Focus on Horizontal Gene Transfer

Nature Reviews Microbiology 3, 675-678 (2005); doi:10.1038/nrmicro1253
September 2005 Vol 3 No 9 FOREWORD

Barth F. Smets1 & Tamar Barkay2

(Note: this is an abstracted version of the Foreword to the Focus on HGT issue, which is available through subscription)

Transgenic organisms hold great promise for improved food production. Concerns about HGT from these organisms have, however, shrouded and limited their application. The appropriateness of current risk-assessment models and monitoring protocols to depict the potential for recombinant gene transfer through HGT to unintended target organisms are issues that are subject to fierce debate. A fuller understanding of the mechanisms and constraints for HGT could ensure development of effective gene-containment strategies within target species and ultimately allow the full realization of the promise of biotechnology.

While the concept of HGT frequently engenders joyful intellectual contemplation and lively philosophical exchanges, it carries more than just ivory tower relevance. The evidence indicates that HGT is a central process in microbial activities that control our health and the environment, and that it holds promise as a tool for their improvement.

The ability to control harmful effects and to enhance desired attributes of HGT depends on the integrated understanding of HGT as a continuum spanning steps 1-5 of the gene-transfer paradigm (Fig. 1) and its integration within an ecological framework.

Several scientific disciplines are addressing HGT, each providing their unique perspective and each using different approaches and methodologies. In general, evolutionary biology considers HGT events that have gone to completion (that is, through step 5). Molecular ecology, on the other hand, tends to focus on HGT events at the level of step 4. Finally, molecular biology is most interested in the mechanisms controlling steps 1 through 4. With such distinct perspectives, conflicts are bound to arise, but opportunities for synthesis are certain to emerge. The goal of this Focus issue of Nature Reviews Microbiology is to present HGT from the perspective of these different disciplines and to provide a path towards the construction of a holistic picture of HGT and its effects on extant microbial communities. We argue that efforts towards such synthesis will accelerate our understanding of the mechanisms and factors that control HGT, the impacts of HGT on the evolutionary history of prokaryotes, the effect of HGT on microbial interactions with each other and their environment, and the means by which HGT can be controlled to affect human and environmental health.

Conclusions

Clearly, HGT has contributed to prokaryotic evolution and is an ongoing process in extant microbial communities. The 'mobilome' is therefore receiving unprecedented attention from a range of scientific disciplines. The purpose of this themed issue is to synthesize the state of our knowledge from these different perspectives. We believe that such a synthesis will be mandatory to obtain a more precise appraisal of HGT as a force in shaping prokaryotic evolution, diversity and activity and, therefore, in modulating the history of life on Earth.

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Abstracts from two items in the Focus on HGT issue:

HORIZONTAL GENE TRANSFER, GENOME INNOVATION AND EVOLUTION
Nature Reviews Microbiology 3, 679-687 (2005); doi:10.1038/nrmicro1204
sept 2005

J. Peter Gogarten & Jeffrey P. Townsend

Abstract

To what extent is the tree of life the best representation of the evolutionary history of microorganisms? Recent work has shown that, among sets of prokaryotic genomes in which most homologous genes show extremely low sequence divergence, gene content can vary enormously, implying that those genes that are variably present or absent are frequently horizontally transferred. Traditionally, successful horizontal gene transfer was assumed to provide a selective advantage to either the host or the gene itself, but could horizontally transferred genes be neutral or nearly neutral? We suggest that for many prokaryotes, the boundaries between species are fuzzy, and therefore the principles of population genetics must be broadened so that they can be applied to higher taxonomic categories.
Summary

* Tree-like binary schemes for taxonomic classification have an illustrious history in evolutionary biology, but they do not provide a complete representation of life's history, especially for prokaryotes. Some genes within an organism have tree-like histories that differ from the histories of other genes within the same organism, owing to horizontal gene transfer (HGT). Although all types of genes can be susceptible to horizontal transfer, different types of genes and groups of organisms vary in their propensity for HGT.
* Phylogenetic analysis of a concatenation of genes with differing gene histories has the potential to create artifactual histories that reflect neither the history of the organism nor the history of the gene. Methods of phylogenetic reconstruction that do not insist on tree-like phylogenies but explicitly allow for reticulation events promise to yield a more realistic reconstruction of much of life's history.
* Phylogenetic reconstruction methodology — and therefore the accurate detection of historical HGT events — can benefit from a better understanding of phylogenetic signal as it relates to rates of change of characters and taxonomic sampling.
* The abundance and atypical composition of genes that are transient in prokaryotic genomes such as that of Escherichia coli lead one to wonder whether such genes (and horizontally transferred genes in general) are deleterious, selected for or neutral on transfer. Recent studies seem to indicate extensive gene swapping and few selective sweeps, arguing that many transferred genes might be nearly neutral in selective effect.
* Quantitative methods for analysing the frequency and nature of HGT events in microbial communities are needed. Quantitative descriptions yield precise predictions that can be tested statistically, and will help to resolve disputes about the frequency and importance of HGT to microbial evolution by improving clarity of expression, as well as enforcing statistical decision criteria.

Web Link: http://www.nature.com/nrmicro/journal/v3/n9/abs/
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MECHANISMS OF, AND BARRIERS TO, HORIZONTAL GENE TRANSFER BETWEEN BACTERIA
Nature Reviews Microbiology 3, 711-721 (2005); doi:10.1038/nrmicro1234

sept 2005

Christopher M. Thomas & Kaare M. Nielsen

Abstract

Bacteria evolve rapidly not only by mutation and rapid multiplication, but also by transfer of DNA, which can result in strains with beneficial mutations from more than one parent. Transformation involves the release of naked DNA followed by uptake and recombination. Homologous recombination and DNA-repair processes normally limit this to DNA from similar bacteria. However, if a gene moves onto a broad-host-range plasmid it might be able to spread without the need for recombination. There are barriers to both these processes but they reduce, rather than prevent, gene acquisition.
Summary

* Mutation and horizontal gene transfer (HGT) continually give rise to new bacterial genotypes. Infrequently, such new bacterial genotypes establish and spread in the larger population through either positive selection or random genetic drift. Therefore, bacterial genomes are in a constant state of flux, and any segment of DNA in a large bacterial population might have the opportunity to be horizontally transferred.
* Three main mechanisms of HGT have been described: natural transformation, the uptake of free DNA in competent bacteria, exhibited by about 1% of validly described bacterial species; transduction, the transfer of bacterial DNA between a bacteriophage-infected bacterium and a bacteriophage-susceptible bacterium; and conjugation, the transfer of mobile genetic elements by pili structures assembled between two adjacently located bacteria.
* A number of factors limit the transfer, uptake and stabilization of foreign DNA molecules acquired by bacteria. These include limited release and stability of adaptive DNA in the environment; limits on competence development; limits on host range of the transfer and maintenance mechanism of mobile genetic elements; recipient restriction enzyme activity; and limited ability of foreign DNA to integrate into a replicating genetic element owing to a lack of DNA sequence similarity.
* Homologous recombination depends on the incoming DNA containing regions between 25 and 200 bp in length, depending on the system, of high similarity to the recipient genome. Dependence on DNA sequence similarity for recombination between species is relaxed in some mutator strains. DNA acquisition through double-stranded breaks and end-joining — illegitimate recombination — applies more to integration of circular DNA than linear fragments.
* Most of the understanding of the processes facilitating HGT and their frequencies of occurrence have come from well designed laboratory studies of a few model bacterial species. These studies have proven suited to resolve the basic biological mechanisms involved, but fail to encompass the environmental variables involved. We have still to develop a quantitative and qualitative understanding of ongoing gene-transfer processes occurring under natural conditions. Biologically significant gene-transfer processes might occur at temporospatial scales that current methodology do not allow us to monitor.

Web Link: http://www.nature.com/nrmicro/journal/v3/n9/abs/
nrmicro1234_fs.html