Horizontal gene transfer/Citable Version

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Legionella pneumophila are prokaryotic bacteria that are able to persist and reproduce inside phagocytic cells such as protists that have eaten them. They occasionally capture genes from their eukaryotic host cells, and are competant in transformation.

Horizontal gene transfer (HGT), also called lateral gene transfer (LGT), is any process in which an organism transfers genetic material to another cell or organism that is neither its own offspring created by division of its own cells, nor its progeny in sexual reproduction.

Horizontal gene transfer is quite distinct from common vertical gene transfer which involves simple inheritance of parental traits by the progeny as part of the normal organism's life cycle, be it a sexual fusion of gametes to form zygotes as occurs in animals and plants, or asexual propagation as occurs with microorganisms such as bacteria and fungi.

Horizontal gene transfer occurs at a lower frequency than vertical gene transfer. It thus is not easily detected directly, and its discovery depends on use of special techniques to enable rare genetic events to be detected or inferred.

The advent of genome science and bioinformatics has provided abundant indirect evidence that extensive natural horizontal gene transfer occurs between diverse biological taxa that are widely separated in the phylogenetic tree. These transfers include gene movement between different microbial species and other microbial taxa such as protists, between different plant families, and between different animals, and between bacteria and plants.

Gene transfers between different biological domains, such as between eukaryotic protists and bacteria [1] , or between bacteria and insects [2] are the most phylogenetically extreme cases of HGT. Bacterial "rol" genes from Agrobacterium species have for instance been found in plants of the tobacco (Nicotiniana) genus. [3].


Horizontal gene transfer is closely connected with mobile DNA ("jumping genes", transposons) and the dynamic changes that occur during genome evolution caused by the DNA rearrangement and transposition processes catalyzed by mobile DNA. Movement of mobile genes (such as transposons) within a genome, and between different parts of an organism's genome (that is, between the chromosomes of the nucleus, the circular mitochondrion chromosome, and the circular plastid (chloroplast) chromosome) are part of the mechanisms that enable horizontal gene transfer between different species.

Main features of horizontal gene transfer in nature

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
  • 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[4] [5] class of transposons, insertion sequence (IS) DNA, and retrovirus genes in diverse species, and shared mitochondrial genes in diverse flowering plants indicate that mobile DNA has natural pathways for movement between different species. Close relatives mariner mobile DNA have been discovered in organisms as diverse as mites, flatworms, hydras, insects, nematodes, mammals and humans[6] [7].
Millet. From: Jumping Genes Cross Plant Species Boundaries PLoS Biology Vol. 4, No. 1, e35 doi:10.1371/journal.pbio.0040035 Open Access License. A genome-wide analysis of millet and rice revealed the clear evidence of horizontal gene transfer between chromosomes in the nucleus of one plant to chromosomes in the nucleus of a reproductively isolated 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. Inter-domain transfer of several genes, from the eukaryote domain to the bacterial domain for instance, as represented by an "accidentally pathogenic" bacterium that resides and replicates within a vacuole of protist and mammalian macrophage cells, namely the Legionella pneumophila bacterium (see illustation image), has also been demonstrated [8].
  • Horizontal gene transfer is also common in diverse groups of unicellular protists, which often contain several genes transferred from both prokaryotes and other protists [9] [10] [11][12][13] [14].
  • Horizontal gene transfer occurs globally on a massive scale among marine microorganisms, and viruses, at total numbers near 1029 being the most many biological entities in the sea, are implicated as a major pathway for inter-species gene movement in the ocean. The estimated virus mediated gene transfer events in the Mediterranean sea are 1013 per year [15][16][17]. Endosymbiosis with an alga is identified as a route for horizontal gene transfer in marine dinoflagellates, the organisms that cause "red tides" [18].
  • 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 intimate 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 characterized but some are clearly identified. As horizontal gene transfer occurs at lower frequencies than with normal sexual reproduction within the species it is difficult to detect directly. Modern techniques of DNA analysis by providing detailed comparison of genomes provide much evidence for past occurrence of horizontal gene transfer. In insects, mites and insect viruses are established as probable vectors for transmission for horizontal gene transfer. In bacteria surface appendages called pili have evolved various roles in DNA uptake, DNA secretion and DNA transfer which have been extensively analyzed. Horizontal gene transfer in bacteria includes plasmid mediated promiscuous mating by bacteria, for instance by the crown-gall bacterium Agrobacterium tumefaciens[19], and carriage of genes between species by viruses[20][21][22]. Direct DNA uptake as another transfer mechanism is illustrated by Legionella bacteria, which are naturally competent for DNA uptake.

Prokaryotes

See main article Horizontal gene transfer in prokaryotes
The three main mechanisms of horizontal gene transfer in bacteria and archaea which this article discusses are:

Eukaryotes

Protists

Analysis of the complete genome sequence of the protist Entamoeba histolytica indicates 96 cases of relatively recent horizontal gene transfer from prokaryotes [23], whereas similar analysis of the complete genome sequence of the protist "Cryptosporidium parvum" reveal 24 candidates of horizontal gene transfer from bacteria [24].There is convincing evidence also that a bacterial gene for a biosynthetic enzyme has been recruited by the protist Trichomonas vaginalis from bacteria related to the ancestors of Pasteurella bacteria.[25] 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 occasionally the genome from food organisms [26]

Fungi

Comparison of the genome sequences of two fungi, the yeast Saccharomyces cerevisiae and Ashbya gossypii , has revealed that baker's yeast Saccharomyces has received two genes from bacteria by horizontal gene transfer. One of them codes for an enzyme that allows baker's yeast to make pyrimidine nucleotide bases anaerobically, and the other allows usage of sulfur from several organic sulfur sources.[27]. Other work with yeasts suggests that eight genes from Yarrowia lipolytica, five genes from Kluyveromyces lactis, and one gene from Debaryomyces hansenii are horizontally transferred. [28]

Other eukaryotes

Analysis of DNA sequences suggests that horizontal gene transfer has also generally occurred within multicellular eukaryotes, via a route that involves transfer of genes from their chloroplast and mitochondrial genomes to their nuclear genomes [29]. As stated in the endosymbiotic theory, chloroplasts and mitochondria probably originated as the bacterial endosymbionts of a progenitor to the eukaryotic cell.

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 [30]. (Taxol is an anti-cancer drug also called paclitaxel found in yew trees.)

Animals

Junk DNA is the most obvious general evidence of horizontal gene transfer in eukaryotes. Such seemingly non-functional repetitive DNA 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 [31].Retroviruses and retrotransposons are other examples of mobile horizontally transferred DNA found in animals.

The adzuki bean beetle, Callosobruchus chinensis, is infected with several distinct strains of bacterial Wolbachia endosymbionts. A genome fragment of one of these Wolbachia endosymbionts has been found transferred to the X chromosome of the host insect [32].

History of discovery of horizontal gene transfer

See main article Horizontal gene transfer (History)
  • Bacterial genetics starts in 1946
see also main article Horizontal gene transfer in prokaryotes
  • First glimpses of horizontal transfer of traits in plant evolution
see also main article Barbara McClintock
  • Discovery of mobile genes in flies, and mariner
  • HGT and genetic engineering

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." [33]

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.

To be specific, the most common gene to be used for constructing phylogenetic relationships in prokaryotes is the small subunit ribosomal RNA (SSU rRNA, 16s rRNA) gene, since its sequences tend to be conserved among members with close phylogenetic distances, but variable enough that differences can be measured [34][35]. The small subunit ribosomal RNA as a measure of evolutionary distances was pioneered by Carl Woese 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.)

However, in recent years it has been argued that small subunit ribosomal RNA genes can also be horizontally transferred. Although this may be infrequent, this possiblity is forcing scrutiny of the validity phylogenetic trees based on these small subunit ribosomal RNAs.

Metaphor of a net rather than a tree?

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 - the root of the Tree of Life - and the problems that arise with respect to that concept when one considers horizontal gene transfer. The article covers a wide area and provides a good introductory overview on horizonal gene transfer and evolution. In this article the microorganism Archaeoglobus fulgidus is cited (p.76) as being an anomaly with respect to a phylogenetic tree based upon the code 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.

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...

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 recognizable because much (though by no means all) of the gene transfer that occurs these days goes on within domains.

While dwelling on the challenges presented by reconstruction of the deeper branches of microbial evolution, biologist Gogarten reinforced these arguments and suggested that "the original metaphor of a tree no longer fits the data from recent genome research" and 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." [36] [37]

Resolution of uncertainty with Phylogenomics

Despite the uncertainties in reconstructing valid phylogenies back to the beginings of life, progress is being made in reconstructing the tree of life in the face of uncertainties raised by horizontal gene transfer.

Resolution of the uncertainty of any inferred phylogenetic tree based on a single gene can be achieved by deliberately using several common genes or even evidence from whole genomes [38] [39]. One approach of this type is sometime called multi-locus typing and has been used to deduce phylogenic trees for organisms that exchange genes, such as meningitis bacteria[40] [41] [42].

Jonathan Eisen and Claire Fraser have pointed out that:

In building the tree of life, analysis of whole genomes has begun to supplement, and in some cases to improve upon, studies previously done with one or a few genes. For example, recent studies of complete bacterial genomes have suggested that the hyperthermophilic species are not deeply branching; if this is true, it casts doubt on the idea that the first forms of life were thermophiles. Analysis of the genome of the eukaryotic parasite Encephalitozoon cuniculi supports suggestions that the group Microsporidia are not deep branching protists but are in fact members of the fungal kingdom. Genome analysis can even help resolve relationships within species, such as by providing new genetic markers for population genetics studies in the bacteria causing anthrax or tuberculosis. In all these studies, it is the additional data provided by a complete genome sequence that allows one to separate the phylogenetic signal from the noise. This is not to say the tree of life is now resolved— we only have sampled a smattering of genomes, and many groups are not yet touched[43].

See also

References

Citations

  1. ↑ Suwwan de Felipe K et al (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer J Bacteriol 187:7716-26
  2. ↑ Kondo N et al (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect PNAS USA 99:14280-5
  3. ↑ Intrieri MC, Buiatti M (2001) The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus "Nicotiana" Mol Phylogen Evol 20:100-10
  4. ↑ Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241-5
  5. ↑ Robertson HM (1996) Reconstruction of the ancient mariners of humans Nature Genetics 12:360-361
  6. ↑ Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241-5
  7. ↑ Robertson HM (1996) Reconstruction of the ancient mariners of humans Nature Genetics 12:360-1
  8. ↑ http://jb.asm.org/cgi/content/full/187/22/7716?view=long&pmid=16267296 de Felipe KS et al (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer J Bacteriol 187:7716-26
  9. ↑ Richards TA et al (2003) Protist 1:17–32
  10. ↑ Graham H. Coomb GH et al (2003) The amitochondriate eukaryote "Trichomonas vaginalis" contains a divergent thioredoxin-linked peroxiredoxin antioxidant system JBC Papers in Press. Published November 20, 2003 as Manuscript M304359200
  11. ↑ Andersson JO et al (2006) Evolution of four gene families with patchy phylogenetic distributions: influx of genes into protist genomes BMC Evolutionary Biology 6:27 doi:10.1186/1471-2148-6-27
  12. ↑ de Koning AP et al (2000) Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis Mol Biol Evol 17:1769-73
  13. ↑ Loftus B et al (2005) The genome of the protist parasite "Entamoeba histolytica" Nature 433:865-8
  14. ↑ Huang J et al (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in "Cryptosporidium parvum" Genome Biol 5:R88
  15. ↑ Weinbauer, Markus G. & Rassoulzadegan, Fereidoun (2004) Are viruses driving microbial diversification and diversity?.Environmental Microbiology 6 (1), 1-11. doi: 10.1046/j.1462-2920.2003.00539.x
  16. ↑ Paul, J.H. (1999) Microbial gene transfer. J Mol Microbiol Biotechnol 1: 45–50.
  17. ↑ Fuhrman, J.A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541–548.
  18. ↑ Yoon HS et al (2005) Tertiary endosymbiosis driven genome evolution in dinoflagellate algae Mol Biol Evol 22:1299-1308; doi:10.1093/molbev/msi118
  19. ↑ Zhu J et al (2000) The bases of crown gall tumorigenesis J Bacteriol 182:3885-95
  20. ↑ Weinbauer, Markus G. & Rassoulzadegan, Fereidoun (2004) Are viruses driving microbial diversification and diversity?.Environmental Microbiology 6 (1), 1-11. doi: 10.1046/j.1462-2920.2003.00539.x
  21. ↑ Analysing incompatibility — Wolbachia on the couch Nature Rev Microbiol 3:667 (2005); doi:10.1038/nrmicro1242
  22. ↑ Besser TE et al (2006) Greater diversity of Shiga toxin-encoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than from humans Appl Environ Microbiol [Epub ahead of print]
  23. ↑ Loftus B et al (2005) The genome of the protist parasite "Entamoeba histolytica" Nature 433:865-8
  24. ↑ Huang J et al (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in "Cryptosporidium parvum" Genome Biol 5:R88
  25. ↑ de Koning et al (2000) Trichomonas vaginalis . Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol Biol Evol 17:1769-73
  26. ↑ Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes Trends Genet 14:307-11
  27. ↑ http://ec.asm.org/cgi/content/abstract/4/6/1102?ijkey=c901c5b18b97e28f1dd1d811d53d3c5ec8dd469c&keytype2=tf_ipsecsha Hall CS et al(2005) Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell 4:1102-1115
  28. ↑ Dujon B et al {2004) Genome evolution in yeasts. Nature 430:35-44.
  29. ↑ Gray MW (1993) Origin and evolution of organelle genomes Curr Opin Genet Dev 3:884-90
  30. ↑ Shrestha K, Strobel GA, Shrivastava SP, Gewali MB. (2001) Evidence for paclitaxel from three new endophytic fungi of Himalayan yew of Nepal Planta Med 67:374-6
  31. ↑ Robertson HM (1996) Reconstruction of the ancient mariners of humans. Nature Genetics 12:360-361.
  32. ↑ Kondo N et al (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect PNAS USA 99:14280-5
  33. ↑ Horizontal Gene Transfer, Oklahoma State
  34. ↑ Woese C, Kandler O, Wheelis M (1990). "Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.". Proc Natl Acad Sci U S A 87 (12): 4576-9. PMID 2112744.
  35. ↑ Woese C, Fox G (1977). "Phylogenetic structure of the prokaryotic domain: the primary kingdoms.". Proc Natl Acad Sci U S A 74 (11): 5088-90. PMID 270744.
  36. ↑ Horizontal Gene Transfer - A New Paradigm for Biology, Peter Gogarten PhD
  37. ↑ Zhaxybayeva O, Gogarten JP (2004) Cladogenesis, coalescence and the evolution of the three domains of life Trends in Genetics 20:
  38. ↑ Henz SR et al (2005) Whole-genome prokaryotic phylogeny Bioinformatics 21:2329-35 Epub 2004 May 27. PMID 15166018
  39. ↑ Fitzpatrick DA et al (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99
  40. ↑ Urwin R, Maiden MC (2003) Multi-locus sequence typing: a tool for global epidemiology Trends Microbiol 11:479-87
  41. ↑ Yang Z (2002) Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci Genetics 162:1811-23
  42. ↑ Jennings WB, Edwards SV (2005) Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees Evolution Int J Org Evolution 59:2033-47
  43. ↑ Eisen, Jonathan A. and Fraser, Claire M. (2003) Viewpoint Phylogenomics: Intersection of Evolution and Genomics. Science 13 June 2003:Vol. 300. no. 5626, pp. 1706 - 1707 DOI: 10.1126/science.1086292

Further Reading

  • A very readable outline of the discovery of genes that move between rice and millet: Jumping genes cross plant species boundaries (2006) PLoS Biol 4: e35 DOI: 10.1371/journal.pbio.0040035
  • 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: Salzberg SL et al (2001) Microbial genes in the human genome: lateral transfer or gene loss?" Science 292:1903-1906 [1] (Free full article)
  • This article shifts the emphasis in early phylogenic adaptation from vertical to horizontal gene transfer. Woese C (2002) On the evolution of cells PNAS USA 99:8742-7 [2] (Free full article)
  • Convincing evidence of horizontal transfer of bacterial DNA to Saccharomyces cerevisiae: Hall C et al (2005) Contribution of horizontal gene transfer to the evolution of "Saccharomyces cerevisiae" Eukaryot Cell 4:1102-15
  • Book providing a comprehensive discussion of mobile DNA, jumping genes, transposons and the like in many organisms, not only bacteria. Berg DE, Howe MM (Eds.)(1989) "Mobile DNA". American Society for Microbiology. Washington D.C.
  • Proposal for 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 et al (1999) Genome phylogeny based on gene content Nature Genetics 21:66-67 [3]
  • This article describes the biology of crown-gall bacterium. The mechanism of DNA injection by this bacterium has been extensively dissected: Zhu J et al (2000) The bases of crown gall tumorigenesis J Bacteriol 182:3885-95 and provides detailed understanding of a process by which genes can move between bacterial species and from bacteria to eukaryotic organisms, and an illustration of the extent to which different species can co-evolve
  • Uprooting the Tree of Life by W. Ford Doolitte (Scientific American February 2000, pp 72-7)
  • A comprehensive treatise: Syvanen M, Kado CI (2002) Horizontal Gene Transfer, 2nd edition, Academic Press.ISBN 0-12-680126-6

External links


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