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  • Review Article
  • Published:

Horizontal gene transfer: building the web of life

Nature Reviews Genetics volume 16, pages 472–482 (2015)Cite this article

Subjects

Key Points

  • Many horizontal gene transfer (HGT) events are initially neutral or nearly neutral (slightly detrimental) and can later adapt to become beneficial to the recipient.

  • HGT events often involve compound mobile genetic elements that promote their own dissemination by associating with adaptive traits in the gene pool of the mobilome.

  • HGT is most frequent between closely related species with highly similar genome features.

  • Large multicellular eukaryotes can evolve through gene acquisitions by the associated microbiome, which responds more quickly than the host to variation in environmental conditions.

  • Endosymbiotic gene transfer frequently involves gene import not only from the endosymbiotic donor to the host, but also from other organisms that contribute to the initial establishment of the endosymbiotic relationship.

  • Novel traits that evolve through HGT can lead to the exploitation of new niches, prompting an adaptive radiation to exploit the new resource without competition.

Abstract

Horizontal gene transfer (HGT) is the sharing of genetic material between organisms that are not in a parent–offspring relationship. HGT is a widely recognized mechanism for adaptation in bacteria and archaea. Microbial antibiotic resistance and pathogenicity are often associated with HGT, but the scope of HGT extends far beyond disease-causing organisms. In this Review, we describe how HGT has shaped the web of life using examples of HGT among prokaryotes, between prokaryotes and eukaryotes, and even between multicellular eukaryotes. We discuss replacement and additive HGT, the proposed mechanisms of HGT, selective forces that influence HGT, and the evolutionary impact of HGT on ancestral populations and existing populations such as the human microbiome.

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Figure 1: Mechanisms of gene transfer.
Figure 2: Nested levels of selection on gene content.
Figure 3: HGT is more frequent between closely related species.
Figure 4: Structured exchange community.
Figure 5: HGT to the plant lineage.

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Acknowledgements

Work in the authors' laboratories was supported through grants from the National Science Foundation Grant (DEB 0830024), NASA Exobiology (NNX13AI03G), Binational Science Foundation (BSF 2013061), NSFC Oversea, Hong Kong, Macao collaborative grant (31328003), and the CAS/SAFEA International Partnership Program for Creative Research Teams. The authors would also like to thank K. Swithers for providing insightful comments and discussion pertaining to the body of this text.

Author information

Authors and Affiliations

  1. Department of Molecular and Cell Biology, University of Connecticut, 91 North Eagleville Road, Storrs, 06269–3125, Connecticut, USA

    Shannon M. Soucy & Johann Peter Gogarten

  2. Department of Biology, East Carolina University, Greenville, 27858, North Carolina, USA

    Jinling Huang

  3. Institute for Systems Genomics, University of Connecticut, 06269–3125, Connecticut, USA

    Johann Peter Gogarten

Authors
  1. Shannon M. Soucy
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  2. Jinling Huang
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  3. Johann Peter Gogarten
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Corresponding author

Correspondence to Johann Peter Gogarten.

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Supplementary information

Supplementary information S1 (table)

Summary of Horizontal Gene Transfers (HGTs) discussed in the main text. (PDF 173 kb)

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Glossary

Selfish genetic element

A gene or group of genes that enhance their own transmission and reproductive success without making a positive contribution to the host's fitness.

Microbiome

Following a definition ascribed to Joshua Lederberg this term is most often used to denote the collective genome of the indigenous microorganisms of a multicellular or unicellular host. However, the term has also been used by Lederberg and others to signify an ecological community of commensal, symbiotic and pathogenic microorganisms.

Phylogenetic conflict

Differences between the evolutionary history of a species and the evolutionary history of its genes are embodied by discrepancies in branching order between the species and the gene tree.

Genome streamlining

The reduction of genome size through relaxed selection and eventual loss of loci that are superfluous to the niche occupied by the organism.

Mobilome

The aggregate of mobile genetic elements in a genome, population or environment of interest.

Genome architecture imparting sequences

Strand-biased sequence motifs that are enriched towards the termini of replication; thought to direct proteins towards the termini.

Ecotypes

Genetically distinct subsets of organisms within a population or species, usually genetic differences correspond to niche adaptation.

Holobiont

A multicellular or unicellular host and its collective symbionts.

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Soucy, S., Huang, J. & Gogarten, J. Horizontal gene transfer: building the web of life. Nat Rev Genet 16, 472–482 (2015). https://doi.org/10.1038/nrg3962

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