Lateral Gene Transfer Dynamics in the Ancient Bacterial Genus Streptomyces.

Paul Keim,Cameron R. Currie,Bradon R. McDonald

doi:10.1128/mbio.00644-17

Paul Keim, Cameron R. Currie + Show 1 more

Open Access

https://doi.org/10.1128/mbio.00644-17

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Abstract

ABSTRACTLateral 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. Here, we show that acquisition and retention of genes through LGT are surprisingly rare in the ubiquitous and biomedically important bacterial genus Streptomyces. Using a molecular clock, we estimate that the Streptomyces bacteria 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, Streptomyces accumulated 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.

Highlights

Lateral gene transfer (LGT) profoundly shapes the evolution of bacterial lineages
We show that acquisition and retention of genes through lateral gene transfer (LGT) are exceedingly rare in the bacterial genus Streptomyces, with merely one gene acquired in Streptomyces lineages every 100,000 years
Using Streptomyces divergence times rather than sequence similarity provides a new perspective on the rate of LGT and its potential impact on bacterial evolution over small and large evolutionary timescales

Summary

Introduction

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. IMPORTANCE 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. Analyses that span the species level to intermediate, genuslevel diversity provide opportunities to investigate the combined effects of LGT and mutation across physiologically similar organisms that are diverging, either due to neutral processes or due to selective pressures in the different ecological niches that they occupy This has the advantage of providing sufficient diversity to reliably detect LGT and identify trends that occur over evolutionary timescales, such as the loss of acquired genes that are selectively neutral or mildly deleterious [16,17,18]. Focusing on a single genus that has broadly similar life history traits and is found in diverse environments enables easier detection of rapidly evolving diversity and ecologically relevant variation

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