population ES9 showed improved salt tolerance, namely increased growth rate (2.0-fold), higher biomass yield (1.8-fold) and shorter lag phase (0.7-fold) under higher salinity conditions. The beneficial nature of several mutations was confirmed by site-directed mutagenesis. All four tested mutations contributed to the shortened lag phases under higher salinity condition. In particular, compared with the salt tolerance improvement in ES9-11, a mutation in a histidine kinase protein genemore » lytS contributed 27% of the growth rate increase and 23% of the biomass yield increase while a mutation in hypothetical gene DVU2472 contributed 24% of the biomass yield increase. In conclusion, our results suggested that a few beneficial mutations could lead to dramatic improvements in salt tolerance.« less

Authors:
 [1];  [2];  [1];  [3];  [1];  [4];  [5];  [5];  [6];  [4];  [7];  [8];  [9];  [10]
  1. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology
  2. Univ. of Washington, Bothell, WA (United States). Biological Sciences Division
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of Missouri, Columbia, MO (United States). Dept. of Biochemistry and Molecular Microbiology and Immunology
  5. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Dalian Univ. of Technology, Dalian (China). Key Lab. of Industrial Ecology and Environmental Engineering (MOE), School of Environmental Science and Technology
  6. Univ. of Washington, Seattle, WA (United States). Dept. of Civil and Environmental Engineering
  7. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Civil and Environmental Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  8. Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology and Immunology
  9. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
  10. Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics, Dept. of Microbiology and Plant Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Science Division; 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) (SC-23)
OSTI Identifier:
1407292
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 9; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Zhou, Aifen, Hillesland, Kristina L., He, Zhili, Schackwitz, Wendy, Tu, Qichao, Zane, Grant M., Ma, Qiao, Qu, Yuanyuan, Stahl, David A., Wall, Judy D., Hazen, Terry C., Fields, Matthew W., Arkin, Adam P., and Zhou, Jizhong. Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris. United States: N. p., 2015. Web. doi:10.1038/ismej.2015.45.
Zhou, Aifen, Hillesland, Kristina L., He, Zhili, Schackwitz, Wendy, Tu, Qichao, Zane, Grant M., Ma, Qiao, Qu, Yuanyuan, Stahl, David A., Wall, Judy D., Hazen, Terry C., Fields, Matthew W., Arkin, Adam P., & Zhou, Jizhong. Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris. United States. doi:10.1038/ismej.2015.45.
Zhou, Aifen, Hillesland, Kristina L., He, Zhili, Schackwitz, Wendy, Tu, Qichao, Zane, Grant M., Ma, Qiao, Qu, Yuanyuan, Stahl, David A., Wall, Judy D., Hazen, Terry C., Fields, Matthew W., Arkin, Adam P., and Zhou, Jizhong. Tue . "Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris". United States. doi:10.1038/ismej.2015.45. https://www.osti.gov/servlets/purl/1407292.
@article{osti_1407292,
title = {Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris},
author = {Zhou, Aifen and Hillesland, Kristina L. and He, Zhili and Schackwitz, Wendy and Tu, Qichao and Zane, Grant M. and Ma, Qiao and Qu, Yuanyuan and Stahl, David A. and Wall, Judy D. and Hazen, Terry C. and Fields, Matthew W. and Arkin, Adam P. and Zhou, Jizhong},
abstractNote = {To investigate the genetic basis of microbial evolutionary adaptation to salt (NaCl) stress, populations of Desulfovibrio vulgaris Hildenborough (DvH), a sulfate-reducing bacterium important for the biogeochemical cycling of sulfur, carbon and nitrogen, and potentially the bioremediation of toxic heavy metals and radionuclides, were propagated under salt stress or non-stress conditions for 1200 generations. Whole-genome sequencing revealed 11 mutations in salt stress-evolved clone ES9-11 and 14 mutations in non-stress-evolved clone EC3-10. Whole-population sequencing data suggested the rapid selective sweep of the pre-existing polymorphisms under salt stress within the first 100 generations and the slow fixation of new mutations. Population genotyping data demonstrated that the rapid selective sweep of pre-existing polymorphisms was common in salt stress-evolved populations. In contrast, the selection of pre-existing polymorphisms was largely random in EC populations. Consistently, at 100 generations, stress-evolved population ES9 showed improved salt tolerance, namely increased growth rate (2.0-fold), higher biomass yield (1.8-fold) and shorter lag phase (0.7-fold) under higher salinity conditions. The beneficial nature of several mutations was confirmed by site-directed mutagenesis. All four tested mutations contributed to the shortened lag phases under higher salinity condition. In particular, compared with the salt tolerance improvement in ES9-11, a mutation in a histidine kinase protein gene lytS contributed 27% of the growth rate increase and 23% of the biomass yield increase while a mutation in hypothetical gene DVU2472 contributed 24% of the biomass yield increase. In conclusion, our results suggested that a few beneficial mutations could lead to dramatic improvements in salt tolerance.},
doi = {10.1038/ismej.2015.45},
journal = {The ISME Journal},
number = 11,
volume = 9,
place = {United States},
year = {2015},
month = {4}
}

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Works referenced in this record:

Compensatory Evolution of Gene Regulation in Response to Stress by Escherichia coli Lacking RpoS
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