Horizontal gene transfer/Citable Version

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The Rhyme of the Ancient Mariner, Samuel Taylor Coleridge
He prayeth well, who loveth well
Both man and bird and beast.
He prayeth best, who loveth best
All things both great and small

Introductory discussions of genetics of multicellular organisms tend to emphasise vertical gene transfer, that is simple heritability of parental traits by progeny when an organism receives genetic material from its ancestor, e.g. its parents or other ancestral members of the same species. The possibility of horizontal gene transfer (HGT), also called lateral gene transfer (LGT), which is any process in which an organism transfers genetic material (i.e. DNA) to another cell that is not its offspring, is often not mentioned.

The historical concept of a genome as a stable structure that is faithfully inherited from generation to generation has also tended to cause the biological importance of horizontal gene transfer to be overlooked. Although Barbara McClintock realised in the 1940s the the genome (in maize) was in fact a dynamic structure, her work was not fully appreciated until mobile DNA and horizontal gene transfer in bacteria was thoroughly studied in the 1960s and 70s [1]

Main features of horizontal gene transfer in nature

  • A hallmark of horizontal gene transfer is the presence of the same gene in distantly related organisms. The frequent discovery of shared DNA sequences such as the mariner class of transposons, insertion sequence (IS) DNA, and retrovirus genes in diverse species, and shared mitochondial genes in diverse flowering plants indicates that mobile DNA has natural pathways for movement between different species.
  • Horizontal movement of genes is common among bacteria and is responsible for infectious multiple-antibiotic resistance in pathogenic bacteria, a major factor limiting the effectiveness of antibiotics.
  • Horizontal gene transfer is also common in diverse groups of unicellular protists, which often contain several genes transfered from both prokaryotes and other protists [2] [3] [4].
  • Horizontal gene transfer globally occurs on a massive scale among marine microorganisms, and viruses, the most numerous biological entities in the sea, are implicated as a major pathway for inter-species gene movement in the ocean. Endosymbiosis with an alga is identified as a route for horizontal gene transfer in marine dinoflagellates, the organisms that cause "red tides" [5].
  • Mechanisms for horizontal gene transfer in flowering plants involving parasitic plants such as dodder or endophytes such as mosses (which facilitate inter-species gene transfer by being in intimite cell-to-cell contact with their host plants) are now well established (see Horizontal gene transfer in plants).
  • Not all the vehicles by which horizontal gene transfer are fully characterised. As horizontal gene transfer occurs at lower frequencies than routine exchange of a full set of genes as with with sexual reproduction within the species, it is difficlt to detect directly, but modern techniques of DNA analysis provide much evidence for it from comparative study of genomes. In insects, mites and insect viruses are established as probable vectors for transmission for horizontal gene transfer. Other mechanisms include plasmid mediated promiscuous mating by bacteria, for instance byAgrobacterium tumefaciens, and carriage of genes by [[viruses]. Bacterial "rol" genes from Agrobacterium species are present in plants of the tobacco (Nicotiniana) genus. [6]


Prokaryotes

See main article Horizontal gene transfer in prokaryotes

This article discusses:

Eukaryotes

Junk DNA is the most obvious evidence of horizontal gene transfer in eukaryotes. Such seemingly non-functional repetitive DNA which contitutes a major portion of many genomes of plants and animals. This DNA usually includes multiple copies of various "Jumping genes" which can proliferate within a genome after they have been transferred from another species. Examples in the human of such horizontally transferred mobile are Hsmar1 and Hsmar2 which are related to the widely studied mariner transposon. Close relatives mariner mobile DNA have been discovered in organisms as diverse as mites, flatworms, hydras, insects, nematodes, mammals and humans[7] [8].

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.

Protists

Analysis of the complete genome sequence of the protist Entamoeba histolytica indicates 96 cases of relatively recent horizontal gene transfer from prokaryotes [9], where as similar analysis of the complete genome sequence of the protist Cryptosporidium parvum reveal 24 candidates of horizontal gene transfer from bacteria [10]. These results fit the idea that "you are what you eat". That is, with unicellular grazing organisms, foreign genetic material is constantly entering the cell and occasionaly the genome from food organisms [11].

Plants

See Horizontal gene transfer in plants for
  • Natural gene transfer between plants that do not cross-pollinate
  • Jumping genes cross naturally between rice and millet
  • Epiphytes and parasites as a bridge for gene flow between diverse plant species
See Transgenic plant for hybridization by cross-pollination and artificial horizontal gene transfer in biotechnology.

Plant genes have also been discovered to be able to move to endophyte fungi that grow on them. Several plant endophyte fungi that grow on taxol producing yew trees have gained ability to make taxol themselves [12]. (Taxol is an anti-cancer drug also called paclitaxel found in yew trees.)

Horizontal transfer of genes from bacteria to some fungi, especially the yeast Saccharomyces cerevisiae movement of plant genes to fungi has been well documented. There is also recent evidence that the adzuki bean beetle has somehow acquired genetic material from its (non-beneficial) endosymbiont Wolbachia; however this claim is disputed and the evidence is not airtight.

Animals

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History of discovery of horizontal gene transfer

1946. The possiblity of horizontal gene transfer was first realised from study of bacterial genetics 1946, when Lederberg and Tatum discover genetic conjugation in Escherichia coli K-12 [13]

1959. Tomoichiro Akiba and Kunitaro Ochia discoverrd the fist interspecies gene transfer, mobile antibiotic resistance genes in bacteria [14].

1969. James Shapiro characterises the first mobile genes, transposons as spontaneously occuring insertions of large inserts of extra DNA can causes mutations in the galactose genes of the bacterium Escherichia coli [15].

see main article Horizontal gene transfer in prokaryotes

First glimses of horizontal transfer of traits in plant evolution

1940s. The earliest glimpses that eukaryotic genomes were indeed dynamic structures was obtained by Barbara McClintock in the 1940s at Cold Spring Harbor Laboratories, New York [16]. Her work led to recognition of transposons and other mobile DNAs in plants, which besides being able to move between different locations within a genome, also move between different species. By 1963 the parallels between McClintock's discoveries in maize and genetic instability in bacteria were clearly recognized [17].

1971.Horizontal gene transfer is suggested as an explanation[18] for the fact that similar traits are often shared by unrelated flowering plants, particularly by those sharing the same ecosystems, and for shared traits carried by plants and endophytic fungi that grow on their surfaces.

1980s. More generally, Horizontal gene transfer is now widely accepted as significant contributer to natural evolution in many species[19].

2003. It was shown that there is widespread horizontal transfer of mitochondrial genes among flowering plants. [20]

Discovery of mobile genes in eukaryotes, including mariners

1970. In February of 1970 wild male fruit-flies from Harbingen, Texas, were discovered to have a second X sex chromosome (dubbed the MR chromosome) that was inherited in an unusual way, and it also was noticed that this MR chromosome participated on genetic recombination, which does not normally occur in male fruit-flies[21].( In the fruit fly, (Drosophila melanogaster) sex is determined in a similar way to humans as far as the chromosomal make-up is concerned. Males are usually XY - Heterogametic and females homogametic XX.)

1970s. Mobile DNA in flies. This discovery of strange genetics in Drosophila immediately generated interest among geneticists, and during the 1970s, this and similar genetic instabilities of the fruit-fly were intensively investigated. By 1977 is was possible for M. Green to point out that the MR chromosome contained mobile genes (P-elements) that were similar to well characterised mobile DNA of bacteria (for instance Insertion sequences (IS) and mutator bacteriophage Mu). Mobile DNA from the MR chromosome had the to move to new chromosomal locations and promote chromosomal aberrations analogous to bacterial mobile DNA.[22]

1980s. By the early 1980s, Margaret Kidwell and others had already well documented the horizontal movement of mobile P genes in fruit fly populations [23], and the existance of horizontal gene transfer in insects, and the similarity of insect P mobile genes to bacterial mobile genes such as IS that have major natural roles in horizontal gene transfer in bacteria, was firmly established and widely known among professional geneticist.

1983. Hugh Robertson reported the widespread but patchy distribution of mariner mobile DNA in insects, and by 1999 Robertson and others had reported close relatives of this mobile DNA in mites, flatworms, hydras, insects, nematodes, mammals and humans.

2000. Subsequent to these discoveries horizontal gene movement has interested a wider audience. Horizontal gene transfer is called by some (Gogarten, 2000) "A New Paradigm for Biology " [24] and emphasised by others as an important factor in "The Hidden Hazards of Genetic Engineering". "While horizontal gene transfer is well-known among bacteria, it is only within the past 10 years that its occurrence has become recognized among higher plants and animals. The scope for horizontal gene transfer is essentially the entire biosphere, with bacteria and viruses serving both as intermediaries for gene trafficking and as reservoirs for gene multiplication and recombination (the process of making new combinations of genetic material)." [25].

HGT and genetic engineering

1975-present.Genetic engineering itself involves frequent use of artificial horizontal gene transfer. Molecular cloning technologies (genetic engineering) were developed in the 1970s using plasmids, the entities involved in much natural horizontal gene transfer from microorganisms, as tools to carry foreign DNA inserts in bacteria, and through use of plasmids as genetic engineering vectors biologists became aquainted with the concept that mammalian genes could function in bacteria, and that bacterial proteins could function in eukaryotes. Mobile DNA such as transposons is now widely used in in vivo genetic engineering in both bacteria and multicellular organs, but was pioneered by John Beckwith, David Botstein, Nancy Kleckner and John Roth in the 1960s-70s with bacteria.

Evolutionary theory

"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." [26]

Horizontal gene transfer is thus a potential confounding factor in inferring phylogenetic trees based on the sequence of one gene. 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 have substantially diverged. 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 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." [27]

"Using single genes as phylogenetic markers, it is difficult to trace organismal phylogeny in the presence of HGT [horizontal gene transfer]. Combining the simple coalescence model of cladogenesis with rare HGT [horizontal gene transfer] events suggest there was no single last 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." [28]

Uprooting the Tree of Life by W. Ford Doolittle (Scientific American, February 2000, pp 72-77) 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.

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."

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.
"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."

See also

References

  1. ↑ Beckwith, J. and Sihavy, T.J. (1992) The Power of Bacterial Genetics: A Literature-based Course. Cold Spring Harbor Laboratory Press. ISBN 0-87969-379-7
  2. ↑ Richards, T. A., Hirt, R. P., Williams, B. A. & Embley, T. M. (2003) Protist 1, 17–32.
  3. ↑ Graham H. Coomb Gareth D. Westrop, Pavel Suchan, Gabriela Puzova, Robert P. Hirt, T. Martin Embley, Jeremy C. Mottramc and Sylke Müllerd (2003) The amitochondriate eukaryote Trichomonas vaginalis contains a divergent thioredoxin-linked peroxiredoxin antioxidant system JBC Papers in Press. Published on November 20, 2003 as Manuscript M304359200
  4. ↑ Jan O Andersson, Robert P Hirt, Peter G Foster and Andrew J Roger (2006) Evolution of four gene families with patchy phylogenetic distributions: influx of genes into protist genomes BMC Evolutionary Biology 2006, 6:27 doi:10.1186/1471-2148-6-27
  5. ↑ Hwan Su Yoon, Jeremiah D. Hackett, Frances M. Van Dolah, Tetyana Nosenko*, Kristy L. Lidie and Debashish Bhattacharya (2005) Tertiary Endosymbiosis Driven Genome Evolution in Dinoflagellate Algae. Molecular Biology and Evolution 2005 22(5):1299-1308; doi:10.1093/molbev/msi118
  6. ↑ Maria Carmela Intrieri and Marcello Buiatti 2002 The Horizontal Transfer of Agrobacterium rhizogenes Genes and the Evolution of the Genus Nicotiana. Molecular Phylogenetics and Evolution Volume 20, Issue 1 , July 2001, Pages 100-110
  7. ↑ Robertson, H. M. (1993) The mariner transposable element is widespread in insects. Nature, 362: p241-245.
  8. ↑ Robertson, H. M. (1996) Reconstruction of the ancient mariners of humans. Nature Genetics 12, page 360-361.
  9. ↑ Loftus B, Anderson I, Davies R, Alsmark UCM, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillen N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El- Sayed NM, Petri WAJ, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N: The genome of the protist parasite Entamoeba histolytica. Nature 2005, 433(7028):865-868.
  10. ↑ Huang J, Mullapudi N, Lancto CA, Scott M, Abrahamsen MS, Kissinger JC: Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 2004, 5(11):R88.
  11. ↑ Doolittle WF.(1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes.Trends Genet. 1998 Aug;14(8):307-11.
  12. ↑ Shrestha K, Strobel GA, Shrivastava SP, Gewali MB. (2001) Evidence for paclitaxel from three new endophytic fungi of Himalayan yew of Nepal. Planta Med. 2001 Jun;67(4):374-6.
  13. ↑ Lederberg, J. and Tatum, E. L. (1946). Novel genotypes in mixed cultures of biochemical mutants of bacteria. Cold Spring Habor Symposia of Quantitative Biology. 11, p113.
  14. ↑ Ochia, K. Yamanaka, T. Kimura, K. and Sawada, O. (1959). Inheritance of drug resistance (and its transfer) between Shigella strains and between Shigella and E. coli strains. Nihon Iji Shimpo 1861: p34 (In Japanese)
  15. ↑ Shapiro, J. (1969) Mutations caused by the insertion of genetic material into the galactose operon of Escherichia coli. J. Molec. Biol. 40, p93-109.
  16. ↑ . McClintock, B. (1956). Controlling elements in maize. Cold Spring Habor Symposium on Quantitative Biology, 21, p197.
  17. ↑ Dawson, M. H. and Smith-Keary, P. F. (1963). Episomic control of mutation in Salmonella typhimurium. Heredity, 18, p1.
  18. ↑ Went, F. W. (1971). Parallel evolution. Taxon 20: p197-226.
  19. ↑ Margaret G. Kidwell (1983) Evolution of Hybrid Dysgenesis Determinants in Drosophila melanogaster PNAS 80: 1655-1659.
  20. ↑ Bergthorsson U, Adams KL, Thomason B, Palmer JD.(2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature. 2003 Jul 10;424(6945):197-201.
  21. ↑ Yuichiro Hiraizumi (1971). Spontaneous Recombination in Drosophila melanogaster Males. Proc. Natl. Acad. Sci. USA 68,268-270.
  22. ↑ Green, M. M. (1977) Genetic Instability in Drosophila melanogaster: De novo Induction of Putative Insertion Mutations.Proc. Nati. Acad. Sci. USA 74, 3490-3493.
  23. ↑ Margaret G. Kidwell (1983) Evolution of Hybrid Dysgenesis Determinants in Drosophila melanogaster PNAS 80: 1655-1659.
  24. ↑ [1]
  25. ↑ [2]
  26. ↑ [3]
  27. ↑ [4]
  28. ↑ [5]


Further Reading

  • 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. Steven L. Salzberg, Owen White, Jeremy Peterson, and Jonathan A. Eisen (2001) "Microbial Genes in the Human Genome: Lateral Transfer or Gene Loss?" Science 292, 1903-1906. [6] (Free full article)
  • This article seeks to shift the emphasis in early phylogenic adaptation from vertical to horizontal gene transfer. Woese, Carl (2002) "On the evolution of cells", PNAS, 99(13) 8742-8747. [7] (Free full article)
  • This article gives convincing evidence of horizontal transfer of bacterial DNA to Saccharomyces cerevisiae "Contribution of Horizontal Gene Transfer to the Evolution of Saccharomyces cerevisiae." Hall C, Brachat S, Dietrich FS. Eukaryot Cell 2005 Jun 4(6):1102-15. [8]
  • This book provides a comprehensive discussion of mobile DNA, jumping genes, transposons and the like in many organisms, not only bacteria. Berg, Douglas E. and Howe, Martha M. (Eds.)(1989). "Mobile DNA". American Society for Microbiology. Washington, D.C.
  • This article gives evidence, but does not conclusively prove, that Wolbachia DNA is in the azuki bean beetle genome (a species of bean weevil). Natsuko Kondo, Naruo Nikoh, Nobuyuki Ijichi, Masakazu Shimada and Takema Fukatsu (2002) "Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect", Proceedings of the National Academy of Sciences of the USA, 99 (22): 14280-14285". [9] (Free full article)
  • 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. Snel B, Bork P, Huynen MA (1999) "Genome phylogeny based on gene content", Nature Genetics, 21(1) 66-67. [10]
  • Webfocus in Nature with free review articles [11]
  • Uprooting the Tree of Life by W. Ford Doolitte (Scientific American, February 2000, pp 72-77)

External links

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