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Horizontal gene transfer, genome innovation and evolution

Nature Reviews Microbiology volume 3, pages 679–687 (2005)Cite this article

Key Points

  • 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.

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.

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Figure 1: The effects of gene transfer on sequence divergence.
Figure 2: The tree of life.
Figure 3: Comparison of two explanations for unexpected phylogenetic distribution.
Figure 4: Graphical schema for the quantification and modelling of recombination with divergent DNA and horizontal gene transfer.

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Acknowledgements

We thank O. Zhaxybayeva, K. Nielsen, P. Lapierre, W.F. Doolittle, J. Lawrence and F.M. Cohan for many stimulating and relevant discussions. Work in J.P.G.'s laboratory was supported by the National Science Foundation's Microbial Genetics programme and the NASA Applied Information Systems Research and Exobiology Programmes.

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  1. Department of Molecular and Cell Biology, University of Connecticut, Storrs, 06269-3125, Connecticut, USA

    J. Peter Gogarten & Jeffrey P. Townsend

  2. J. Peter Gogarten & Jeffrey P. Townsend

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  1. J. Peter Gogarten
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DATABASES

Entrez

Archaeoglobus fulgidus

Bacillus subtilis

Methanocaldococcus jannaschii

Methanothermobacter thermautotrophicus

Pyrococcus abyssi

Pyrococcus furiosus

Streptococcus pneumoniae

Streptococcus thermophilus

Thermotoga maritima

FURTHER INFORMATION

J. Peter Gogarten's laboratory

Jeffrey P. Townsend's laboratory

Glossary

TREE OF LIFE

The tree-like representation of the history of all living and extinct organisms.

MUTUALISM

An association between two organisms, often from different species, that benefits both partners.

RETICULATION

A network that is formed through the fusion of independent branches.

PHYLOGENY

The origin and evolution of a group of organisms, usually of species. Phylogenies are not necessarily tree-like. The term phylogeny is frequently applied to genes and different levels of taxonomic units. These are often labelled as operational taxonomic units.

GENE TREE

A depiction of the history of families of homologous genes. Intragenic recombination can gives rise to non-tree-like gene phylogenies.

HOMOLOGUES

Characters or sequences that are derived from the same ancestral feature.

SUPERTREES

Trees calculated from smaller trees with sets of overlapping operational taxonomic units.

ORTHOLOGUES

Homologues that are related to each other through a speciation event.

PURIFYING SELECTION

Kimura's neutral theory of molecular evolution posits that most variations observed at the molecular level do not provide a selective advantage or disadvantage. However, many nucleotide mutations are never observed in a population because they are associated with a strong selective disadvantage. This is the case for mutations that change a catalytically important amino acid. The selection that prevents these detrimental mutations from becoming fixed in a population is known as purifying selection.

BIPARTITION

A bipartition corresponds to an internal branch in a phylogenetic tree. A single bipartition divides the data (sequences, genomes or species) into two groups, but it does not consider the relationships within each of these groups.

LENTO PLOTS

Phylogenetic analyses using bipartition data named after G.M. Lento. For each bipartition, the bipartition spectra give the support for the bipartition as a histogram bar in the positive direction, and the support for all conflicting bipartitions as a bar in the negative direction.

GALLED TREES

Trees that contain local deviations from a strictly furcating pattern.

SELFISH OPERON THEORY

Explains the formation of operons through gene transfer. According to this theory, genes encoding parts of the same process become clustered because functionally unrelated intervening genes become useless and are deleted following a transfer, and because such clustered genes are more likely to be successfully transferred as a unit compared to genes encoded in distant parts of the genome.

ORFANS

Open reading frames that do not have a recognizable homologue among known sequences.

RIBOTYPE

In analogy to genotype and phenotype, the type of RNA in an organism, usually referring to the type of ribosomal RNA.

SELECTIVE SWEEP

Fixation of an advantageous character in a population. In the absence of recombination, the advantageous character carries with it the whole chromosome and erases diversity within the population.

MORONS

Genetic elements in lambdoid phages acquired through recent gene transfer. These genes are unrelated in function to the genes surrounding them. They were named morons because their addition to the phage genome means that there is 'more DNA' than there is without the element.

ILLEGITIMATE RECOMBINATION

Recombination between two non-homologous DNA segments. Usually, illegitimate recombination is fairly infrequent.

LEADING AND LAGGING DNA STRAND

DNA replication on the leading strand occurs continuously in a 5′ to 3′ direction, whereas DNA replication on the lagging strand occurs discontinuously through the synthesis of short Okazaki fragments.

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Gogarten, J., Townsend, J. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3, 679–687 (2005). https://doi.org/10.1038/nrmicro1204

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