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 has 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.

[edit] 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]

[edit] Mechanism

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 so in eukaryotes. Transformation is often used in laboratories 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, or phage).
• Bacterial conjugation, a process in which a bacterial cell transfers genetic material to another cell by cell-to-cell contact.

[edit] Viruses

The virus called Mimivirus infects amoebae. Another virus, called Sputnik, also infects amoebae 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]

[edit] Prokaryotes

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

[edit] Eukaryotes

Analysis of DNA sequences suggests that horizontal gene transfer has also occurred within eukaryotes from the chloroplast and mitochondrial genomes to the 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]

Researchers at the University of Arizona have found that the genome of pea aphids contains genes that were horizontally transferred from fungi.^[23] The transferred genes enable carotenoid production in the aphids, which is not known to occur in any other animals.

Striga hermonthica, a eudicot, has undergone a horizontal gene transfer from Sorghum (Sorghum bicolor) to its nuclear genome^[24]. The gene is of unknown functionality.

[edit] Importance in evolution

In May 2010 a research paper^[25] demonstrated that there was indeed one Last Universal Common Ancestor to all existing life and not a cluster of organisms. "There is strong quantitative support, by a formal test"^[25] for the theory that all living organisms on Earth are descended from a common ancestor.^[26] A statistical comparison of various alternative hypotheses has shown that universal common ancestry is significantly more probable than models involving multiple origins.^[25] "A universal common ancestor is at least 10²⁸⁶⁰ times more probable than having multiple ancestors'"^[27] "A model with a single common ancestor but allowing for some gene swapping among species was'10³⁴⁸⁹ times more probable than the best multi-ancestor model'"^[27]

Horizontal gene transfer is a potential confounding factor in inferring phylogenetic trees based on the sequence of one gene.^[28] 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 the 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]

[edit] Scientific American Article (2000)

Uprooting the Tree of Life by W. Ford Doolittle (Scientific American, February 2000, pp 90'95)^[29] 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.^[29]

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."^[29]

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.^[29]

"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."^[29]

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."^[30]

However, in May 2010 a research paper^[25] demonstrated that there was indeed one Last Universal Common Ancestor to all existing life and not a cluster of organisms. This paper shows that as descendant species of the LUCA innovated new genes, some of these genes were horizontally transferred.

[edit] Genes

This list is incomplete; you can help by expanding it.

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

• Lycopene cyclase for carotenoid biosynthesis, between Chlorobi and Cyanobacteria.^[31]

[edit] See also

• Agrobacterium, a bacterium well known for its ability to transfer DNA between itself and plants.
• Endogenous retrovirus
• Integron
• Provirus
• Retrotransposon
• Genetically modified organism
• Mobile genetic elements
• Tree of life (science)
• Phylogenetic tree

[edit] Sources and notes

[edit] Further reading

• Citizendium:Horizontal gene transfer
• Citizendium:Horizontal gene transfer in prokaryotes
• Citizendium:Horizontal gene transfer in plants
• Citizendium:Horizontal gene transfer (History)
• - Papers by Dr Michael Syvanen on Horizontal Gene Transfer
• Salzberg SL, White O, Peterson J, Eisen JA (June 2001). "Microbial genes in the human genome: lateral transfer or gene loss?". Science 292 (5523): 1903'6. doi:10.1126/science.1061036. PMID 11358996. http://www.cbcb.umd.edu/~salzberg/docs/ScienceLateralTransfer.pdf.  This article points out that one dramatic claim of horizontal gene transfer - in which a distinguished group of scientists claimed that bacteria transferred their DNA directly into the human lineage - was simply wrong.
• Woese CR (June 2002). "On the evolution of cells". Proc. Natl. Acad. Sci. U.S.A. 99 (13): 8742'7. doi:10.1073/pnas.132266999. PMID 12077305.  This article seeks to shift the emphasis in early phylogenic adaptation from vertical to horizontal gene transfer. He uses the term "Darwinian Threshold" for the time of major transition of evolutionary mechanisms from mostly horizontal to mostly vertical transfer, and the "origin of speciation".
• Snel B, Bork P, Huynen MA (January 1999). "Genome phylogeny based on gene content". Nat. Genet. 21 (1): 108'10. doi:10.1038/5052. PMID 9916801.  This article proposes using the presence or absence of a set of genes to infer phylogenies, in order to avoid confounding factors such as horizontal gene transfer.
• Webfocus in Nature with free review articles [3]
• Patil PB, Sonti RV (October 2004). "Variation suggestive of horizontal gene transfer at a lipopolysaccharide (lps) biosynthetic locus in Xanthomonas oryzae pv. oryzae, the bacterial leaf blight pathogen of rice". BMC Microbiol. 4: 40. doi:10.1186/1471-2180-4-40. PMID 15473911. 
• Jin G, Nakhleh L, Snir S, Tuller T (November 2006). "Maximum likelihood of phylogenetic networks". Bioinformatics 22 (21): 2604'11. doi:10.1093/bioinformatics/btl452. PMID 16928736.  for a technique to decrease the impact of HGT events on maximum likelihood cladistical analyses.
• Horizontal Gene Transfer - A New Paradigm for Biology
• Horizontal Gene Transfer (page 334 of Molecular Genetics by Ulrich Melcher)
• Report on horizontal gene transfer by Mae-Wan Ho, March 22, 1999
• Recent Evidence Confirms Risks of Horizontal Gene Transfer
• Horizontal Gene Transfer at sciences.sdsu.edu
• 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. 
• PDF article on Horizontal Gene Transfer
• The New Yorker, July 12, 1999, pp. 44-61 "Smallpox knows how to make a mouse protein. How did smallpox learn that? 'The poxviruses are promiscuous at capturing genes from their hosts,' Esposito said. 'It tells you that smallpox was once inside a mouse or some other small rodent.'"
• Szpirer C, Top E, Couturier M, Mergeay M (1 December 1999). "Retrotransfer or gene capture: a feature of conjugative plasmids, with ecological and evolutionary significance". Microbiology (Reading, Engl.) 145 (Pt 12): 3321'9. PMID 10627031. http://mic.sgmjournals.org/cgi/content/full/145/12/3321. 
• Results of research into horizontal gene transfer Can transgenes from genetically modified plants be absorbed by micro-organisms and spread in this way?
• Gene Therapy Net
• A study of Horizontal Gene Transfer in eukaryotes