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

Journal Article · · mBio (Online)
 [1];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology and Great Lakes Bioenergy Research Center

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.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF)
Grant/Contract Number:
FC02-07ER64494; AC02-05CH11231; T32 GM007215; DEB-0747002; MCB-0702025; U19 Al109673
OSTI ID:
1427704
Journal Information:
mBio (Online), Vol. 8, Issue 3; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 55 works
Citation information provided by
Web of Science

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How and Why to Build a Unified Tree of Life journal October 2017
Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 m of bioprospecting campaigns journal December 2019
Local Adaptation of Bacterial Symbionts within a Geographic Mosaic of Antibiotic Coevolution journal November 2019
Emerging evolutionary paradigms in antibiotic discovery journal September 2018
Phylogenomic analyses and distribution of terpene synthases among Streptomyces journal January 2019
Genome mining of biosynthetic and chemotherapeutic gene clusters in Streptomyces bacteria journal February 2020
Antibiotic Resistance Mechanisms in Bacteria: Relationships Between Resistance Determinants of Antibiotic Producers, Environmental Bacteria, and Clinical Pathogens journal November 2018
Detecting and prioritizing biosynthetic gene clusters for bioactive compounds in bacteria and fungi journal March 2019
AnnoTree: visualization and exploration of a functionally annotated microbial tree of life journal April 2019
The biosynthetic diversity of the animal world journal October 2019
Silencing cryptic specialized metabolism in Streptomyces by the nucleoid-associated protein Lsr2 journal June 2019
A Human Lung-Associated Streptomyces sp. TR1341 Produces Various Secondary Metabolites Responsible for Virulence, Cytotoxicity and Modulation of Immune Response journal January 2020
Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow journal October 2018
Within-Species Genomic Variation and Variable Patterns of Recombination in the Tetracycline Producer Streptomyces rimosus journal March 2019
Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces journal September 2019
Evolutionary dynamics of natural product biosynthesis in bacteria journal January 2020
Hidden antibiotics in actinomycetes can be identified by inactivation of gene clusters for common antibiotics journal September 2019
CRAGE enables rapid activation of biosynthetic gene clusters in undomesticated bacteria journal October 2019
Phylogenetic reconciliation reveals the natural history of glycopeptide antibiotic biosynthesis and resistance journal August 2019