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Title: Population Genomic Analysis of Strain Variation in Leptospirillum Group II Bacteria Involved in Acid Mine Drainage Formation

Abstract

Deeply sampled community genomic (metagenomic) datasets enable comprehensive analysis of heterogeneity in natural microbial populations. In this study, we used sequence data obtained from the dominant member of a lowdiversity natural chemoautotrophic microbial community to determine how coexisting closely related individuals differ from each other in terms of gene sequence and gene content, and to uncover evidence of evolutionary processes that occur over short timescales. DNA sequence obtained from an acid mine drainage biofilm was reconstructed, taking into account the effects of strain variation, to generate a nearly complete genome tiling path for a Leptospirillum group II species closely related to L. ferriphilum (sampling depth ;203). The population is dominated by one sequence type, yet we detected evidence for relatively abundant variants (.99.5% sequence identity to the dominant type) at multiple loci, and a few rare variants. Blocks of other Leptospirillum group II types (;94% sequence identity) have recombined into one or more variants. Variant blocks of both types are more numerous near the origin of replication. Heterogeneity in genetic potential within the population arises from localized variation in gene content, typically focused in integrated plasmid/phage-like regions. Some laterally transferred gene blocks encode physiologically important genes, including quorum-sensing genes ofmore » the LuxIR system. Overall, results suggest inter- and intrapopulation genetic exchange involving distinct parental genome types and implicate gain and loss of phage and plasmid genes in recent evolution of this Leptospirillum group II population. Population genetic analyses of single nucleotide polymorphisms indicate variation between closely related strains is not maintained by positive selection, suggesting that these regions do not represent adaptive differences between strains. Thus, the most likely explanation for the observed patterns of polymorphism is divergence of ancestral strains due to geographic isolation, followed by mixing and subsequent recombination.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [1]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  2. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Chemistry Directorate
Publication Date:
Research Org.:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF)
OSTI Identifier:
1627157
Grant/Contract Number:  
FG02-05ER64134; DEB-0221768
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online); Journal Volume: 6; Journal Issue: 7; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Genomics; leptospirillum; single nucleotide polymers; DNA-binding proteins; population genetics; metagenomics; genome analysis; viral genomics

Citation Formats

Simmons, Sheri L., DiBartolo, Genevieve, Denef, Vincent J., Goltsman, Daniela S. Aliaga, Thelen, Michael P., and Banfield, Jillian F. Population Genomic Analysis of Strain Variation in Leptospirillum Group II Bacteria Involved in Acid Mine Drainage Formation. United States: N. p., 2008. Web. doi:10.1371/journal.pbio.0060177.
Simmons, Sheri L., DiBartolo, Genevieve, Denef, Vincent J., Goltsman, Daniela S. Aliaga, Thelen, Michael P., & Banfield, Jillian F. Population Genomic Analysis of Strain Variation in Leptospirillum Group II Bacteria Involved in Acid Mine Drainage Formation. United States. https://doi.org/10.1371/journal.pbio.0060177
Simmons, Sheri L., DiBartolo, Genevieve, Denef, Vincent J., Goltsman, Daniela S. Aliaga, Thelen, Michael P., and Banfield, Jillian F. Tue . "Population Genomic Analysis of Strain Variation in Leptospirillum Group II Bacteria Involved in Acid Mine Drainage Formation". United States. https://doi.org/10.1371/journal.pbio.0060177. https://www.osti.gov/servlets/purl/1627157.
@article{osti_1627157,
title = {Population Genomic Analysis of Strain Variation in Leptospirillum Group II Bacteria Involved in Acid Mine Drainage Formation},
author = {Simmons, Sheri L. and DiBartolo, Genevieve and Denef, Vincent J. and Goltsman, Daniela S. Aliaga and Thelen, Michael P. and Banfield, Jillian F.},
abstractNote = {Deeply sampled community genomic (metagenomic) datasets enable comprehensive analysis of heterogeneity in natural microbial populations. In this study, we used sequence data obtained from the dominant member of a lowdiversity natural chemoautotrophic microbial community to determine how coexisting closely related individuals differ from each other in terms of gene sequence and gene content, and to uncover evidence of evolutionary processes that occur over short timescales. DNA sequence obtained from an acid mine drainage biofilm was reconstructed, taking into account the effects of strain variation, to generate a nearly complete genome tiling path for a Leptospirillum group II species closely related to L. ferriphilum (sampling depth ;203). The population is dominated by one sequence type, yet we detected evidence for relatively abundant variants (.99.5% sequence identity to the dominant type) at multiple loci, and a few rare variants. Blocks of other Leptospirillum group II types (;94% sequence identity) have recombined into one or more variants. Variant blocks of both types are more numerous near the origin of replication. Heterogeneity in genetic potential within the population arises from localized variation in gene content, typically focused in integrated plasmid/phage-like regions. Some laterally transferred gene blocks encode physiologically important genes, including quorum-sensing genes of the LuxIR system. Overall, results suggest inter- and intrapopulation genetic exchange involving distinct parental genome types and implicate gain and loss of phage and plasmid genes in recent evolution of this Leptospirillum group II population. Population genetic analyses of single nucleotide polymorphisms indicate variation between closely related strains is not maintained by positive selection, suggesting that these regions do not represent adaptive differences between strains. Thus, the most likely explanation for the observed patterns of polymorphism is divergence of ancestral strains due to geographic isolation, followed by mixing and subsequent recombination.},
doi = {10.1371/journal.pbio.0060177},
journal = {PLoS Biology (Online)},
number = 7,
volume = 6,
place = {United States},
year = {Tue Jul 22 00:00:00 EDT 2008},
month = {Tue Jul 22 00:00:00 EDT 2008}
}

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