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Ancient horizontal gene transfer

Nature Reviews Genetics volume 4, pages 121–132 (2003)Cite this article

Key Points

  • Ancient horizontal gene transfer (HGT) is the transfer of genes between the three domains of life: the Archaea, the Bacteria and the eukaryotes.

  • Ancient HGT seems to have been a main force in organism evolution because examples of gene transfers exist for many combinations of species of Archaea, Bacteria and eukaryotes.

  • The extent of HGT and the mechanisms surrounding it are still open to debate because there are no broadly occurring extant examples of inter-domain gene transfers.

  • To many researchers, ancient HGT has seriously challenged the concept of the universal tree of life.

  • Methods for detecting HGT include phylogenetic analysis, nucleotide composition analysis, analysis of gene distributions and homology analysis.

  • Phylogenetic analysis remains the best method for establishing the occurrence of ancient HGT, although there are caveats about the methodology and the limited availability of sequence data from evolutionarily pivotal groups.

  • Homology analysis of HGT, based on the comparisons of BLAST scores, can lead to overestimates or incorrect assignment of HGT events.

  • Phylogenetic analyses based on whole-genome data generally support the basic tenets of the universal tree of life.

  • The monophyly of the three domains of life is supported by proteins that show a closer evolutionary relationship between the Archaea and the eukaryotes.

  • Eukaryotic genes that are similar to their bacterial counterparts might have evolved as a consequence of endosymbiotic events that evidently led to the evolution of organelles, such as mitochondria and plastids. However, many genes involved in mitochondrial or chloroplast maintenance did not evolve from putative bacterial endosymbionts (α-proteobacteria and cyanobacteria, respectively).

  • New genomic data, in particular from protists that have secondarily lost their mitochondria, will show the extent of ancient HGT.

Abstract

The cornerstone of Charles Darwin's theory of evolution is the vertical inheritance of traits from parent to offspring across successive generations. However, molecular evolutionary biologists have shown that extensive horizontal (also known as lateral) gene transfer (HGT) can occur between distantly related species. Comparative sequence analyses of genomes indicates that the universal tree of life might be at risk because of pervasive, ancient HGT. Considerable debate now ensues about the role of HGT in genome evolution. At stake are a fundamental understanding of how life evolved and a deeper knowledge of the functioning of all genomes, including that of humans.

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Figure 1: Phylogenetic tree for glutamine synthetase indicates HGT between the three domains.
Figure 2: Phylogeny of methionyl-tRNA synthetase.

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Acknowledgements

The support of GlaxoSmithKline R & D, Genetics Research, Bioinformatics Division is gratefully acknowledged. I thank two anonymous reviewers for their comments on this manuscript.

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  1. Bioinformatics Division, GlaxoSmithKline, 1250 South Collegeville Road, UP1345, Collegeville, 19426, Pennsylvania, USA

    James R. Brown

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FURTHER INFORMATION

The European Ribosomal RNA Database

The Institute for Genome Research

Mitochondria Genome Project (MITOP)

National Center for Biotechnology Information

Phylogeny Programmes, University of Washington

PlasmoDB — The Plasmodium Genome Resource

The Tree of Life

Treeview

The Wellcome Trust Sanger Institute

Glossary

UNIVERSAL TREE OF LIFE

The relationships of all living species based on the phylogeny of ribosomal RNA molecules. The universal tree topology shows the three domains of life to be separate and unique (monophyletic). Independent protein phylogenies show that the Archaea and the eukaryotes are sister groups, so the tree must be rooted in the Bacteria.

ROOTING

Orientating a phylogenetic tree using an outgroup taxon to determine the order of evolution in the group of taxa of interest.

MONOPHYLY

Monophyletic taxa are derived from a single common ancestor.

ORTHOLOGUE

A homologous gene that is derived from a speciation event or by vertical descent.

PARAPHYLY

Paraphyletic taxa are derived from a single common ancestor but the group does not include all of the descendants.

POLYPHYLY

Polyphyletic taxa are descended from different ancestors.

PROTEOBACTERIA

A group of Gram-negative bacteria, often called purple bacteria, that includes Escherichia coli. They are subdivided into α-, β-, γ-, δ- and ε-proteobacteria. The α-proteobacteria are believed to be the endosymbiont progenitors of mitochondria.

OUTGROUP

A species or sequence that is known to diverge earlier than the other species or sequences being analysed.

DENDOGRAMS

A branching tree-like diagram.

16S SSU RIBOSOMAL RNA

Ribosomal RNA (rRNA) molecules of discrete sizes that, along with ribosomal proteins, comprise the ribosomes of prokaryotes and eukaryotes. Small subunit (SSU) 16S rRNA is widely used as a phylogenetic marker.

PARALOGUES

Homologous genes that have evolved from a gene duplication.

GRAM-POSITIVE BACTERIA

A group of bacteria that take up Gram stains during histological preparation for identification. Bacillus subtilis, as well as Streptococci and Staphylococci pathogens, belong to this group.

PROTISTS

Single-celled eukaryotic organisms with, or without, organelles.

ARCHEZOA

A group of protists that lack mitochondria and, therefore, were previously thought to have evolved before endosymbiosis. However, it is now believed that the Archezoa secondarily lost their mitochondria.

CONVERGENCE

The independent evolution of similar features (such as genes) in evolutionarily distinct lineages.

AMELIORATE

The process by which, over successive generations, the nucleotide composition of a horizontally transferred DNA segment becomes identical to that of the host genome.

70 kDa HEAT-SHOCK PROTEIN

(HSP70). A member of a large set of proteins that are expressed in response to several physical and chemical stresses.

COMPETENCY

The ability of prokaryotes to stably incorporate exogenous DNA fragments from the environment into their genomes.

TUMOUR-INDUCING (TI) PLASMID

The plasmid responsible for transferring DNA from Agrobacterium to plant cells. This is the only known natural example of inter-domain DNA transfer.

ENDOSYMBIONT

An intracellular organism that contributes to the survival of the host cell and depends on the host for its own persistence.

PSEUDOGENE

A DNA sequence that was derived originally from a functional protein-coding gene that has lost its function, owing to the presence of one, or more, inactivating mutations.

FIXATION

The accumulation of a gene or an allele to a frequency of 100% in a population.

NEIGHBOUR-JOINING METHOD

A distance-based molecular phylogenetic method that involves the sequential addition of taxa and the minimization of branch lengths, but does not assume a molecular clock.

MAXIMUM PARSIMONY

A mathematical method for determining the evolutionary relationship between proteins, which takes account of the minimum number of mutations that are required to effect the transition from one member of the family to another.

RIBOSOMAL PROTEIN S14

A protein associated with the small (30S) ribosomal subunit that has a possible role in ribosome assembly and is associated with the peptidyl transferase centre.

PYRUVATE:FERREDOXIN OXIDOREDUCTASE GENES

An iron sulphur protein that functions in central metabolism by decarboxylating pyruvate to acetyl-CoA in anaerobic eukeryotes and bacteria.

GLUTAMINE SYNTHETASE

An essential enzyme for ammonia assimilation and glutamine biosynthesis.

REVERSE GYRASE

An enzyme that is responsible for generating positive DNA supercoils in the chromosomes of thermophilic Archaea and Bacteria. It has resulted from the fusion of two proteins — a partial helicase and a type I DNA topoisomerase.

CATALASE-PEROXIDASE

A family of enzymes, found in the Bacteria and the Archaea, that are involved in the removal of cellular peroxide molecules.

TWO-COMPONENT SIGNAL-TRANSDUCTION SYSTEMS

Two interacting proteins — a histidine kinase with an extracellular domain and an intracellular response regulator — that form the central signalling pathway in bacteria.

GLUTAMINYL-tRNA SYNTHETASE

A member of the class I aminoacyl-tRNA synthetase family that is responsible for attaching the amino acid glutamine to its cognate tRNA.

PARABASLIDS

Single-celled eukaryotes that usually live as parasites or symbionts in animals. They lack mitochondria but have hydrogen-producing organelles called hydrogenosomes. Trichonomas vaginalis is a member species.

GENETIC DRIFT

Changes in gene frequencies in a population due to chance alone.

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Brown, J. Ancient horizontal gene transfer. Nat Rev Genet 4, 121–132 (2003). https://doi.org/10.1038/nrg1000

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