Crossing the line: Selection and evolution of virulence traits

PLoS Pathogens

Volumn 2, Issue 5, 2006, Pages 346-353

  Brown, Nat F ^a   Wickham, Mark E ^a   Coombes, Brian K ^a,b   Finlay, B Brett ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; LIFE CYCLE; MICROBIAL GROWTH; MUTATION RATE; NONHUMAN; PATHOGENESIS; REVIEW; VIRULENCE; VIRUS TRANSMISSION; ANIMAL; EVOLUTION; GENETIC SELECTION; GENETICS;

VIRULENCE FACTOR;

ANIMALS; EVOLUTION; HUMANS; SELECTION (GENETICS); VIRULENCE FACTORS;

EID: 33646901855     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020042     Document Type: Review

References (94)

1. Lederberg J (2000) Infectious history. Science 288: 287-293.
2. Darwin C (1859) On the origin of species by means of natural selection. London: John Murray.
3. Casadevall A, Pirofski LA (1999) Host-pathogen interactions: Redefining the basic concepts of virulence and pathogenicity. Infect Immun 67: 3703-3713.
4. de Roode JC, Pansini R, Cheesman SJ, Helinski ME, Huijben S, et al. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci U S A 102: 7624-7628.
5. Cooper VS, Reiskind MH, Miller JA, Shelton KA, Walther BA, et al. (2002) Timing of transmission and the evolution of virulence of an insect virus. Proc Biol Sci 269: 1161-1165.
6. Gandon S, Mackinnon MJ, Nee S, Read AF (2001) Imperfect vaccines and the evolution of pathogen virulence. Nature 414: 751-756.
7. Walther BA, Ewald PW (2004) Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc 79: 849-869.
8. Williams PD, Day T (2001) Interactions between sources of mortality and the evolution of parasite virulence. Proc Biol Sci 268: 2331-2337.
9. Day T (2002) On the evolution of virulence and the relationship between various measures of mortality. Proc Biol Sci 269: 1317-1323.
10. Lenski RE, May RM (1994) The evolution of virulence in parasites and pathogens: Reconciliation between two competing hypotheses. J Theor Biol 169: 253-265.
11. Lipsitch M, Moxon ER (1997) Virulence and transmissibility of pathogens: What is the relationship? Trends Microbiol 5: 31-37.
12. Falkow S (1997) What is a pathogen? ASM News 63: 159-165.
13. Shuman HA, Purcell M, Segal G, Hales L, Wiater LA (1998) Intracellular multiplication of Legionella pneumophila: Human pathogen or accidental tourist? Curr Top Microbiol Immunol 225: 99-112.
14. Casadevall A, Pirofski LA (2000) Host-pathogen interactions: Basic concepts of microbial commensalism, colonization, infection, and disease. Infect Immun 68: 6511-6518.
15. Reidl J, Klose KE (2002) Vibrio cholerae and cholera: Out of the water and into the host. FEMS Microbiol Rev 26: 125-139.
16. Alexander M (1981) Why microbial predators and parasites do not eliminate their prey and hosts. Annu Rev Microbiol 35: 113-133.
17. Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Ann Rev Ecol Syst 14: 465-485.
18. Chen RT, Broome CV, Weinstein RA, Weaver R, Tsai TF (1985) Diphtheria in the United States, 1971-81. Am J Public Health 75: 1393-1397.
19. Beuzon CR, Holden DW (2001) Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3: 1345-1352.
20. Day T (2002) The evolution of virulence in vector-borne and directly transmitted parasites. Theor Popul Biol 62: 199-213.
21. Ewald PW (1994) Evolution of infectious disease. New York: Oxford University Press. 298 p.
22. Stewart AD, Logsdon JM Jr, Kelley SE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution Int J Org Evolution 59: 730-739.
23. Andre JB, Hochberg ME (2005) Virulence evolution in emerging infectious diseases. Evolution Int J Org Evolution 59: 1406-1412.
24. Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, et al. (2005) Characterization of the 1918 influenza virus polymerase genes. Nature 437: 889-893.
25. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, et al. (1996) CC CKR5: A RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
26. Gabriel SE, Brigman KN, Koller BH, Boucher RC, Stutts MJ (1994) Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 266: 107-109.
27. Martinson JJ, Chapman NH, Rees DC, Liu YT, Clegg JB (1997) Global distribution of the CCR5 gene 32-basepair deletion. Nat Genet 16: 100-103.
28. Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189: 561-563.
29. Pasvol G, Jungery M, Weatherall DJ, Parsons SF, Anstee DJ, et al. (1982) Glycophorin as a possible receptor for Plasmodium falciparum. Lancet 2: 947-950.
30. Pasvol G, Weatherall DJ, Wilson RJ (1978) Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 274: 701-703.
31. Pier GB, Grout M, Zaidi T, Meluleni G, Mueschenborn SS, et al. (1998) Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393: 79-82.
32. Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, et al. (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9: 87-92.
33. Haas R, Meyer TF (1986) The repertoire of silent pilus genes in Neisseria gonorrhoeae: Evidence for gene conversion. Cell 44: 107-115.
34. Harris LA, Logan SM, Guerry P, Trust TJ (1987) Antigenic variation of Campylobacter flagella. J Bacteriol 169: 5066-5071.
35. Kamp D, Kahmann R, Zipser D, Broker TR, Chow LT (1978) Inversion of the G DNA segment of phage Mu controls phage infectivity. Nature 271: 577-580.
36. Lederberg J, Iino T (1956) Phase variation in Salmonella. Genetics 41: 743-757.
37. Swanson J, Bergstrom S, Robbins K, Barrera O, Corwin D, et al. (1986) Gene conversion involving the pilin structural gene correlates with pilus+ in equilibrium with pilus- changes in Neisseria gonorrhoeae. Cell 47: 267-276.
38. Symonds N, Coelho A (1978) Role of the G segment in the growth of phage Mu. Nature 271: 573-574.
39. Pays E, Van Assel S, Laurent M, Darville M, Vervoort T, et al. (1983) Gene conversion as a mechanism for antigenic variation in trypanosomes. Cell 34: 371-381.
40. Stern A, Brown M, Nickel P, Meyer TF (1986) Opacity genes in Neisseria gonorrhoeae: Control of phase and antigenic variation. Cell 47: 61-71.
41. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, et al. (2005) Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121: 13-24.
42. Freitas-Junior LH, Hernandez-Rivas R, Ralph SA, Montiel-Condado D, Ruvalcaba-Salazar OK, et al. (2005) Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121: 25-36.
43. Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284: 967-970.
44. Alcami A, Koszinowski UH (2000) Viral mechanisms of immune evasion. Immunol Today 21: 447-455.
45. Hengel H, Koszinowski UH (1997) Interference with antigen processing by viruses. Curr Opin Immunol 9: 470-476.
46. Smith GL (1996) Virus proteins that bind cytokines, chemokines or interferons. Curr Opin Immunol 8: 467-471.
47. Nuismer SL, Otto SP (2004) Host-parasite interactions and the evolution of ploidy. Proc Natl Acad Sci U S A 101: 11036-11039.
48. Earl DJ, Deem MW (2004) Evolvability is a selectable trait. Proc Natl Acad Sci U S A 101: 11531-11536.
49. Mao EF, Lane L, Lee J, Miller JH (1997) Proliferation of mutators in A cell population. J Bacteriol 179: 417-422.
50. Maisnier-Patin S, Roth JR, Fredriksson A, Nystrom T, Berg OG, et al. (2005) Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nat Genet 37: 1376-1379.
51. Gross MD, Siegel EC (1981) Incidence of mutator strains in Escherichia coli and coliforms in nature. Mutat Res 91: 107-110.
52. LeClerc JE, Li B, Payne WL, Cebula TA (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208-1211.
53. Pfeiffer JK, Kirkegaard K (2005) Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 1: e11.
54. Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148: 1667-1686.
55. Kepler TB (1997) Codon bias and plasticity in immunoglobulins. Mol Biol Evol 14: 637-643.
56. Plotkin JB, Dushoff J (2003) Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc Natl Acad Sci U S A 100: 7152-7157.
57. Bjorkman J, Nagaev I, Berg OG, Hughes D, Andersson DI (2000) Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479-1482.
58. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2: 414-424.
59. Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, et al. (1999) High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci U S A 96: 4506-4511.
60. Tait A (1980) Evidence for diploidy and mating in trypanosomes. Nature 287: 536-538.
61. Matthews L, Woolhouse M (2005) New approaches to quantifying the spread of infection. Nat Rev Microbiol 3: 529-536.
62. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, et al. (2000) Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299: 27-51.
63. Sanderson KE, Demerec M (1965) The linkage map of Salmonella typhimurium. Genetics 51: 897-913.
64. Yanofsky C, Lennox ES (1959) Transduction and recombination study of linkage relationships among the genes controlling tryptophan synthesis in Escherichia coli. Virology 8: 425-447.
65. Lawrence J (1999) Sel.sh operons: The evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev 9: 642-648.
66. Price MN, Huang KH, Arkin AP, Alm EJ (2005) Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res 15: 809-819.
67. Ochman H, Soncini FC, Solomon F, Groisman EA (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
68. Behlau I, Miller SI (1993) A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J Bacteriol 175: 4475-4484.
69. Bijlsma JJ, Groisman EA (2005) The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57: 85-96.
70. Lee AK, Detweiler CS, Falkow S (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J Bacteriol 182: 771-781.
71. Dorman CJ (2004) H-NS: A universal regulator for a dynamic genome. Nat Rev Microbiol 2: 391-400.
72. Cornelis GR, Sluiters C, Delor I, Geib D, Kaniga K, et al. (1991) ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Mol Microbiol 5: 1023-1034.
73. Ellison DW, Young B, Nelson K, Miller VL (2003) YmoA negatively regulates expression of invasion from Yersinia enterocolitica. J Bacteriol 185: 7153-7159.
74. Fahlen TF, Wilson RL, Boddicker JD, Jones BD (2001) Hha is a negative modulator of transcription of hilA, the Salmonella enterica serovar Typhimurium invasion gene transcriptional activator. J Bacteriol 183: 6620-6629.
75. Coombes BK, Wickham ME, Lowden MJ, Brown NF, Finlay BB (2005) Negative regulation of Salmonella pathogenicity island 2 is required for contextual control of virulence during typhoid. Proc Natl Acad Sci U S A 102: 17460-17465.
76. Ehrbar K, Hardt WD (2005) Bacteriophage-encoded type III effectors in Salmonella enterica subspecies 1 serovar Typhimurium. Infect Genet Evol 5: 1-9.
77. Coombes BK, Wickham ME, Brown NF, Lemire S, Bossi L, et al. (2005) Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar typhimurium with autonomous expression from its associated phage. J Mol Biol 348: 817-830.
78. Lederberg J, Cavalli LL, Lederberg EM (1952) Sex compatability in Escherichia coli. Genetics 37: 720-730.
79. Hayes W (1964) The genetics of bacteria and their viruses. New York: John Wiley & Sons Inc. 740 p.
80. Acheson DW, Reidl J, Zhang X, Keusch GT, Mekalanos JJ, et al. (1998) In vivo transduction with shiga toxin 1-encoding phage. Infect Immun 66: 4496-4498.
81. Toth I, Schmidt H, Dow M, Malik A, Oswald E, et al. (2003) Transduction of porcine enteropathogenic Escherichia coli with a derivative of a shiga toxin 2-encoding bacteriophage in a porcine ligated ileal loop system. Appl Environ Microbiol 69: 7242-7247.
82. Figueroa-Bossi N, Bossi L (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33: 167-176.
83. Wagner PL, Neely MN, Zhang X, Acheson DW, Waldor MK, et al. (2001) Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 183: 2081-2085.
84. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, et al. (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95: 3134-3139.
85. Lindsay JA, Ruzin A, Ross HF, Kurepina N, Novick RP (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29: 527-543.
86. O'Shea YA, Boyd EF (2002) Mobilization of the Vibrio pathogenicity island between Vibrio cholerae isolates mediated by CP-T1 generalized transduction. FEMS Microbiol Lett 214: 153-157.
87. Zhang X, McDaniel AD, Wolf LE, Keusch GT, Waldor MK, et al. (2000) Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis 181: 664-670.
88. Beaber JW, Hochhut B, Waldor MK (2004) SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427: 72-74.
89. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, et al. (2004) SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305: 1629-1631.
90. Rosenberger CM, Gallo RL, Finlay BB (2004) Interplay between antibacterial effectors: A macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc Natl Acad Sci U S A 101: 2422-2427.
91. Salomon RA, Farias RN (1992) Microcin 25, a novel antimicrobial peptide produced by Escherichia coli. J Bacteriol 174: 7428-7435.
92. Shi J, Ross CR, Chengappa MM, Sylte MJ, McVey DS, et al. (1996) Antibacterial activity of a synthetic peptide (PR-26) derived from PR-39, a proline-arginine-rich neutrophil antimicrobial peptide. Antimicrob Agents Chemother 40: 115-121.
93. Subbalakshmi C, Sitaram N (1998) Mechanism of antimicrobial action of indolicidin. FEMS Microbiol Lett 160: 91-96.
94. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U, et al. (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122: 461-472.