Review
Lateral genomics

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Abstract

More than 20 complete prokaryotic genome sequences are now publicly available, each by itself an unparalleled resource for understanding organismal biology. Collectively, these data are even more powerful: they could force a dramatic reworking of the framework in which we understand biological evolution. It is possible that a single universal phylogenetic tree is not the best way to depict relationships between all living and extinct species. Instead a web- or net-like pattern, reflecting the importance of horizontal or lateral gene transfer between lineages of organisms, might provide a more appropriate visual metaphor. Here, I ask whether this way of thinking is really justified, and explore its implications.

Section snippets

What we might lose

If lateral gene transfer can affect all genes, and has affected some substantial fraction of genes over the past 3.8 billion years (since the origin of life), then much of what molecular phylogeneticists have hoped to accomplish is at risk, especially in the area of prokaryote evolution. These researchers can establish genealogical relationships only through analyses of genes that organisms share by virtue of descent from common ancestors. Yet even strains of a single prokaryotic ‘species’ can

Reality checks

These are serious blows to molecular phylogenetics, and lateral gene transfer might owe as much of its current popularity to these iconoclastic consequences as to the weight of evidence. Many of the data are indeed ‘anecdotal’ – isolated cases of incongruent trees that alone might have other explanations and seem but a drop in the genomic ocean6, 7, 8. Many of the exhaustive comparisons of two or more genomes base their shocking conclusions on sequence similarity scores alone, not trees15, 17,

What’s to be gained?

How would science benefit by whole-hearted adoption of the notion that prokaryotic evolution should be viewed as net-like, not tree-like? What might we gain by focusing on how genes themselves have evolved and the role that transfer of genes has played in generating the pattern of diversity we see in the microbial world? Note that there still will be groups of related organisms. As long as species split into new species frequently with respect to the rate of loss or gain (by transfer) of new

A new synthesis

Phylogeneticists, genomicists, molecular biologists and population geneticists have different perspectives on prokaryote evolution, and their respective literatures on lateral gene transfer seem disconnected. Come the millennium, we could hope for more disciplinary interpenetration and a more sophisticated understanding of how life’s history is sometimes like a tree and sometimes like a net. An evolutionary model in which novel genes transferred between populations play a major role in

Acknowledgements

I thank the Canadian Institute for Advanced Research for a Fellowship, the Medical Research Council of Canada for research support, and Dave Faguy, John Logsdon, and Andrew Roger for stimulating discussions about lateral gene transfer.

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