Biased gene transfer and its implications for the concept of lineage

Cheryl P Andam,J Peter Gogarten

doi:10.1186/1745-6150-6-47

Abstract

BackgroundIn the presence of horizontal gene transfer (HGT), the concepts of lineage and genealogy in the microbial world become more ambiguous because chimeric genomes trace their ancestry from a myriad of sources, both living and extinct.ResultsWe present the evolutionary histories of three aminoacyl-tRNA synthetases (aaRS) to illustrate that the concept of organismal lineage in the prokaryotic world is defined by both vertical inheritance and reticulations due to HGT. The acquisition of a novel gene from a distantly related taxon can be considered as a shared derived character that demarcates a group of organisms, as in the case of the spirochaete Phenylalanyl-tRNA synthetase (PheRS). On the other hand, when organisms transfer genetic material with their close kin, the similarity and therefore relatedness observed among them is essentially shaped by gene transfer. Studying the distribution patterns of divergent genes with identical functions, referred to as homeoalleles, can reveal preferences for transfer partners. We describe the very ancient origin and the distribution of the archaeal homeoalleles for Threonyl-tRNA synthetases (ThrRS) and Seryl-tRNA synthetases (SerRS).ConclusionsPatterns created through biased HGT can be undistinguishable from those created through shared organismal ancestry. A re-evaluation of the definition of lineage is necessary to reflect genetic relatedness due to both HGT and vertical inheritance. In most instances, HGT bias will maintain and strengthen similarity within groups. Only in cases where HGT bias is due to other factors, such as shared ecological niche, do patterns emerge from gene phylogenies that are in conflict with those reflecting shared organismal ancestry.ReviewersThis article was reviewed by W. Ford Doolittle, François-Joseph Lapointe, and Frederic Bouchard.

Highlights

In the presence of horizontal gene transfer (HGT), the concepts of lineage and genealogy in the microbial world become more ambiguous because chimeric genomes trace their ancestry from a myriad of sources, both living and extinct
A recent study reported that the genes involved in the degradation of an algal polysaccharide were transferred via seaweed consumption from marine bacteria to the gut bacterium Bacteroides isolated from Japanese individuals [2]
HGTs contribute to bacterial adaptation by bringing in novel genes into the genome, the majority of transfers may be nearly neutral to the recipient, impacting the gene content without conferring any immediate benefits to the recipient organisms [7]

Summary

Introduction

In the presence of horizontal gene transfer (HGT), the concepts of lineage and genealogy in the microbial world become more ambiguous because chimeric genomes trace their ancestry from a myriad of sources, both living and extinct. HGTs contribute to bacterial adaptation by bringing in novel genes into the genome, the majority of transfers may be nearly neutral to the recipient, impacting the gene content without conferring any immediate benefits to the recipient organisms [7]. Some of these horizontally acquired genes, can be considered as a pre-adaptation, which the recipient can potentially use

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