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Title: Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations

Abstract

© 2016 International Society for Microbial Ecology. Multiple models describe the formation and evolution of distinct microbial phylogenetic groups. These evolutionary models make different predictions regarding how adaptive alleles spread through populations and how genetic diversity is maintained. Processes predicted by competing evolutionary models, for example, genome-wide selective sweeps vs gene-specific sweeps, could be captured in natural populations using time-series metagenomics if the approach were applied over a sufficiently long time frame. Direct observations of either process would help resolve how distinct microbial groups evolve. Here, from a 9-year metagenomic study of a freshwater lake (2005-2013), we explore changes in single-nucleotide polymorphism (SNP) frequencies and patterns of gene gain and loss in 30 bacterial populations. SNP analyses revealed substantial genetic heterogeneity within these populations, although the degree of heterogeneity varied by > 1000-fold among populations. SNP allele frequencies also changed dramatically over time within some populations. Interestingly, nearly all SNP variants were slowly purged over several years from one population of green sulfur bacteria, while at the same time multiple genes either swept through or were lost from this population. These patterns were consistent with a genome-wide selective sweep in progress, a process predicted by the 'ecotype model' of speciationmore » but not previously observed in nature. In contrast, other populations contained large, SNP-free genomic regions that appear to have swept independently through the populations prior to the study without purging diversity elsewhere in the genome. Evidence for both genome-wide and gene-specific sweeps suggests that different models of bacterial speciation may apply to different populations coexisting in the same environment.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]; ORCiD logo [1];  [3]; ORCiD logo [4];  [5];  [6];  [7];  [1]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  3. Uppsala Univ. (Sweden). Dept. of Ecology and Genetics
  4. Univ. of Georgia, Athens, GA (United States). Dept. of Marine Sciences
  5. Michigan State Univ., East Lansing, MI (United States). Microbiology and Molecular Genetics
  6. Univ. of Wiscon, Milwaukee, WI (United States). School of Freshwater Sciences
  7. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology; Univ. of Wisconsin, Madison, WI (United States). Civil and Environmental Engineering
Publication Date:
Research Org.:
Dept. of Energy Joint Genome Inst., Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1347107
Alternate Identifier(s):
OSTI ID: 1379499
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 7; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bendall, Matthew L., Stevens, Sarah L.R., Chan, Leong-Keat, Malfatti, Stephanie, Schwientek, Patrick, Tremblay, Julien, Schackwitz, Wendy, Martin, Joel, Pati, Amrita, Bushnell, Brian, Froula, Jeff, Kang, Dongwan, Tringe, Susannah G., Bertilsson, Stefan, Moran, Mary A., Shade, Ashley, Newton, Ryan J., McMahon, Katherine D., and Malmstrom, Rex R. Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. United States: N. p., 2016. Web. doi:10.1038/ismej.2015.241.
Bendall, Matthew L., Stevens, Sarah L.R., Chan, Leong-Keat, Malfatti, Stephanie, Schwientek, Patrick, Tremblay, Julien, Schackwitz, Wendy, Martin, Joel, Pati, Amrita, Bushnell, Brian, Froula, Jeff, Kang, Dongwan, Tringe, Susannah G., Bertilsson, Stefan, Moran, Mary A., Shade, Ashley, Newton, Ryan J., McMahon, Katherine D., & Malmstrom, Rex R. Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. United States. doi:10.1038/ismej.2015.241.
Bendall, Matthew L., Stevens, Sarah L.R., Chan, Leong-Keat, Malfatti, Stephanie, Schwientek, Patrick, Tremblay, Julien, Schackwitz, Wendy, Martin, Joel, Pati, Amrita, Bushnell, Brian, Froula, Jeff, Kang, Dongwan, Tringe, Susannah G., Bertilsson, Stefan, Moran, Mary A., Shade, Ashley, Newton, Ryan J., McMahon, Katherine D., and Malmstrom, Rex R. Fri . "Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations". United States. doi:10.1038/ismej.2015.241. https://www.osti.gov/servlets/purl/1347107.
@article{osti_1347107,
title = {Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations},
author = {Bendall, Matthew L. and Stevens, Sarah L.R. and Chan, Leong-Keat and Malfatti, Stephanie and Schwientek, Patrick and Tremblay, Julien and Schackwitz, Wendy and Martin, Joel and Pati, Amrita and Bushnell, Brian and Froula, Jeff and Kang, Dongwan and Tringe, Susannah G. and Bertilsson, Stefan and Moran, Mary A. and Shade, Ashley and Newton, Ryan J. and McMahon, Katherine D. and Malmstrom, Rex R.},
abstractNote = {© 2016 International Society for Microbial Ecology. Multiple models describe the formation and evolution of distinct microbial phylogenetic groups. These evolutionary models make different predictions regarding how adaptive alleles spread through populations and how genetic diversity is maintained. Processes predicted by competing evolutionary models, for example, genome-wide selective sweeps vs gene-specific sweeps, could be captured in natural populations using time-series metagenomics if the approach were applied over a sufficiently long time frame. Direct observations of either process would help resolve how distinct microbial groups evolve. Here, from a 9-year metagenomic study of a freshwater lake (2005-2013), we explore changes in single-nucleotide polymorphism (SNP) frequencies and patterns of gene gain and loss in 30 bacterial populations. SNP analyses revealed substantial genetic heterogeneity within these populations, although the degree of heterogeneity varied by > 1000-fold among populations. SNP allele frequencies also changed dramatically over time within some populations. Interestingly, nearly all SNP variants were slowly purged over several years from one population of green sulfur bacteria, while at the same time multiple genes either swept through or were lost from this population. These patterns were consistent with a genome-wide selective sweep in progress, a process predicted by the 'ecotype model' of speciation but not previously observed in nature. In contrast, other populations contained large, SNP-free genomic regions that appear to have swept independently through the populations prior to the study without purging diversity elsewhere in the genome. Evidence for both genome-wide and gene-specific sweeps suggests that different models of bacterial speciation may apply to different populations coexisting in the same environment.},
doi = {10.1038/ismej.2015.241},
journal = {The ISME Journal},
number = 7,
volume = 10,
place = {United States},
year = {2016},
month = {1}
}

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