A natural barrier to lateral gene transfer from prokaryotes to eukaryotes revealed from genomes: the 70% rule.

William F Martin,Chuan Ku

doi:10.1186/s12915-016-0315-9

Abstract

BackgroundThe literature harbors many claims for lateral gene transfer (LGT) from prokaryotes to eukaryotes. Such claims are typically founded in analyses of genome sequences. It is undisputed that many genes entered the eukaryotic lineage via the origin of mitochondria and the origin of plastids. Claims for lineage-specific LGT to eukaryotes outside the context of organelle origins and claims of continuous LGT to eukaryotic lineages are more problematic. If eukaryotes acquire genes from prokaryotes continuously during evolution, then sequenced eukaryote genomes should harbor evidence for recent LGT, like prokaryotic genomes do.ResultsHere we devise an approach to investigate 30,358 eukaryotic sequences in the context of 1,035,375 prokaryotic homologs among 2585 phylogenetic trees containing homologs from prokaryotes and eukaryotes. Prokaryote genomes reflect a continuous process of gene acquisition and inheritance, with abundant recent acquisitions showing 80–100 % amino acid sequence identity to their phylogenetic sister-group homologs from other phyla. By contrast, eukaryote genomes show no evidence for either continuous or recent gene acquisitions from prokaryotes. We find that, in general, genes in eukaryotic genomes that share ≥70 % amino acid identity to prokaryotic homologs are genome-specific; that is, they are not found outside individual genome assemblies.ConclusionsOur analyses indicate that eukaryotes do not acquire genes through continual LGT like prokaryotes do. We propose a 70 % rule: Coding sequences in eukaryotic genomes that share more than 70 % amino acid sequence identity to prokaryotic homologs are most likely assembly or annotation artifacts. The findings further uncover that the role of differential loss in eukaryote genome evolution has been vastly underestimated.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0315-9) contains supplementary material, which is available to authorized users.

Highlights

The literature harbors many claims for lateral gene transfer (LGT) from prokaryotes to eukaryotes
Cognizant biologists have learned one thing for certain about LGT: Not all papers bearing claims for LGT are evidence for the workings of LGT, especially when it comes to LGT from prokaryotes to eukaryotes, which is the focus of our paper
We showed that acquisitions of prokaryotic genes by the eukaryotic lineage correspond to endosymbiotic events [50] and that many of the patterns of "patchy" gene distributions that some reports interpret as evidence for LGT [51, 52] are more likely the result of differential loss [50] superimposed upon vertical inheritance

Summary

Introduction

The literature harbors many claims for lateral gene transfer (LGT) from prokaryotes to eukaryotes. Such claims are typically founded in analyses of genome sequences. Apart from the natural and well-documented process of gene acquisition from the ancestors of organelles in the wake of mitochondrial and plastid origin — endosymbiotic gene transfer [11, 12] — how much prokaryote-toeukaryote LGT, if any, is really going on in nature?. A great deal is known about the genes and proteins that moderate these LGT mechanisms in prokaryotes [19,20,21]. These LGT mechanisms merely introduce DNA into the prokaryotic cell; whether or not it recombines into the genome is governed by the genes and proteins that mediate DNA insertion and/or recombination [22, 23]

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Conclusion