Abstract

A large-scale survey of potential recently acquired integrative elements in 119 archaeal and bacterial genomes reveals that many recently acquired genes have originated from integrative elements

Highlights

  • Archaeal and bacterial genomes contain a number of genes of foreign origin that arose from recent horizontal gene transfer, but the role of integrative elements (IEs), such as viruses, plasmids, and transposable elements, in this process has not been extensively quantified

  • It is widely assumed that most cellular genomes harbor IEs, but their proportion has not been quantified on a large scale

  • We show that the use of a Markov model (MM)-based method to identify open reading frame (ORF) with atypical composition in groups of closely related genomes, coupled to the identification of cluster of genes with atypical composition (CAG), their genomic context and gene content, is a powerful approach to identify foreign elements that have recently integrated into archaeal and bacterial genomes

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Summary

Introduction

Archaeal and bacterial genomes contain a number of genes of foreign origin that arose from recent horizontal gene transfer, but the role of integrative elements (IEs), such as viruses, plasmids, and transposable elements, in this process has not been extensively quantified It is not known whether IEs play an important role in the origin of ORFans (open reading frames without matches in current sequence databases), whose proportion remains stable despite the growing number of complete sequenced genomes. Consistent with this hypothesis, Daubin and Ochman [14] noticed that ORFans from γ-Proteobacteria share several features with viral ORFans (for example, small size, AT-rich) and suggested that 'ORFans in the genomes of free-living microorganisms apparently derive from bacteriophages and occasionally become established by assuming roles in key cellular functions.' Yin and Fisher [10] recently reported that, on average, only 2.8% of all cellular ORFans have homologues in current viral sequence databases, raising doubts about the hypothesis of a viral origin of ORFans, and proposed that 'lateral transfer from viruses alone is unlikely to explain the origin of the majority of ORFans in the majority of prokaryotes and other, not necessarily exclusive, mechanisms are likely to better explain the origin of the increasing number of ORFans.' More recently, the same authors found that only 18% of viral ORFans (ORFs present in only one viral genome) have homologues in archaeal or bacterial genomes, and concluded that 'phage ORFans play a lesser role in horizontal gene transfer to prokaryotes' [12]

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