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12 - Eukaryotic Gene Transfer: Adaptation and Replacements

from PART IV - Interkingdom Transfer and Endosymbiosis

Published online by Cambridge University Press:  16 September 2009

By
Jan O. Andersson
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

The current view of eukaryote phylogeny indicates that microbial eukaryotes (protists) represent the vast majority of the biological diversity within the eukaryotic domain of life, and that multicellular eukaryotes have evolved from protist lineages several times independently (Adl et al., 2005). Accordingly, most eukaryote genome evolution has occurred in microbial lineages, and multicellular eukaryotes with sequestered germlines, such as animals and plants, should be seen as recent evolutionary exceptions, rather than the norm, within the eukaryotic domain (Figure 12.1). Yet, most knowledge about eukaryotic genome evolution comes from multicellular organisms and a few representatives of unicellular lineages, such as yeast. Fortunately, this narrow view of eukaryote genome evolution is now expanding with the advance of genomic sequences from diverse protist lineages.

Several aspects of the lifestyles of protists are more similar to prokaryotic organisms, than to multicellular eukaryotes; differentiation into germ and soma cells are rare, and protists often live in close contacts with cells of distantly related species in the environment. Furthermore, many protists have asexual life cycles, although meiosis appears to be ancestral to eukaryotes (Ramesh et al., 2005). These similarities suggest that protists may share some aspects of genome evolution with prokaryotes. As is obvious from this book, the transfer of genetic material between unrelated lineages, lateral (or horizontal) gene transfer (LGT), is a fundamental mechanism in prokaryotic genome evolution, resulting in genomic plasticity which, for example, provides the basis for adaptation processes (Boucher et al., 2003; Gogarten and Townsend, 2005; Pál et al., 2005).

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Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 293 - 316
Publisher: Cambridge University Press
Print publication year: 2008

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References

Adam, R. D. (2001). Biology of Giardia lamblia. Clin Microbiol Rev, 14, 447–75.CrossRefGoogle ScholarPubMed
Adl, S. M., Simpson, A. G., Farmer, M. A., et al. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol, 52, 399–451.CrossRefGoogle ScholarPubMed
Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. Cell Mol Life Sci, 62, 1182–97.CrossRefGoogle ScholarPubMed
Andersson, J. O. (2006a). Convergent evolution: gene sharing by eukaryotic plant pathogens. Curr Biol, 16, R804–6.CrossRefGoogle ScholarPubMed
Andersson, J. O. (2006b). Genome evolution of anaerobic protists: metabolic adaptation via gene acquisition. In Katz, L. A., and Bhattacharya, D. (Eds.). Genomics and evolution of microbial eukaryotes. Oxford: Oxford University Press.Google Scholar
Andersson, J. O., and Roger, A. J. (2003). Evolution of glutamate dehydrogenase genes: evidence for lateral gene transfer within and between prokaryotes and eukaryotes. BMC Evol Biol, 3, 14.CrossRefGoogle ScholarPubMed
Andersson, J. O., Sjögren, Å. M., Davis, L. A. M., Embley, T. M., and Roger, A. J. (2003). Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol, 13, 94–104.CrossRefGoogle ScholarPubMed
Andersson, J. O., Sarchfield, S. W., and Roger, A. J. (2005). Gene transfers from Nanoarchaeota to an ancestor of diplomonads and parabasalids. Mol Biol Evol, 22, 85–90.CrossRefGoogle Scholar
Andersson, J. O., Hirt, R. P., Foster, P. G., and Roger, A. J. (2006). Evolution of four gene families with patchy phylogenetic distribution: influx of genes into protist genomes. BMC Evol Biol, 6, 27.CrossRefGoogle ScholarPubMed
Andersson, J. O., Sjögren, Å. M., Horner, D. S., et al. (2007). A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics, 8, 51.CrossRefGoogle ScholarPubMed
Archibald, J. M., and Keeling, P. J. (2002). Recycled plastids: a ‘green movement’ in eukaryotic evolution. Trends Genet, 18, 577–84.CrossRefGoogle ScholarPubMed
Archibald, J. M., Rogers, M. B., Toop, M., Ishida, K., and Keeling, P. J. (2003). Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA, 100, 7678–83.CrossRefGoogle ScholarPubMed
Baldauf, S. L. (2003). The deep roots of eukaryotes. Science, 300, 1703–6.CrossRefGoogle ScholarPubMed
Beiko, R. G., Harlow, T. J., and Ragan, M. A. (2005). Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA, 102, 14332–7.CrossRefGoogle ScholarPubMed
Belbahri, L., Calmin, G., Mauch, F., and Andersson, J. O. (2008). Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene, 31, 1–8.CrossRefGoogle Scholar
Bergthorsson, U., Adams, K. L., Thomason, B., and Palmer, J. D. (2003). Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature, 424, 197–201.CrossRefGoogle ScholarPubMed
Biagini, G. A., Yarlett, N., Ball, G. E., et al. (2003). Bacterial-like energy metabolism in the amitochondriate protozoon Hexamita inflata. Mol Biochem Parasitol, 128, 11–9.CrossRefGoogle ScholarPubMed
Boucher, Y., Douady, C. J., Papke, R. T., et al. (2003). Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet, 37, 283–328.CrossRefGoogle ScholarPubMed
Carlton, J. M., Hirt, R. P., Silva, J. C., et al. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science, 315, 207–12.CrossRefGoogle ScholarPubMed
Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol, 52, 297–354.CrossRefGoogle ScholarPubMed
Ciuffetti, L. M., Tuori, R. P., and Gaventa, J. M. (1997). A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell, 9, 135–44.CrossRefGoogle ScholarPubMed
Doolittle, W. F. (1998). You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet, 14, 307–11.CrossRefGoogle ScholarPubMed
Doolittle, W. F. (1999). Phylogenetic classification and the universal tree. Science, 284, 2124–9.CrossRefGoogle ScholarPubMed
Doolittle, W. F., Boucher, Y., Nesbø, C. L., et al. (2003). How big is the iceberg of which organellar genes in nuclear genomes are but the tip?Philos Trans R Soc Lond B Biol Sci, 358, 39–58.CrossRefGoogle Scholar
Edwards, J. E., McEwan, N. R., Travis, A. J., and Wallace, J. R. (2004). 16S rRNA library-based analysis of ruminal bacterial diversity. Antonie van Leeuwenhoek, 86, 263–81.CrossRefGoogle Scholar
El-Sayed, N. M., Myler, P. J., Blandin, G., et al. (2005). Comparative genomics of trypanosomatid parasitic protozoa. Science, 309, 404–9.CrossRefGoogle ScholarPubMed
Esser, C., Ahmadinejad, N., Wiegand, C., et al. (2004). A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Molecular Biology and Evolution, 21, 1643–60.CrossRefGoogle Scholar
Figge, R. M., and Cerff, R. (2001). GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity. Mol Biol Evol, 18, 2240–9.CrossRefGoogle ScholarPubMed
Filee, J., Siguier, P., and Chandler, M. (2007). I am what I eat and I eat what I am: acquisition of bacterial genes by giant viruses. Trends Genet, 23, 10–5.CrossRefGoogle ScholarPubMed
Friesen, T. L., Stukenbrock, E. H., Liu, Z., et al. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet, 38, 953–6.CrossRefGoogle ScholarPubMed
Garcia-Vallve, S., Romeu, A., and Palau, J. (2000). Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol, 17, 352–61.CrossRefGoogle ScholarPubMed
Genereux, D. P., and Logsdon, J. M. (2003). Much ado about bacteria-to-vertebrate lateral gene transfer. Trends Genet, 19, 191–5.CrossRefGoogle ScholarPubMed
Gile, G. H., Patron, N. J., and Keeling, P. J. (2006). EFL GTPase in cryptomonads and the distribution of EFL and EF-1α in chromalveolates. Protist, 157, 435–44.CrossRefGoogle ScholarPubMed
Gogarten, J. P. (2003). Gene transfer: gene swapping craze reaches eukaryotes. Curr Biol, 13, R53–4.CrossRefGoogle ScholarPubMed
Gogarten, J. P., and Townsend, J. P. (2005). Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol, 3, 679–87.CrossRefGoogle ScholarPubMed
Gojkovic, Z., Knecht, W., Zameitat, E., et al. (2004). Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol Genet Genomics, 271, 387–93.CrossRefGoogle ScholarPubMed
Hall, C., Brachat, S., and Dietrich, F. S. (2005). Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell, 4, 1102–15.CrossRefGoogle ScholarPubMed
Harper, J. T., and Keeling, P. J. (2004). Lateral gene transfer and the complex distribution of insertions in eukaryotic enolase. Gene, 340, 227–35.CrossRefGoogle ScholarPubMed
Huang, J., and Gogarten, J. P. (2006). Ancient horizontal gene transfer can benefit phylogenetic reconstruction. Trends Genet, 22, 361–6.CrossRefGoogle ScholarPubMed
Huang, J., Mullapudi, N., Lancto, C. A., et al. (2004). Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol, 5, R88.CrossRefGoogle ScholarPubMed
Huang, J., Xu, Y., and Gogarten, J. P. (2005). The presence of a haloarchaeal type tyrosyl-tRNA synthetase marks the opisthokonts as monophyletic. Mol Biol Evol, 22, 2142–6.CrossRefGoogle ScholarPubMed
Jenkins, C., Samudrala, R., Anderson, I., et al. (2002). Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proc Natl Acad Sci USA, 99, 17049–54.CrossRefGoogle ScholarPubMed
Jørgensen, A., and Sterud, E. (2007). Phylogeny of Spironucleus (Eopharyngia: Diplomonadida: Hexamitinae). Protist, 158, 157–54.CrossRefGoogle Scholar
Keeling, P. J., and Inagaki, Y. (2004). A class of eukaryotic GTPase with a punctate distribution suggesting multiple functional replacements of translation elongation factor 1α. Proc Natl Acad Sci USA, 101, 15380–5.CrossRefGoogle ScholarPubMed
Kenrick, P., and Crane, P. R. (1997). The origin and early evolution of plants on land. Nature, 389, 33–9.CrossRefGoogle Scholar
Kolattukudy, P. E., Rogers, L. M., Li, D., Hwang, C. S., and Flaishman, M. A. (1995). Surface signaling in pathogenesis. Proc Natl Acad Sci USA, 92, 4080–7.CrossRefGoogle ScholarPubMed
Koonin, E. V. (2003). Horizontal gene transfer: the path to maturity. Mol Microbiol, 50, 725–7.CrossRefGoogle Scholar
Kurland, C. G., Canback, B., and Berg, O. G. (2003). Horizontal gene transfer: a critical view. Proc Natl Acad Sci USA, 100, 9658–62.CrossRefGoogle ScholarPubMed
Latijnhouwers, M., Wit, P. J., and Govers, F. (2003). Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol, 11, 462–9.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (2005). Common themes in the genome strategies of pathogens. Curr Opin Genet Dev, 15, 584–8.CrossRefGoogle ScholarPubMed
Loftus, B., Anderson, I., Davies, R., et al. (2005). The genome of the protist parasite Entamoeba histolytica. Nature, 433, 865–8.CrossRefGoogle ScholarPubMed
Martin, W., Brinkmann, H., Savonna, C., and Cerff, R. (1993). Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA, 90, 8692–6.CrossRefGoogle ScholarPubMed
Martin, W., Rujan, T., Richly, E., et al. (2002). Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA, 99, 12246–51.CrossRefGoogle ScholarPubMed
Ochman, H., Lawrence, J. G., and Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.CrossRefGoogle ScholarPubMed
Pál, C., Papp, B., and Lercher, M. J. (2005). Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet, 37, 1372–5.CrossRefGoogle ScholarPubMed
Qian, Q., and Keeling, P. J. (2001). Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and prokaryote-to-eukaryote lateral gene transfer. Protist, 152, 193–201.CrossRefGoogle Scholar
Ramesh, M. A., Malik, S. B., and Logsdon, J. M. (2005). A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol, 15, 185–91.Google ScholarPubMed
Reyes-Prieto, A., Hackett, J. D., Soares, M. B., Bonaldo, M. F., and Bhattacharya, D. (2006). Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr Biol, 16, 2320–5.CrossRefGoogle ScholarPubMed
Ricard, G., Mcewan, N. R., Dutilh, B. E., et al. (2006). Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic carbohydrates rich environment. BMC Genomics, 7, 22.CrossRefGoogle ScholarPubMed
Rice, D. W., and Palmer, J. D. (2006). An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol, 4, 31.CrossRefGoogle ScholarPubMed
Richards, T. A., Hirt, R. P., Williams, B. A., and Embley, T. M. (2003). Horizontal gene transfer and the evolution of parasitic protozoa. Protist, 154, 17–32.CrossRefGoogle ScholarPubMed
Richards, T. A., Dacks, J. B., Campbell, S. A., et al. (2006a). Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell, 5, 1517–31.CrossRefGoogle ScholarPubMed
Richards, T. A., Dacks, J. B., Jenkinson, J. M., Thornton, C. R., and Talbot, N. J. (2006b). Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol [0960-9822], 16, 1857–64.CrossRefGoogle ScholarPubMed
Richardson, A. O., and Palmer, J. D. (2006). Horizontal gene transfer in plants. J Exp Bot, 58, 1–9.CrossRefGoogle ScholarPubMed
Rocap, G., Larimer, F. W., Lamerdin, J., et al. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424, 1042–7.CrossRefGoogle ScholarPubMed
Roxström-Lindquist, K., Palm, D., Reiner, D., Ringqvist, E., and Svärd, S. G. (2006). Giardia immunity - an update. Trends Parasitol, 22, 26–31.CrossRefGoogle ScholarPubMed
Sanders, I. R. (2006). Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol Evol, 21, 656–8.CrossRefGoogle ScholarPubMed
Sarti, P., Fiori, P. L., Forte, E., et al. (2004). Trichomonas vaginalis degrades nitric oxide and expresses a flavorubredoxin-like protein: a new pathogenic mechanism?Cell Mol Life Sci, 61, 618–23.CrossRefGoogle ScholarPubMed
Schlieper, D., Oliva, M. A., Andreu, J. M., and Lowe, J. (2005). Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. Proc Natl Acad Sci USA, 102, 9170–5.CrossRefGoogle ScholarPubMed
Shi, N. Q., and Jeffries, T. W. (1998). Anaerobic growth and improved fermentation of Pichia stipitis bearing a URA1 gene from Saccharomyces cerevisiae. Appl Microbiol Biotechnol, 50, 339–45.CrossRefGoogle ScholarPubMed
Simpson, A. G. B., and Roger, A. J. (2004). The real ‘kingdoms’ of eukaryotes. Curr Biol, 14, R693–6.CrossRefGoogle ScholarPubMed
Stechmann, A., Baumgartner, M., Silberman, J. D., and Roger, A. J. (2006). The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic. BMC Evol Biol, 6, 101.CrossRefGoogle ScholarPubMed
Steele, R. E., Hampson, S. E., Stover, N. A., Kibler, D. F., and Bode, H. R. (2004). Probable horizontal transfer of a gene between a protist and a cnidarian. Curr Biol, 14, R298–9.CrossRefGoogle Scholar
Sztukowska, M., Bugno, , Potempa, M., Travis, J., Kurtz, J., , D. M. (2002). Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol, 44, 479–88.CrossRefGoogle ScholarPubMed
Takishita, K., Ishida, K., and Maruyama, T. (2003). An enigmatic GAPDH gene in the symbiotic dinoflagellate genus Symbiodinium and its related species (the order Suessiales): possible lateral gene transfer between two eukaryotic algae, dinoflagellate and euglenophyte. Protist, 154, 443–54.CrossRefGoogle ScholarPubMed
Temporini, E. D., and VanEtten, H. D. (2004). An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Neocosmospora boniensis. Curr Genet, 46, 29–36.CrossRefGoogle ScholarPubMed
Waller, R. F., Slamovits, C. H., and Keeling, P. J. (2006). Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol Biol Evol, 23, 1437–43.CrossRefGoogle Scholar
Watkins, R. F., and Gray, M. W. (2006). The frequency of eubacterium-to-eukaryote lateral gene transfers shows significant cross-taxa variation within amoebozoa. J Mol Evol, 63, 801–14.CrossRefGoogle ScholarPubMed
Wenzl, P., Wong, L., Kwang-Won, K., and Jefferson, R. A. (2005). A functional screen identifies lateral transfer of β-glucuronidase (gus) from bacteria to fungi. Mol Biol Evol, 22, 308–16.CrossRefGoogle ScholarPubMed
Wolf, Y. I., Aravind, L., Grishin, N. V., and Koonin, E. V. (1999). Evolution of aminoacyl-tRNA synthetases-analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res, 9, 689–710.Google ScholarPubMed

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