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Title: Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces

Abstract

Lateral gene transfer (LGT) profoundly shapes the evolution of bacterial lineages. LGT across disparate phylogenetic groups and genome content diversity between related organisms suggest a model of bacterial evolution that views LGT as rampant and promiscuous. It has even driven the argument that species concepts and tree-based phylogenetics cannot be applied to bacteria. For this paper, we show that acquisition and retention of genes through LGT are surprisingly rare in the ubiquitous and biomedically important bacterial genusStreptomyces. Using a molecular clock, we estimate that theStreptomycesbacteria are ~380 million years old, indicating that this bacterial genus is as ancient as land vertebrates. Calibrating LGT rate to this geologic time span, we find that on average only 10 genes per million years were acquired and subsequently maintained. Over that same time span,Streptomycesaccumulated thousands of point mutations. By explicitly incorporating evolutionary timescale into our analyses, we provide a dramatically different view on the dynamics of LGT and its impact on bacterial evolution.Tree-based phylogenetics and the use of species as units of diversity lie at the foundation of modern biology. In bacteria, these pillars of evolutionary theory have been called into question due to the observation of thousands of lateral gene transfer (LGT) eventsmore » within and between lineages. Here, we show that acquisition and retention of genes through LGT are exceedingly rare in the bacterial genusStreptomyces, with merely one gene acquired inStreptomyceslineages every 100,000 years. These findings stand in contrast to the current assumption of rampant genetic exchange, which has become the dominant hypothesis used to explain bacterial diversity. Our results support a more nuanced understanding of genetic exchange, with LGT impacting evolution over short timescales but playing a significant role over long timescales. Deeper understanding of LGT provides new insight into the evolutionary history of life on Earth, as the vast majority of this history is microbial.« less

Authors:
 [1];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology and Great Lakes Bioenergy Research Center
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1427704
Grant/Contract Number:  
FC02-07ER64494; AC02-05CH11231; T32 GM007215; DEB-0747002; MCB-0702025; U19 Al109673
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; antibiotics; evolutionary genomics; horizontal gene transfer; molecular clock; species concepts

Citation Formats

McDonald, Bradon R., and Currie, Cameron R. Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces. United States: N. p., 2017. Web. doi:10.1128/mBio.00644-17.
McDonald, Bradon R., & Currie, Cameron R. Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces. United States. https://doi.org/10.1128/mBio.00644-17
McDonald, Bradon R., and Currie, Cameron R. Tue . "Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces". United States. https://doi.org/10.1128/mBio.00644-17. https://www.osti.gov/servlets/purl/1427704.
@article{osti_1427704,
title = {Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces},
author = {McDonald, Bradon R. and Currie, Cameron R.},
abstractNote = {Lateral gene transfer (LGT) profoundly shapes the evolution of bacterial lineages. LGT across disparate phylogenetic groups and genome content diversity between related organisms suggest a model of bacterial evolution that views LGT as rampant and promiscuous. It has even driven the argument that species concepts and tree-based phylogenetics cannot be applied to bacteria. For this paper, we show that acquisition and retention of genes through LGT are surprisingly rare in the ubiquitous and biomedically important bacterial genusStreptomyces. Using a molecular clock, we estimate that theStreptomycesbacteria are ~380 million years old, indicating that this bacterial genus is as ancient as land vertebrates. Calibrating LGT rate to this geologic time span, we find that on average only 10 genes per million years were acquired and subsequently maintained. Over that same time span,Streptomycesaccumulated thousands of point mutations. By explicitly incorporating evolutionary timescale into our analyses, we provide a dramatically different view on the dynamics of LGT and its impact on bacterial evolution.Tree-based phylogenetics and the use of species as units of diversity lie at the foundation of modern biology. In bacteria, these pillars of evolutionary theory have been called into question due to the observation of thousands of lateral gene transfer (LGT) events within and between lineages. Here, we show that acquisition and retention of genes through LGT are exceedingly rare in the bacterial genusStreptomyces, with merely one gene acquired inStreptomyceslineages every 100,000 years. These findings stand in contrast to the current assumption of rampant genetic exchange, which has become the dominant hypothesis used to explain bacterial diversity. Our results support a more nuanced understanding of genetic exchange, with LGT impacting evolution over short timescales but playing a significant role over long timescales. Deeper understanding of LGT provides new insight into the evolutionary history of life on Earth, as the vast majority of this history is microbial.},
doi = {10.1128/mBio.00644-17},
journal = {mBio (Online)},
number = 3,
volume = 8,
place = {United States},
year = {Tue Jun 06 00:00:00 EDT 2017},
month = {Tue Jun 06 00:00:00 EDT 2017}
}

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