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Review
. 2016 Jul 25:5:F1000 Faculty Rev-1805.
doi: 10.12688/f1000research.8737.1. eCollection 2016.

Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions

Eugene V Koonin  1
Affiliations
Review

Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions

Eugene V Koonin. F1000Res. .

Abstract

The wide spread of gene exchange and loss in the prokaryotic world has prompted the concept of 'lateral genomics' to the point of an outright denial of the relevance of phylogenetic trees for evolution. However, the pronounced coherence congruence of the topologies of numerous gene trees, particularly those for (nearly) universal genes, translates into the notion of a statistical tree of life (STOL), which reflects a central trend of vertical evolution. The STOL can be employed as a framework for reconstruction of the evolutionary processes in the prokaryotic world. Quantitatively, however, horizontal gene transfer (HGT) dominates microbial evolution, with the rate of gene gain and loss being comparable to the rate of point mutations and much greater than the duplication rate. Theoretical models of evolution suggest that HGT is essential for the survival of microbial populations that otherwise deteriorate due to the Muller's ratchet effect. Apparently, at least some bacteria and archaea evolved dedicated vehicles for gene transfer that evolved from selfish elements such as plasmids and viruses. Recent phylogenomic analyses suggest that episodes of massive HGT were pivotal for the emergence of major groups of organisms such as multiple archaeal phyla as well as eukaryotes. Similar analyses appear to indicate that, in addition to donating hundreds of genes to the emerging eukaryotic lineage, mitochondrial endosymbiosis severely curtailed HGT. These results shed new light on the routes of evolutionary transitions, but caution is due given the inherent uncertainty of deep phylogenies.

Keywords: Horizontal gene transfer; evolutionary transitions; microbial evolution; prokaryotes; statistical tree of life.

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Conflict of interest statement

Competing interests: The author declares that he has no competing interests.

No competing interests were disclosed.

Figures

Figure 1.
Figure 1.. Domestication of selfish genetic elements en route to dedicated vehicles for horizontal gene transfer.
The figure depicts the hypothetical stages of the evolutionary paths from a lytic phage to a gene transfer agent and from a small, high copy number plasmid to an integrative and conjugative element. Abbreviations: GTA, gene transfer agent; ICE, integrative and conjugative element.
Figure 2.
Figure 2.. Eukaryogenesis and horizontal gene transfer.
The figure presents the ‘endosymbiotic’ model of eukaryogenesis under which the host of the protomitochondrial endosymbiont was a typical archaeon albeit one with a relatively complex intracellular organization and numerous genes captured from bacteria via HGT. Abbreviations: HGT, horizontal gene transfer.
See this image and copyright information in PMC

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Grants and funding

The author’s research is supported by intramural funds of the US Department of Health and Human Services (to the National Library of Medicine).

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