The advantages and disadvantages of horizontal gene transfer and the emergence of the first species
Tóm tắt
Horizontal Gene Transfer (HGT) is beneficial to a cell if the acquired gene confers a useful function, but is detrimental if the gene has no function, if it is incompatible with existing genes, or if it is a selfishly replicating mobile element. If the balance of these effects is beneficial on average, we would expect cells to evolve high rates of acceptance of horizontally transferred genes, whereas if it is detrimental, cells should reduce the rate of HGT as far as possible. It has been proposed that the rate of HGT was very high in the early stages of prokaryotic evolution, and hence there were no separate lineages of organisms. Only when the HGT rate began to fall, would lineages begin to emerge with their own distinct sets of genes. Evolution would then become more tree-like. This phenomenon has been called the Darwinian Threshold. We study a model for genome evolution that incorporates both beneficial and detrimental effects of HGT. We show that if rate of gene loss during genome replication is high, as was probably the case in the earliest genomes before the time of the last universal common ancestor, then a high rate of HGT is favourable. HGT leads to the rapid spread of new genes and allows the build-up of larger, fitter genomes than could be achieved by purely vertical inheritance. In contrast, if the gene loss rate is lower, as in modern prokaryotes, then HGT is, on average, unfavourable. Modern cells should therefore evolve to reduce HGT if they can, although the prevalence of independently replicating mobile elements and viruses may mean that cells cannot avoid HGT in practice. In the model, natural selection leads to gradual improvement of the replication accuracy and gradual decrease in the optimal rate of HGT. By clustering genomes based on gene content, we show that there are no separate lineages of organisms when the rate of HGT is high; however, as the rate of HGT decreases, a tree-like structure emerges with well-defined lineages. The model therefore passes through a Darwinian Threshold. This article was reviewed by Eugene V. Koonin, Anthony Poole and J. Peter Gogarten.
Tài liệu tham khảo
Gogarten JP, Doolittle WF, Lawrence JG: Prokaryotic Evolution in Light of Gene Transfer. Mol Biol Evol. 2002, 19: 2226-2238.
Bapteste E, O'Malley MA, Beiko RG, Ereshefsky M, Gogarten JP, Franklin-Hall L, Lapointe FJ, Dupre J, Daga T, Boucher Y, Martin W: Prokaryotic evolution and the tree of life are two different things. Biology Direct. 2009, 4: 34-10.1186/1745-6150-4-34.
Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P: Toward automatic reconstruction of a highly-resolved tree of life. Science. 2006, 311: 1283-1287. 10.1126/science.1123061.
Dagan T, Martin W: The tree of one percent. Genome Biol. 2006, 7: 118-10.1186/gb-2006-7-10-118.
Ge F, Wang LS, Kim J: The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PloS Biol. 2005, 3: 1709-1718. 10.1371/journal.pbio.0030316.
Puigbò P, Wolf YI, Koonin EV: Search for a 'Tree of Life' in the thicket of the phylogenetic forest. J Biol. 2009, 8: 59-
Woese CR: On the evolution of cells. Proc Nat Acad Sci USA. 2002, 99: 8742-8747. 10.1073/pnas.132266999.
Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R: The microbial pan-genome. Current Opinion Genet Devel. 2005, 15: 589-594. 10.1016/j.gde.2005.09.006.
Lapierre P, Gogarten JP: Estimating the size of the bacterial pan-genome. Trends Genet. 2008, 25: 107-110. 10.1016/j.tig.2008.12.004.
Lorenz MG, Wackernagel W: Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev. 1994, 58: 563-602.
Thomas CM, Nielsen KM: Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol. 2005, 3: 711-721. 10.1038/nrmicro1234.
Frost LS, Leplae R, Summers AO, Toussaint A: Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol. 2005, 3: 722-732. 10.1038/nrmicro1235.
Matic I, Rayssiguier C, Radman M: Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in the evolution of species. Cell. 1995, 80: 507-515. 10.1016/0092-8674(95)90501-4.
Cohan FM: Sexual isolation and speciation in bacteria. Genetica. 2002, 116: 359-370. 10.1023/A:1021232409545.
Rocha EP, Danchin A, Viari A: Evolutionary role of restriction/modification systems as revealed by comparative genome analysis. Genome Res. 2001, 11: 946-958. 10.1101/gr.GR-1531RR.
Navarre WW, McClelland M, Libby SJ, Fang FC: Silencing of xenogenic DNA by H-NS: facilitation of lateral gene transfer in bacteria by a defence system that recognizes foreign DNA. Genes Devel. 2007, 21: 1456-1471. 10.1101/gad.1543107.
Korbel JO, Snel B, Huynen MA, Bork P: SHOT: a web server for the construction of genome phylogenies. Trends Genet. 2002, 18: 158-162. 10.1016/S0168-9525(01)02597-5.
Biebricher CK, Eigen M: The error threshold. Virus Res. 2005, 107: 117-127. 10.1016/j.virusres.2004.11.002.
Eigen M, Schuster P: The Hypercycle: A principle of natural self-organization. 1979, Berlin: Springer
Wu M, Higgs PG: Origin of Self-replicating Biopolymers: Autocatalytic Feedback can Jump-start the RNA World. J Mol Evol. 2009, 69: 541-554. 10.1007/s00239-009-9276-8.
Szathmáry E, Demeter L: Group selection of early replicators and the origin of life. J Theor Biol. 1987, 128: 463-486.
Niesert U, Harnasch D, Bresch C: Origin of life between Scylla and Charybdis. J Mol Evol. 1981, 17: 348-353. 10.1007/BF01734356.
Koch AL: Evolution vs the number of gene copies per primitive cell. J Mol Evol. 1984, 20: 71-76. 10.1007/BF02101988.
Grey D, Hutson V, Szathmáry E: A reexamination of the stochastic corrector model. Proc R Soc Lond B Biol Sci. 1995, 262: 29-35. 10.1098/rspb.1995.0172.
Maynard Smith J, Szathmary E: The origin of chromosomes I. Selection for linkage. J Theor Biol. 1993, 164: 437-446. 10.1006/jtbi.1993.1165.
Poole AM: Horizontal gene transfer and the earliest stages of the evolution of life. Res Microbiol. 2009, 160: 473-480. 10.1016/j.resmic.2009.07.009.
Finkel SE, Kolter R: DNA as a nutrient: Novel role for bacterial competence gene homologs. J Bacteriol. 2001, 183: 6288-6293. 10.1128/JB.183.21.6288-6293.2001.
Claverys JP, Prudhomme M, Martin B: Induction of competence regulons as a general response to stress in Gram-positive bacteria. Annu Rev Microbiol. 2006, 60: 451-475. 10.1146/annurev.micro.60.080805.142139.
Hao W, Golding GB: The fate of laterally transferred genes: Life in the fast lane to adaptation or death. Genome Res. 2006, 16: 636-643. 10.1101/gr.4746406.
Kuo CH, Ochman H: The fate of new bacterial genes. FEMS Microbiol Rev. 2009, 33: 38-43. 10.1111/j.1574-6976.2008.00140.x.
Cordero OX, Hogeweg P: The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proc Nat Acad Sci USA. 2009, 106: 21748-21753. 10.1073/pnas.0907584106.
Novozhilov AS, Karev GP, Koonin EV: Mathematical modelling of evolution of horizontally transferred genes. Mol Biol Evol. 2005, 22: 1721-1732. 10.1093/molbev/msi167.
Baumdicker F, Hess WR, Pfaffelhuber P: The diversity of a distributed genome in bacterial populations. Ann Appl Prob. 2010, [http://www.imstat.org/aap/future_papers.html]
Maynard Smith J: Hypercycles and the origin of life. Nature. 1979, 280: 445-446. 10.1038/280445a0.
Maynard Smith J, Szathmáry E: The major transitions in evolution. 1995, Oxford: W.H. Freeman/Spektrum
Andam CP, Williams D, Gogarten JP: Biased gene transfer mimics patterns created through shared ancestry. Proceedings of the National Academy of Sciences of the United States of America. 2010, 107: 10679-10684. 10.1073/pnas.1001418107.
Vos M: Why do bacteria engage in homologous recombination?. Trends in microbiology. 2009, 17: 226-232. 10.1016/j.tim.2009.03.001.
Muller HJ: The relation of recombination to mutational advance. Mutat Res. 1964, 1: 2-9. 10.1016/0027-5107(64)90047-8.
Papke RT: A Critique of Prokaryotic Species Concepts. Methods in molecular biology (Clifton, NJ). 2009, 532: 379-395. full_text.
Hendrickson H, Lawrence JG: Selection for chromosome architecture in bacteria. J Mol Evol. 2006, 62: 615-629. 10.1007/s00239-005-0192-2.
Findlay WA, Redfield RJ: Coevolution of DNA uptake sequences and bacterial proteomes. Genome Biol Evol. 2009, 1: 45-55. 10.1093/gbe/evp005.
Gogarten JP, Townsend JP: Horizontal gene transfer, genome innovation and evolution. Nature reviews. 2005, 3: 679-687. 10.1038/nrmicro1204.
Lawrence JG, Ochman H: Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol. 1997, 44: 383-397. 10.1007/PL00006158.
Mira A, Ochman H, Moran NA: Deletional bias and the evolution of bacterial genomes. Trends Genet. 2001, 17: 589-596. 10.1016/S0168-9525(01)02447-7.
Williams D, Andam CP, Gogarten JP: Horizontal Gene Transfer and the Formation of Groups of Microorganisms. Molecular Phylogeny of Microorganisms. Edited by: Oren A. 2010, Papke RT: Caister Academic Press
Blankenship RE: Origin and Early Evolution of Photosynthesis. Photosynth Res. 1992, 33 (2): 91-111. 10.1007/BF00039173.
Fournier GP, Gogarten JP: Evolution of acetoclastic methanogenesis in Methanosarcina via horizontal gene transfer from cellulolytic Clostridia. Journal of bacteriology. 2008, 190 (3): 1124-1127. 10.1128/JB.01382-07.
Lang AS, Beatty JT: Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends in microbiology. 2007, 15 (2): 54-62. 10.1016/j.tim.2006.12.001.
Olendzenski L, Gogarten JP: Evolution of genes and organisms: the tree/web of life in light of horizontal gene transfer. Annals of the New York Academy of Sciences. 2009, 1178: 137-145. 10.1111/j.1749-6632.2009.04998.x.
Gogarten JP, Taiz L: Evolution of proton pumping ATPases: Rooting the tree of life. Photosynthesis Research. 1992, 33: 137-146. 10.1007/BF00039176.
Zhaxybayeva O, Gogarten JP: Cladogenesis, coalescence and the evolution of the three domains of life. Trends in Genetics. 2004, 20 (4): 182-187. 10.1016/j.tig.2004.02.004.
Zhaxybayeva O, Lapierre P, Gogarten JP: Ancient gene duplications and the root(s) of the tree of life. Protoplasma. 2005, 227 (1): 53-64. 10.1007/s00709-005-0135-1.
Fournier GP, Gogarten JP: Rooting the Ribosomal Tree of Life. Mol Biol Evol. 2010.
Dagan T, Roettger M, Bryant D, Martin W: Genome networks root the tree of life between prokaryotic domains. Genome Biol Evol. 2010, 2: 379-392. 10.1093/gbe/evq025.
Wolf YI, Aravind L, Grishin NV, Koonin EV: Evolution of aminoacyl-tRNA synthetases--analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome research. 1999, 9 (8): 689-710.