Horizontal gene transfer in eukaryotic evolution

Key Points

  • Horizontal gene transfer (HGT; also known as lateral gene transfer) is the non-sexual movement of genetic information between genomes. Incoming DNA or RNA can replace existing genes, or can introduce new genes into a genome.

  • HGT in eukaryotes has been overshadowed by its prevalence in bacterial genomes, but a large number of cases involving eukaryotes have nevertheless been described. Its impact is variable from lineage to lineage, and many of the lineages that are most affected by HGT are the least studied at the genomic level (for example, protists), so the importance of HGT will probably increase as databases expand.

  • There is an extensive history of endosymbiosis in eukaryotic evolution. Endosymbiosis-derived organelles like mitochondria and plastids contributed many genes to the nucleus, and subsequent endosymbioses in plastid evolution has also allowed genes to move between eukaryotes. Other persistent endosymbionts (for example, Wolbachia) have now been recognized as a major source of DNA in the nuclei of their hosts.

  • HGT without symbiosis is also common, most documented cases involve genes from bacteria being present in the nucleus. Their prevalence might be because they are more obvious than genes from another eukaryote, but bacteria might be the major source of new genes owing to their abundance.

  • The complex distribution of some previously 'simple' bacteria–eukaryote transfers suggests eukaryote–eukaryote transfers might be more common than is appreciated. Extensive exchange of genetic information between mitochondrial genomes of plants is now well documented, providing the highest known levels of eukaryote–eukaryote transfer.

  • In many instances, genes acquired by HGT have clear functional or ecological implications for their new host. For example, several highly derived anaerobes have acquired many metabolic genes from bacteria that probably contributed to their adaptation to anaerobic environments.

  • Although the confounding effect of HGT on phylogenetic reconstruction is well known, ancient HGT events have been recognized as useful clues to organismal relationships. Several ancient HGT events are shared by two or more major eukaryotic lineages, such as animals and fungi, or chromalveolates, and such shared characters (interpreted with caution) help understand the tree of eukaryotes.

  • Recent transfers are observed more often than ancient ones. This might be a sampling bias, but could indicate that transferred genes provide a transient advantage but are frequently not retained over prolonged periods of time. If so, the impact of HGT in the long term might not be so profound.

  • Even with the growth of genomic data, several questions remain challenging: the fate of transferred genes over time, the mechanisms of HGT, and what dictates the impact of HGT on different lineages are all major outstanding questions. On the basis of the history of HGT research in bacteria, it seems likely that many questions that seem simple now will become more complex as data accumulates.

Abstract

Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.

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Figure 1: The major bifurcations and reticulations in eukaryotic evolution.
Figure 2: You are what you eat, what you live on, what lives on you, and what lives in you.
Figure 3: Different kinds of transfer and their effects on gene phylogeny.

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Acknowledgements

The authors wish to thank numerous colleagues for supplying unpublished data and several of the photos in Figure 2 (see the figure for photo credits). P.J.K.'s research on HGT is supported by grants from the Natural Sciences and Engineering Research Council of Canada and the Tula Foundation, and he is a Fellow of the Canadian Institute for Advanced Research. J.D.P.'s research on HGT is supported by a grant from the National Institutes of Health and by the METACyt Initiative of Indiana University, funded in part through a major grant from the Lilly Endowment, Inc.

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Correspondence to Patrick J. Keeling.

Supplementary information

Supplementary information S1 (table)

Number of genes putatively acquired from prokaryotesa in heavily sequenced protists (PDF 127 kb)

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Glossary

Polytomy

In a phylogeny, when a branching pattern cannot be resolved, the branches in question can be collapsed to show the absence of a hypothesis for the relationships among the lineages that they represent.

Endocytosis

A general eukaryotic cellular process using the cytoskeleton and endomembrane system to take up material from the environment.

Ectosymbiont

An organism living in a symbiotic association with another, specifically by attachment to the surface of its host.

Endosymbiont

An organism living in a symbiotic association with another, specifically by living inside a host cell.

Rumen

A fermentative compartment of the digestive system in many cellulose-digesting vertebrates, the contents of which are rich in anaerobic protists and prokaryotes.

Ciliate

A lineage of protists (for example, Tetrahymena and Paramecium), predominantly predators, defined by the presence of dimorphic nuclei and large numbers of short flagella (cilia) on the surface. They are members of the Chromalveolates.

Trypanosomid

A lineage of protist flagellates (for example, Trypanosoma, the sleeping-sickness agent), predominantly made up of parasites, and home to many unusual characteristics of genome structure (for example, RNA editing). They are members of the Excavates.

Diplomonad

A lineage of anaerobic or microaerophic protist flagellates (for example, Giardia lamblia), predominantly parasitic and often studied because of their reduced metabolism and mitochondria. They are members of the Excavates.

Parabasalian

A lineage of anaerobic or microaerophic protist flagellates (for example, Trichomonas), predominantly parasitic and often studied owing to their reduced metabolism and their hydrogenosome, a hydrogen-producing mitochondrial relict. They are members of the Excavates.

Dinoflagellate

A lineage of protist flagellates (for example, Alexandrium, a red tide alga) with photosynthetic, heterotrophic and parasitic representatives, which are known for many unusual modifications to genome structure — they are members of the Chromalveolates.

Oomycete

A lineage of protist parasites (for example, Phytophthora, the potato late-blight agent) that are responsible for numerous plant diseases, and were once mistakenly thought to be fungi but are really heterokonts. They are members of the Chromalveolates.

Osmotrophy

Feeding by absorption of nutrients directly from the environment (which can include a host organism in the case of parasites).

Heterokont

A lineage of protist (for example, oomycete parasites and kelps) with photosynthetic, heterotrophic and parasitic representatives, all of which are united by the possession of uniquely dimorphic flagella. They are members of the Chromalveolates.

Haptophyte

A lineage of photosynthetic protist (for example, Emiliania), predominantly marine, some of which form massive marine blooms, and many of which make distinctive calcium carbide scales that have contributed significantly to limestone deposits. They are members of the Chromalveolates.

Chlorarachniophyte

A lineage of photosynthetic protist (for example, Bigelowiella) with amoeboid and flagellate life stages, best known for their retention of a relict nucleus of their green algal plastid endosymbiont, known as a nucleomorph. They are members of the Rhizaria.

Monophyly

In phylogeny, a common ancestor and all its descendants are monophyletic (for example, animals), as opposed to a collection of organisms that does not include their common ancestor, which are polyphyletic (for example, flying animals). Monophyletic is sometimes subdivided into holophyletic (the most recent common ancestor and all things that evolved from it, for example, animals) and paraphyletic (the most recent common ancestor, but not all the things derived from it, for example, reptiles — from which birds evolved).

Chromalveolates

A hypothetical 'supergroup' of protists, including apicomplexa, dinoflagellates, ciliates, heterokonts, haptophytes and cryptomonads, all of which are hypothesized to have diverged from an ancient common ancestor that has acquired a plastid by secondary endosymbiosis with a red alga.

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Keeling, P., Palmer, J. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9, 605–618 (2008). https://doi.org/10.1038/nrg2386

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