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Current tree of life showing horizontal gene transfers.

Horizontal gene transfer (HGT), also Lateral gene transfer (LGT), is any process in which an organism incorporates genetic material from another organism without being the offspring of that organism. By contrast, vertical transfer occurs when an organism receives genetic material from its ancestor, e.g. its parent or a species from which it evolved.

Most thinking in genetics has focused upon vertical transfer, but there is a growing awareness that horizontal gene transfer is a highly significant phenomenon, and amongst single-celled organisms perhaps the dominant form of genetic transfer. Artificial horizontal gene transfer is a form of genetic engineering.

Contents

History

Horizontal gene transfer was first described in Japan in a 1959 publication that demonstrated the transfer of antibiotic resistance between different species of bacteria.[1][2] In the mid-1980s, Syvanen [3] predicted that lateral gene transfer existed, had biological significance, and was involved in shaping evolutionary history from the beginning of life on Earth.

As Jain, Rivera and Lake (1999) put it: "Increasingly, studies of genes and genomes are indicating that considerable horizontal transfer has occurred between prokaryotes."[4] (see also Lake and Rivera, 2007).[5] The phenomenon appears to have had some significance for unicellular eukaryotes as well. As Bapteste et al. (2005) observe, "additional evidence suggests that gene transfer might also be an important evolutionary mechanism in protist evolution."[6]

There is some evidence that even higher plants and animals have been affected and this has raised concerns for safety.[7] However, Richardson and Palmer (2007) state: "Horizontal gene transfer (HGT) has played a major role in bacterial evolution and is fairly common in certain unicellular eukaryotes. However, the prevalence and importance of HGT in the evolution of multicellular eukaryotes remain unclear."[8]

Due to the increasing amount of evidence suggesting the importance of these phenomena for evolution (see below), molecular biologists such as Peter Gogarten have described horizontal gene transfer as "A New Paradigm for Biology".[9]

It should also be noted that the process may be a hidden hazard of genetic engineering, as it may allow dangerous transgenic DNA to spread from species to species.[7]

Viruses

The virus called Mimivirus infects amoebae. Another virus, called Sputnik, also infects them but it cannot reproduce unless mimivirus has already infected the same cell.[10] "Sputnik’s genome reveals further insight into its biology. Although 13 of its genes show little similarity to any other known genes, three are closely related to mimivirus and mamavirus genes, perhaps cannibalized by the tiny virus as it packaged up particles sometime in its history. This suggests that the satellite virus could perform horizontal gene transfer between viruses – paralleling the way that bacteriophages ferry genes between bacteria."[11]

Prokaryotes

Horizontal gene transfer is common among bacteria, even very distantly-related ones. This process is thought to be a significant cause of increased drug resistance;[12] when one bacterial cell acquires resistance, it can quickly transfer the resistance genes to many species.[13]

There are three common mechanisms for horizontal gene transfer:[citation needed]

  • Transformation, the genetic alteration of a cell resulting from the introduction, uptake and expression of foreign genetic material (DNA or RNA). This process is relatively common in bacteria, but less common in eukaryotes. Transformation is often used to insert novel genes into bacteria for experiments, or for industrial or medical applications. See also molecular biology and biotechnology.
  • Transduction, the process in which bacterial DNA is moved from one bacterium to another by a bacterial virus (a bacteriophage, commonly called a phage).
  • Bacterial conjugation, a process in which a living bacterial cell transfers genetic material through cell-to-cell contact.

Eukaryotes

Analysis of DNA sequences suggests that horizontal gene transfer has also occurred within eukaryotes, from their chloroplast and mitochondrial genome to their nuclear genome. As stated in the endosymbiotic theory, chloroplasts and mitochondria probably originated as bacterial endosymbionts of a progenitor to the eukaryotic cell.[14]

Horizontal transfer of genes from bacteria to some fungi, especially the yeast Saccharomyces cerevisiae, has been well documented.[15]

There is also recent evidence that the azuki bean beetle has somehow acquired genetic material from its (non-beneficial) endosymbiont Wolbachia.[16] New examples have recently been reported, demonstrating that Wolbachia bacteria represent an important potential source of genetic material in arthropods and filarial nematodes.[17]

There is also evidence for horizontal transfer of mitochondrial genes to parasites of the Rafflesiaceae plant family from their hosts (also plants),[18][19] from chloroplasts of a not-yet-identified plant to the mitochondria of the bean Phaseolus,[20] and from a heterokont alga to its predator, the sea slug Elysia chlorotica.[21]

"Sequence comparisons suggest recent horizontal transfer of many genes among diverse species including across the boundaries of phylogenetic "domains". Thus determining the phylogenetic history of a species can not be done conclusively by determining evolutionary trees for single genes."[22]

Importance in evolution

Horizontal gene transfer is a potential confounding factor in inferring phylogenetic trees based on the sequence of one gene.[23] For example, given two distantly related bacteria that have exchanged a gene, a phylogenetic tree including those species will show them to be closely related because that gene is the same, even though most other genes are dissimilar. For this reason, it is often ideal to use other information to infer robust phylogenies, such as the presence or absence of genes, or, more commonly, to include as wide a range of genes for phylogenetic analysis as possible.

For example, the most common gene to be used for constructing phylogenetic relationships in prokaryotes is the 16s rRNA gene, since its sequences tend to be conserved among members with close phylogenetic distances, but variable enough that differences can be measured. However, in recent years it has also been argued that 16s rRNA genes can also be horizontally transferred. Although this may be infrequent, validity of 16s rRNA-constructed phylogenetic trees must be reevaluated.

Biologist Johann Peter Gogarten suggests "the original metaphor of a tree no longer fits the data from recent genome research" therefore "biologists should use the metaphor of a mosaic to describe the different histories combined in individual genomes and use the metaphor of a net to visualize the rich exchange and cooperative effects of HGT among microbes."[9]

Using single genes as phylogenetic markers, it is difficult to trace organismal phylogeny in the presence of horizontal gene transfer. Combining the simple coalescence model of cladogenesis with rare HGT horizontal gene transfer events suggest there was no single most recent common ancestor that contained all of the genes ancestral to those shared among the three domains of life. Each contemporary molecule has its own history and traces back to an individual molecule cenancestor. However, these molecular ancestors were likely to be present in different organisms at different times."[9]

Uprooting the Tree of Life by W. Ford Doolittle (Scientific American, February 2000, pp 90–95)[24] contains a discussion of the Last Universal Common Ancestor, and the problems that arose with respect to that concept when one considers horizontal gene transfer. The article covers a wide area - the endosymbiont hypothesis for eukaryotes, the use of small subunit ribosomal RNA (SSU rRNA) as a measure of evolutionary distances (this was the field Carl Woese worked in when formulating the first modern "tree of life", and his research results with SSU rRNA led him to propose the Archaea as a third domain of life) and other relevant topics. Indeed, it was while examining the new three-domain view of life that horizontal gene transfer arose as a complicating issue: Archaeoglobus fulgidus is cited in the article (p. 76) as being an anomaly with respect to a phylogenetic tree based upon the encoding for the enzyme HMGCoA reductase - the organism in question is a definite Archaean, with all the cell lipids and transcription machinery that are expected of an Archaean, but whose HMGCoA genes are actually of bacterial origin.[24]

Again on p. 76, the article continues with:

"The weight of evidence still supports the likelihood that mitochondria in eukaryotes derived from alpha-proteobacterial cells and that chloroplasts came from ingested cyanobacteria, but it is no longer safe to assume that those were the only lateral gene transfers that occurred after the first eukaryotes arose. Only in later, multicellular eukaryotes do we know of definite restrictions on horizontal gene exchange, such as the advent of separated (and protected) germ cells."[24]

The article continues with:

"If there had never been any lateral gene transfer, all these individual gene trees would have the same topology (the same branching order), and the ancestral genes at the root of each tree would have all been present in the last universal common ancestor, a single ancient cell. But extensive transfer means that neither is the case: gene trees will differ (although many will have regions of similar topology) and there would never have been a single cell that could be called the last universal common ancestor.[24]
"As Woese has written, 'the ancestor cannot have been a particular organism, a single organismal lineage. It was communal, a loosely knit, diverse conglomeration of primitive cells that evolved as a unit, and it eventually developed to a stage where it broke into several distinct communities, which in their turn became the three primary lines of descent (bacteria, archaea and eukaryotes)' In other words, early cells, each having relatively few genes, differed in many ways. By swapping genes freely, they shared various of their talents with their contemporaries. Eventually this collection of eclectic and changeable cells coalesced into the three basic domains known today. These domains become recognisable because much (though by no means all) of the gene transfer that occurs these days goes on within domains."[24]

With regard to how horizontal gene transfer affects evolutionary theory (common descent, universal phylogenetic tree) Carl Woese says:

"What elevated common descent to doctrinal status almost certainly was the much later discovery of the universality of biochemistry, which was seemingly impossible to explain otherwise. But that was before horizontal gene transfer (HGT), which could offer an alternative explanation for the universality of biochemistry, was recognized as a major part of the evolutionary dynamic. In questioning the doctrine of common descent, one necessarily questions the universal phylogenetic tree. That compelling tree image resides deep in our representation of biology. But the tree is no more than a graphical device; it is not some a priori form that nature imposes upon the evolutionary process. It is not a matter of whether your data are consistent with a tree, but whether tree topology is a useful way to represent your data. Ordinarily it is, of course, but the universal tree is no ordinary tree, and its root no ordinary root. Under conditions of extreme HGT, there is no (organismal) "tree." Evolution is basically reticulate."[25]
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Genes

There is evidence for historical horizontal transfer of the following genes:

Gene persistence and transfer

  • Persistence of plasmid DNA.[27]

See also

Sources and notes

  1. ^ Ochiai K, Yamanaka T, Kimura K, Sawada, O (1959). "Inheritance of drug resistance (and its transfer) between Shigella strains and Between Shigella and E. coli strains" (in Japanese). Hihon Iji Shimpor 1861: 34. 
  2. ^ Akiba T, Koyama K, Ishiki Y, Kimura S, Fukushima T (April 1960). "On the mechanism of the development of multiple-drug-resistant clones of Shigella". Jpn. J. Microbiol. 4: 219–27. PMID 13681921. 
  3. ^ Syvanen M (January 1985). "Cross-species gene transfer; implications for a new theory of evolution" (PDF). J. Theor. Biol. 112 (2): 333–43. doi:10.1016/S0022-5193(85)80291-5. PMID 2984477. http://www.dcn.davis.ca.us/vme/hgt/JTheoBiolvol112pp333-343yr1985.PDF. 
  4. ^ Jain R, Rivera MC, Lake JA (March 1999). "Horizontal gene transfer among genomes: the complexity hypothesis". Proc. Natl. Acad. Sci. U.S.A. 96 (7): 3801–6. doi:10.1073/pnas.96.7.3801. PMID 10097118. PMC 22375. http://www.pnas.org/cgi/pmidlookup?view=long&pmid=10097118. 
  5. ^ Rivera MC, Lake JA (September 2004). "The ring of life provides evidence for a genome fusion origin of eukaryotes". Nature 431 (7005): 152–5. doi:10.1038/nature02848. PMID 15356622. http://www.sdsc.edu/~shindyal/ejc121304.pdf. 
  6. ^ Bapteste E, Susko E, Leigh J, MacLeod D, Charlebois RL, Doolittle WF (2005). "Do orthologous gene phylogenies really support tree-thinking?". BMC Evol. Biol. 5 (1): 33. doi:10.1186/1471-2148-5-33. PMID 15913459. 
  7. ^ a b Mae-Wan Ho (1999). Cauliflower Mosaic Viral Promoter - A Recipe for Disaster? Microbial Ecology in Health and Disease, 11:194–197. Reprint. Accessed 2008-06-09.
  8. ^ Richardson, Aaron O. and Jeffrey D. Palmer (January 2007). "Horizontal Gene Transfer in Plants". Journal of Experimental Botany 58 (1): 1–9 [1]. doi:10.1093/jxb/erl148. PMID 17030541. 
  9. ^ a b c Gogarten, Peter (2000). "Horizontal Gene Transfer: A New Paradigm for Biology". Esalen Center for Theory and Research Conference. http://www.esalenctr.org/display/confpage.cfm?confid=10&pageid=105&pgtype=1. Retrieved 2007-03-18. 
  10. ^ La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D (September 2008). "The virophage as a unique parasite of the giant mimivirus". Nature 455 (7209): 100–4. doi:10.1038/nature07218. PMID 18690211. 
  11. ^ Pearson H (August 2008). "'Virophage' suggests viruses are alive" ( – Scholar search). Nature 454 (7205): 677. doi:10.1038/454677a. PMID 18685665. http://www.nature.com/news/2008/080806/full/454677a.html. 
  12. ^ Barlow M (2009). "What antimicrobial resistance has taught us about horizontal gene transfer". Methods in Molecular Biology (Clifton, N.J.) 532: 397–411. doi:10.1007/978-1-60327-853-9_23. PMID 19271198. 
  13. ^ Hawkey PM, Jones AM (September 2009). "The changing epidemiology of resistance". The Journal of Antimicrobial Chemotherapy 64 Suppl 1: i3–10. doi:10.1093/jac/dkp256. PMID 19675017. 
  14. ^ Blanchard JL, Lynch M (July 2000). "Organellar genes: why do they end up in the nucleus?". Trends Genet. 16 (7): 315–20. doi:10.1016/S0168-9525(00)02053-9. PMID 10858662. http://linkinghub.elsevier.com/retrieve/pii/S0168-9525(00)02053-9.  (Discusses theories on how mitochondria and chloroplast genes are transferred into the nucleus, and also what steps a gene needs to go through in order to complete this process.)
  15. ^ Hall C, Brachat S, Dietrich FS (June 2005). "Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae". Eukaryotic Cell 4 (6): 1102–15. doi:10.1128/EC.4.6.1102-1115.2005. PMID 15947202. PMC 1151995. http://ec.asm.org/cgi/content/full/4/6/1102.  The article argues that horizontal transfer of bacterial DNA to Saccharomyces cerevisiae has occurred.
  16. ^ Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T (October 2002). "Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect". Proc. Natl. Acad. Sci. U.S.A. 99 (22): 14280–5. doi:10.1073/pnas.222228199. PMID 12386340.  This article argues that Wolbachia DNA is in the azuki bean beetle genome (a species of bean weevil.
  17. ^ Dunning Hotopp JC, Clark ME, Oliveira DC, et al. (September 2007). "Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes". Science 317 (5845): 1753–6. doi:10.1126/science.1142490. PMID 17761848. 
  18. ^ Charles C. Davis and Kenneth J. Wurdack (30 July 2004). "Host-to-Parasite Gene Transfer in Flowering Plants: Phylogenetic Evidence from Malpighiales". Science 305 (5684): 676–8. doi:10.1126/science.1100671. PMID 15256617. http://www.sciencemag.org/cgi/content/abstract/305/5684/676. 
  19. ^ Daniel L Nickrent, Albert Blarer, Yin-Long Qiu, Romina Vidal-Russell and Frank E Anderson (2004). "Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer". BMC Evolutionary Biology 4 (40): 40. doi:10.1186/1471-2148-4-40. http://www.biomedcentral.com/1471-2148/4/40. 
  20. ^ Magdalena Woloszynska, Tomasz Bocer, Pawel Mackiewicz and Hanna Janska (November 2004). "A fragment of chloroplast DNA was transferred horizontally, probably from non-eudicots, to mitochondrial genome of Phaseolus". Plant Molecular Biology 56 (5): 811–20. doi:10.1007/s11103-004-5183-y. PMID 15803417. 
  21. ^ Rumpho ME, Worful JM, Lee J, et al. (November 2008). "From the Cover: Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica". Proc. Natl. Acad. Sci. U.S.A. 105 (46): 17867–71. doi:10.1073/pnas.0804968105. PMID 19004808. PMC 2584685. http://www.pnas.org/cgi/pmidlookup?view=long&pmid=19004808. 
  22. ^ okstate.edu
  23. ^ Graham Lawton Why Darwin was wrong about the tree of life New Scientist Magazine issue 2692 21 January 2009 [2] Accessed February 2009
  24. ^ a b c d e Doolittle, Ford W. (February 2000). "Uprooting the Tree of Life". Scientific American: 72–7. 
  25. ^ Woese CR (June 2004). "A new biology for a new century". Microbiol. Mol. Biol. Rev. 68 (2): 173–86. doi:10.1128/MMBR.68.2.173-186.2004. PMID 15187180. PMC 419918. http://mmbr.asm.org/cgi/content/full/68/2/173. 
  26. ^ D.A. Bryant & N.-U. Frigaard (November 2006). "Prokaryotic photosynthesis and phototrophy illuminated". Trends Microbiol. 14 (11): 488. doi:10.1016/j.tim.2006.09.001. PMID 16997562. 
  27. ^ Meenakshisundaram Kandhavelu and S. John Vennison (July 2008). "Persistence of plasmid DNA in different soils". African Journal of Biotechnology. 7 (15): 2543–6. 

Further reading


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