Horizontal Gene Transfer of the Secretome Drives the Evolution of Bacterial Cooperation and Virulence

Current Biology

Volumn 19, Issue 20, 2009, Pages 1683-1691

  Nogueira, Teresa ^a,b,c,d   Rankin, Daniel J ^e,f   Touchon, Marie ^a,b   Taddei, François ^g,h   Brown, Sam P ⁱ   Rocha, Eduardo P C ^a,b  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^d UNIVERSITY OF LISBON   (Portugal)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^g INSERM   (France)

^h UNIVERSITÉ PARIS DESCARTES   (France)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

EVOL_ECOL

Indexed keywords

ESCHERICHIA COLI PROTEIN;

ARTICLE; BACTERIAL GENOME; ESCHERICHIA COLI; GENETICS; HORIZONTAL GENE TRANSFER; ORGANISMAL INTERACTION; PATHOGENICITY; PHYSIOLOGY; SECRETION; THEORETICAL MODEL; VIRULENCE;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; MICROBIAL INTERACTIONS; MODELS, THEORETICAL; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA;

EID: 70350488795     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2009.08.056     Document Type: Article

References (72)

1. Ley R.E., Peterson D.A., and Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124 (2006) 837-848
2. Ochman H., and Jones I.B. Evolutionary dynamics of full genome content in Escherichia coli. EMBO J. 19 (2000) 6637-6643
3. Perna N.T., Plunkett III G., Burland V., Mau B., Glasner J.D., Rose D.J., Mayhew G.F., Evans P.S., Gregor J., Kirkpatrick H.A., et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409 (2001) 529-533
4. van Passel M.W., Marri P.R., and Ochman H. The emergence and fate of horizontally acquired genes in Escherichia coli. PLoS Comput. Biol. 4 (2008) e1000059
5. Touchon M., Hoede C., Tenaillon O., Barbe V., Baeriswyl S., Bidet P., Bingen E., Bonacorsi S., Bouchier C., Bouvet O., et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5 (2009) e1000344
6. Le Gall T., Clermont O., Gouriou S., Picard B., Nassif X., Denamur E., and Tenaillon O. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol. Biol. Evol. 24 (2007) 2373-2384
7. Henke J.M., and Bassler B.L. Bacterial social engagements. Trends Cell Biol. 14 (2004) 648-656
8. Sanchez B., Bressollier P., and Urdaci M.C. Exported proteins in probiotic bacteria: Adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol. Med. Microbiol. 54 (2008) 1-17
9. Cascales E., Buchanan S.K., Duche D., Kleanthous C., Lloubes R., Postle K., Riley M., Slatin S., and Cavard D. Colicin biology. Microbiol. Mol. Biol. Rev. 71 (2007) 158-229
10. Lehmann L., Bargum K., and Reuter M. An evolutionary analysis of the relationship between spite and altruism. J. Evol. Biol. 19 (2006) 1507-1516
11. West S.A., Griffin A.S., Gardner A., and Diggle S.P. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4 (2006) 597-607
12. Brown S.P., and Buckling A. A social life for discerning microbes. Cell 135 (2008) 600-603
13. Smith J. The social evolution of bacterial pathogenesis. Proc. Biol. Sci. 268 (2001) 61-69
14. Hamilton W.D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7 (1964) 1-16
15. Rousset F., and Ronce O. Inclusive fitness for traits affecting metapopulation demography. Theor. Popul. Biol. 65 (2004) 127-141
16. Lehmann L., Feldman M.W., and Foster K.R. Cultural transmission can inhibit the evolution of altruistic helping. Am. Nat. 172 (2008) 12-24
17. Lehmann L., and Keller L. The evolution of cooperation and altruism-a general framework and a classification of models. J. Evol. Biol. 19 (2006) 1365-1376
18. Gardy J.L., and Brinkman F.S. Methods for predicting bacterial protein subcellular localization. Nat. Rev. Microbiol. 4 (2006) 741-751
19. Tobe T., Beatson S.A., Taniguchi H., Abe H., Bailey C.M., Fivian A., Younis R., Matthews S., Marches O., Frankel G., et al. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc. Natl. Acad. Sci. USA 103 (2006) 14941-14946
20. Griffin A.S., West S.A., and Buckling A. Cooperation and competition in pathogenic bacteria. Nature 430 (2004) 1024-1027
21. Sandoz K.M., Mitzimberg S.M., and Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. USA 104 (2007) 15876-15881
22. Daubin V., and Ochman H. Bacterial genomes as new gene homes: The genealogy of ORFans in E. coli. Genome Res. 14 (2004) 1036-1042
23. Kurokawa K., Itoh T., Kuwahara T., Oshima K., Toh H., Toyoda A., Takami H., Morita H., Sharma V.K., Srivastava T.P., et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 14 (2007) 169-181
24. Brown S.P., Hochberg M.E., and Grenfell B.T. Does multiple infection select for raised virulence?. Trends Microbiol. 10 (2002) 401-405
25. Harrison F., Browning L.E., Vos M., and Buckling A. Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol. 4 (2006) 21
26. Steiner T.S., Lima A.A., Nataro J.P., and Guerrant R.L. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J. Infect. Dis. 177 (1998) 88-96
27. Schlee M., Wehkamp J., Altenhoefer A., Oelschlaeger T.A., Stange E.F., and Fellermann K. Induction of human beta-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect. Immun. 75 (2007) 2399-2407
28. Pruimboom-Brees I.M., Morgan T.W., Ackermann M.R., Nystrom E.D., Samuel J.E., Cornick N.A., and Moon H.W. Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc. Natl. Acad. Sci. USA 97 (2000) 10325-10329
29. Akashi H., and Gojobori T. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. USA 99 (2002) 3695-3700
30. Dionisio F., Matic I., Radman M., Rodrigues O.R., and Taddei F. Plasmids spread very fast in heterogeneous bacterial communities. Genetics 162 (2002) 1525-1532
31. Perez-Mendoza D., and de la Cruz F. Escherichia coli genes affecting recipient ability in plasmid conjugation: Are there any?. BMC Genomics 10 (2009) 71
32. West S.A., Griffin A.S., and Gardner A. Social semantics: Altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20 (2007) 415-432
33. Frank S.A. Perspective: Repression of competition and the evolution of cooperation. Evolution Int. J. Org. Evolution 57 (2003) 693-705
34. Naito T., Kusano K., and Kobayashi I. Selfish behavior of restriction-modification systems. Science 267 (1995) 897-899
35. Hayes F. Toxins-antitoxins: Plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301 (2003) 1496-1499
36. Rowe-Magnus D.A., Guerout A.M., Biskri L., Bouige P., and Mazel D. Comparative analysis of superintegrons: Engineering extensive genetic diversity in the Vibrionaceae. Genome Res. 13 (2003) 428-442
37. Hartl D.L., and Dykhuizen D.E. The population genetics of Escherichia coli. Annu. Rev. Genet. 18 (1984) 31-68
38. O'Ryan M., Prado V., and Pickering L.K. A millennium update on pediatric diarrheal illness in the developing world. Semin. Pediatr. Infect. Dis. 16 (2005) 125-136
39. Smith P.A., and Romesberg F.E. Combating bacteria and drug resistance by inhibiting mechanisms of persistence and adaptation. Nat. Chem. Biol. 3 (2007) 549-556
40. Brown S.P., West S.A., Diggle S.P., and Griffin A.S. Social evolution in microorganisms and a Trojan horse approach to medical intervention strategies. Philos. Trans. R. Soc. Lond. B Biol. Sci. (2009) in press
41. Finlay B.B., and Falkow S. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61 (1997) 136-169
42. Wildschutte H., Wolfe D.M., Tamewitz A., and Lawrence J.G. Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc. Natl. Acad. Sci. USA 101 (2004) 10644-10649
43. Petersen L., Bollback J.P., Dimmic M., Hubisz M., and Nielsen R. Genes under positive selection in Escherichia coli. Genome Res. 17 (2007) 1336-1343
44. Moxon E.R., Rainey P.B., Nowak M.A., and Lenski R.E. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4 (1994) 24-33
45. Palmer G.H., and Brayton K.A. Gene conversion is a convergent strategy for pathogen antigenic variation. Trends Parasitol. 23 (2007) 408-413
46. Shih A.C., Hsiao T.C., Ho M.S., and Li W.H. Simultaneous amino acid substitutions at antigenic sites drive influenza A hemagglutinin evolution. Proc. Natl. Acad. Sci. USA 104 (2007) 6283-6288
47. Mrazek J., Guo X., and Shah A. Simple sequence repeats in prokaryotic genomes. Proc. Natl. Acad. Sci. USA 104 (2007) 8472-8477
48. Treangen T.J., Abraham A.L., Touchon M., and Rocha E.P. Genesis, effects and fates of repeats in prokaryotic genomes. FEMS Microbiol. Rev. 33 (2009) 539-571
49. Bayliss C.D. Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol. Rev. 33 (2009) 504-520
50. Lawrence J.G., and Roth J.R. Selfish operons: Horizontal transfer may drive the evolution of gene clusters. Genetics 143 (1996) 1843-1860
51. Amábile-Cuevas C.F., and Chicurel M.E. Bacterial plasmids and gene flux. Cell 70 (1992) 189-199
52. Burrus V., Pavlovic G., Decaris B., and Guedon G. Conjugative transposons: The tip of the iceberg. Mol. Microbiol. 46 (2002) 601-610
53. Bates S., Cashmore A.M., and Wilkins B.M. IncP plasmids are unusually effective in mediating conjugation of Escherichia coli and Saccharomyces cerevisiae: Involvement of the tra2 mating system. J. Bacteriol. 180 (1998) 6538-6543
54. Ghigo J.M. Natural conjugative plasmids induce bacterial biofilm development. Nature 412 (2001) 442-445
55. Foster K.R., and Wenseleers T. A general model for the evolution of mutualisms. J. Evol. Biol. 19 (2006) 1283-1293
56. Gordon D.M., Bauer S., and Johnson J.R. The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148 (2002) 1513-1522
57. Probert C.J., Emmett P.M., and Heaton K.W. Intestinal transit time in the population calculated from self made observations of defecation. J. Epidemiol. Community Health 47 (1993) 331-333
58. Acheson D.W., Reidl J., Zhang X., Keusch G.T., Mekalanos J.J., and Waldor M.K. In vivo transduction with shiga toxin 1-encoding phage. Infect. Immun. 66 (1998) 4496-4498
59. Netherwood T., Bowden R., Harrison P., O'Donnell A.G., Parker D.S., and Gilbert H.J. Gene transfer in the gastrointestinal tract. Appl. Environ. Microbiol. 65 (1999) 5139-5141
60. Dionisio F. Plasmids survive despite their cost and male-specific phages due to heterogeneity of bacterial populations. Evol. Ecol. Res. 7 (2005) 1089-1107
61. Lili L.N., Britton N.F., and Feil E.J. The persistence of parasitic plasmids. Genetics 177 (2007) 399-405
62. Brown S.P., Le Chat L., De Paepe M., and Taddei F. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16 (2006) 2048-2052
63. Bremer H., and Dennis P.P. Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt F.C., and Curtiss R. (Eds). Escherichia coli and Salmonella: Cellular and Molecular Biology (1996), ASM Press, Washington, DC 1553-1569
64. Stoebel D.M., Dean A.M., and Dykhuizen D.E. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178 (2008) 1653-1660
65. Hamilton W.D. The genetical theory of kin selection. J. Theor. Biol. 7 (1964) 1-52
66. Soler M., Soler J., Martinez J., and Moller A. Magpie host manipulation by great spotted cuckoos: Evidence for an avian mafia?. Evolution Int. J. Org. Evolution 49 (1995) 770-775
67. Thomas F., Adamo S., and Moore J. Parasitic manipulation: Where are we and where should we go?. Behav. Processes 68 (2005) 185-199
68. Paradis E., Claude J., and Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20 (2004) 289-290
69. Emanuelsson O., Brunak S., von Heijne G., and Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protocols 2 (2007) 953-971
70. Gardy J.L., Laird M.R., Chen F., Rey S., Walsh C.J., Ester M., and Brinkman F.S. PSORTb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21 (2005) 617-623
71. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
72. Rice P., Longden I., and Bleasby A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16 (2000) 276-277