Natural GMOS Part 39. You are what you eat, what you live on, what lives on you, and what lives in you.

Horizontal gene transfer in eukaryotic evolution.
Keeling PJ, Palmer JD.
Nat Rev Genet. 2008 Aug;9(8):605-18.

Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z, Canada. pkeeling@interchange.ubc.ca

Summary
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.

Despite such analytical limitations, most of the protist genomes that have been examined contain a significant number of genes of probable bacterial origin (Supplementary information S1 (table)). On a percentage basis, HGT (from bacteria at least) contributes less to protistan genomes than it does to bacterial genomes, although rumen-dwelling ciliates, which are estimated to have acquired 4% of their genes from bacteria49, approach levels of HGT that are commonly found in bacteria.
The number of bacterial genes in any particular nuclear genome is likely to be a complex function of multiple factors affecting the likelihood of both the acquisition of bacterial genes and their fixation and persistence. One commonly noted factor affecting incorporation of bacterial genes is opportunity, or exposure to bacterial DNA. Many protists are phagotrophs, they subsist by eating bacteria and sometimes other eukaryotes (FIG. 2). This has led to the ‘you are what you eat’ theory of HGT50. Other protists, although not phagotrophs now, might have been so for long periods in their past and/or might live in environments where they are frequently exposed to bacterial DNA (for example, parasites, rumen dwellers and so on). But not all protists are exposed in this way, and this probably correlates with a lack of bacterial genes. For example, the non-phagotrophic green alga Chlamydomonas reinhardtii so far seems to lack bacterial genes 51,52, although its recently sequenced genome has not yet been examined in this regard.

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Another factor that is commonly mentioned 53,54 is that eukaryotes with a highly segregated germ line (that is, animals) will tend to be most sheltered from heritably meaningful exposure to foreign DNA (and might, for example, have a role in the contrast between animal and plant mitochondria mentioned below). This is probably a relatively strong deterrent to HGT in animals, although certainly not an absolute one. Several strong cases for HGT into animal genomes are now known55,56, and we suspect that when more animal genomes are searched systematically for HGT other cases will emerge.

Key citations
55. Kondrashov, F. A., Koonin, E. V., Morgunov, I. G., Finogenova, T. V. & Kondrashova, M. N. Evolution of glyoxylate cycle enzymes in metazoa: evidence of
multiple horizontal transfer events and pseudogene formation. Biol. Direct 1, 31 (2006).
56. Nakashima, K., Yamada, L., Satou, Y., Azuma, J. & Satoh, N. The evolutionary origin of animal cellulose synthase. Dev. Genes Evol. 214, 81–88 (2004).


Eukaryote–prokaryote transfers

Providing new functions to bacteria. Few cases of eukaryotic-to-prokaryotic HGT have been reported, the most interesting being several apparently recent transfers of genes that are otherwise found only in eukaryotes. In two cases the proteins have central roles in the cytoskeleton, and therefore they must impart some novel function to their new hosts. Alpha- and betatubulins are encoded in the bacterium Prosthecobacter by an operon that includes another eukaryotic gene — for kinesin light chain 91. Both tubulins seem to have structural differences compared with canonical tubulins 92, but they do form profilaments with similar properties and seem to polymerize by some cooperative assembly mechanism 92,93. Similarly, genes for actin and the functionally associated profilin have been found adjacent to each other in the genome of a single strain of the cyanobacterium Microcystis aeruginosa 94. As with the Prosthecobacter tubulins, the actin has been localized and found to form a shell within the cell wall, suggesting again that the protein has taken on some structural role in the bacterium 94. Another interesting case is fructose bisphosphate aldolase (FBA), an enzyme that exists as two non-homologous analogues, one common to bacteria and one common to eukaryotes. Several isolates of the closely related cyanobacteria Prochlorococcus and Synechococcus have been found to possess a eukaryotic FBA, which is located adjacent to the bacterial analogue that is ancestral to cyanobacteria 95.

Legend to Figure 2 You are what you eat, what you live on, what lives on you, and what lives in you.

Several behaviours and life-styles can enhance horizontal gene transfer (HGT), some of which are shown here. The predatory ciliate Didinium engulfs and digests another ciliate, Paramecium, as shown by SEM (a) (photo courtesy of W. Foissner, University of Salzburg). Phagotrophy, especially in microbial eukaryotes in which the germ and soma cells are the same, could greatly enhance the access of an organism to foreign DNA. The stem of the parasitic plant Cuscuta (dodder) entwines the stem of its host plant, Glechoma (b) (photo courtesy of K. Robertson, Illinois Natural History Survey). The parasite Cuscuta forms intimate connections with the vascular system of its host, Glechoma, which are called haustoria (c) (photo courtesy of H. Albrecht and J. Yoder, University of California, Davis). Several cases of mitochondrial HGT between parasitic plants and their hosts have been described (BOX 3). Plastid movement by successive rounds of endosymbiosis has affected several groups of eukaryotes. Kryptoperidinium is a consortium between a dinoflagellate and a diatom (d). Nuclei of both partners (blue) are adjacent to one another (the dinoflagellate nucleus is round with bright spots, the diatom nucleus is multi-lobed and less bright) and the diatom plastids are red (photo by P.K.). The sea slug Elysia clarki is bright green (e) because it retains photosynthetically active plastids from its food algae for months after the food has otherwise been digested (photo courtesy of S. Pierce, Gulfbase at Texas A&M University–Corpus Christi). Permanent and long-term endosymbiotic associations lead to large-scale sequence migrations, but the depth of this impact has not been wholly investigated in most systems, including in Kryptoperidium and Elysia clarki. Some interspecies associations that are highly specific and long term are probably less integrated at the genetic level but nonetheless provide opportunities for transfer. The surface of a devescovinid flagellate is completely covered with a uniform layer of bacteria (f), whereas the flagellate Barbulonympha also takes up bacteria into its cytoplasm (g) (both photos by K. Carpenter, University of British Columbia and P.K.).