Postgenomic analysis of bacterial pathogens repertoire reveals genome reduction rather than virulence factors

Briefings in Functional Genomics

Volumn 12, Issue 4, 2013, Pages 291-304

  Merhej, Vicky ^a   Georgiades, Kalliopi ^b   Raoult, Didier ^c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF CYPRUS   (Cyprus)

^c AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Antivirulence genes; Microbial genomics; Pathogenicity; Reductive evolution; Toxin

Indexed keywords

ANTITOXIN; DNA; RIBOSOME RNA; TOXIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; DNA REPLICATION; GENE SEQUENCE; GENOMICS; MICROORGANISM DETECTION; MOLECULAR EVOLUTION; MYCOBACTERIUM; NONHUMAN; OPERON; PATHOGENICITY; REDUCTION; RICKETTSIA; SHIGELLA; YERSINIA PESTIS;

ANTIVIRULENCE GENES; MICROBIAL GENOMICS; PATHOGENICITY; REDUCTIVE EVOLUTION; TOXIN;

BACTERIA; BIOLOGICAL EVOLUTION; GENOME, BACTERIAL; VIRULENCE; VIRULENCE FACTORS;

EID: 84882967629     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/elt015     Document Type: Article

References (95)

1. Wilson G, Miles A, Parker MT. Topley and Wilson's Principles of Bacteriology, Virology and Immunity. 7 edn. London: Edward Arnold, 1983.
2. Roux E, Yersin A. Contribution à l'étude de la diphthérie. Ann Inst Pasteur 1888;2:620-9.
3. Ramon G. Sur le pouvoir floculant et sur les propriétés immunisantes d'une toxine diphthérique rendue anatoxique (anatoxine). Comptes rendues de l'académie de sciences 1923;177: 1330-8.
4. Pasteur L. De l'atténuation du virus du cholera des poules. CR Acad Sci Paris 1880;91:673-80.
5. Fleischmann RD, Adams MD, White O, et al. Wholegenome random sequencing and assembly of Haemophilus influenzae Rd. Science 1995;269:496-512.
6. Ogata H, Audic S, Renesto-Audiffren P, et al. Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 2001;293:2093-8.
7. Brosch R, Gordon SV, Pym A, et al. Comparative genomics of the Mycobacteria. Int J Med Microbiol 2000;290: 143-52.
8. Cole ST, Eiglmeier K, Parkhill J, et al. Massive gene decay in the leprosy bacillus. Nature 2001;409:1007-11.
9. Schmidt H, Hensel M. Pathogenicity islands in bacterial pathogenesis. ClinMicrobiol Rev 2004;17:14-56.
10. Dobrindt U, Hochhut B, Hentschel U, et al. Genomic islands in pathogenic and environmental microorganisms. Nat RevMicrobiol 2004;2:414-24.
11. Hacker J, Blum-Oehler G, Muhldorfer I, et al. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 1997;23: 1089-97.
12. Cossart P, Vicente MF, Mengaud J, et al. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun 1989;57:3629-36.
13. Dobrindt U, Blum-Oehler G, Nagy G, et al. Genetic structure and distribution of four pathogenicity islands (PAI I(536) to PAI IV(536)) of uropathogenic Escherichia coli strain 536. Infect Immun 2002;70:6365-72.
14. Jermyn WS, Boyd EF. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 2002;148:3681-93.
15. Perna NT, Plunkett G, III, Burland V, et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 2001;409:529-33.
16. Braun V, Hundsberger T, Leukel P, et al. Definition of the single integration site of the pathogenicity locus in Clostridium difficile. Gene 1996;181:29-38.
17. Carbonetti NH. Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. FutureMicrobiol 2010;5:455-69.
18. Fitzgerald JR, Monday SR, Foster TJ, et al. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 2001;183: 63-70.
19. Lindsay JA, Ruzin A, Ross HF, et al. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 1998;29: 527-43.
20. Christie PJ. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. MolMicrobiol 2001;40:294-305.
21. Cornelis GR, Van GF. Assembly and function of type III secretory systems. Annu RevMicrobiol 2000;54:735-74.
22. Elliott SJ, Wainwright LA, McDaniel TK, et al. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 1998;28:1-4.
23. Parkhill J, Dougan G, James KD, et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovarTyphi CT18. Nature 2001;413:848-52.
24. Selbach M, Moese S, Hurwitz R, et al. The Helicobacter pylori CagA protein induces cortactin dephosphorylation and actin rearrangement by c-Src inactivation. EMBO J 2003;22:515-28.
25. Groisman EA, Ochman H. How Salmonella became a pathogen. TrendsMicrobiol 1997;5:343-9.
26. Bielecki J, Youngman P, Connelly P, et al. Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 1990;345:175-6.
27. Dobrindt U, Emody L, Gentschev I, et al. Efficient expression of the alpha-haemolysin determinant in the uropathogenic Escherichia coli strain 536 requires the leuX-encoded tRNA(5)(Leu). Mol Genet Genomics 2002;267:370-9.
28. Hacker J, Bender L, Ott M, et al. Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog 1990;8:213-25.
29. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
30. Vaandrager AB. Structure and function of the heat-stable enterotoxin receptor/guanylyl cyclase C. Mol Cell Biochem 2002;230:73-83.
31. Hacker J, Kaper JB. Pathogenicity islands and the evolution of microbes. AnnuRevMicrobiol 2000;54:641-79.
32. Frost LS, Leplae R, Summers AO, et al. Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 2005;3:722-32.
33. Hughes VM, Datta N. Conjugative plasmids in bacteria of the ̀pre-antibiotic' era. Nature 1983;302:725-6.
34. Poyart-Salmeron C, Carlier C, Trieu-Cuot P, et al. Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes. Lancet 1990;335:1422-6.
35. Buchrieser C, Rusniok C, Frangeul L, et al. The 102-kilobase pgm locus of Yersinia pestis: sequence analysis and comparison of selected regions among different Yersiniapestis and Yersinia pseudotuberculosis strains. Infect Immun 1999;67: 4851-61.
36. Oelschlaeger TA, Zhang D, Schubert S, et al. The highpathogenicity island is absent in human pathogens of Salmonella enterica subspecies I but present in isolates of subspecies III and VI. J Bacteriol 2003;185:1107-11.
37. Bechah Y, Capo C, Mege JL, et al. Epidemic typhus. Lancet Infect Dis 2008;8:417-26.
38. Raoult D, Roux V. Rickettsioses as paradigms of new or emerging infectious diseases. Clin Microbiol Rev 1997;10: 694-719.
39. Rovery C, Raoult D. Mediterranean spotted fever. Infect Dis ClinNorth Am 2008;22:515-30, ix.
40. Josenhans C, Suerbaum S. The role of motility as a virulence factor in bacteria. Int J Med Microbiol 2002;291: 605-14.
41. Frischknecht F, Way M. Surfing pathogens and the lessons learned for actin polymerization. Trends Cell Biol 2001;11:30-8.
42. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003;112:453-65.
43. Teysseire N, Chiche-Portiche C, Raoult D. Intracellular movements of Rickettsia conorii and Rickettsia typhi based on actin polymerization. ResMicrobiol 1992;143:821-9.
44. Gouin E, Egile C, Dehoux P, et al. The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature 2004; 427:457-61.
45. Kleba B, Clark TR, Lutter EI, et al. Disruption of the Rickettsia rickettsii Sca2 autotransporter inhibits actin-based motility. Infect Immun 2010;78:2240-7.
46. Balraj P, Nappez C, Raoult D, et al. Western-blot detection of RickA within spotted fever group rickettsiae using a specific monoclonal antibody. FEMS Microbiol Lett 2008; 286:257-62.
47. Ammerman NC, Gillespie JJ, Neuwald AF, et al. A typhus group-specific protease defies reductive evolution in rickettsiae. J Bacteriol 2009;191:7609-13.
48. Andersson SG, Kurland CG. Reductive evolution of resident genomes. Trends Microbiol 1998;6:263-8.
49. Blanc G, Ogata H, Robert C, et al. Reductive genome evolution from the mother of Rickettsia. PLoS Genet 2007; 3:e14.
50. Renvoise A, Merhej V, Georgiades K, et al. Intracellular Rickettsiales: insights into manipulators of eukaryotic cells. Trends Mol Med 2011;17:573-83.
51. Bechah Y, El Karkouri K, Mediannikov O, et al. Genomic, proteomic, and transcriptomic analysis of virulent and avirulent Rickettsia prowazekii reveals its adaptive mutation capabilities. GenomeRes 2010;20:655-63.
52. Moran NA. Microbial minimalism: genome reduction in bacterial pathogens. Cell 2002;108:583-6.
53. Rovery C, Renesto P, Crapoulet N, et al. Transcriptional response of Rickettsia conorii exposed to temperature variation and stress starvation. ResMicrobiol 2005;156:211-8.
54. Fournier PE, El Karkouri K, Leroy Q, et al. Analysis of the Rickettsia africae genome reveals that virulence acquisition in Rickettsia species may be explained by genome reduction. BMCGenomics 2009;10:166.
55. Cole ST, Brosch R, Parkhill J, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998;393:537-44.
56. Demangel C, Stinear TP, Cole ST. Buruli ulcer: reductive evolution enhances pathogenicity of Mycobacterium ulcerans. Nat RevMicrobiol 2009;7:50-60.
57. Stinear TP, Seemann T, Pidot S, et al. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 2007;17:192-200.
58. Abdallah AM, Gey van Pittius NC, Champion PA, et al. Type VII secretion-mycobacteria show the way. Nat Rev Microbiol 2007;5:883-91.
59. Brodin P, Rosenkrands I, Andersen P, et al. ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol 2004;12:500-8.
60. Shimono N, Morici L, Casali N, et al. Hypervirulent mutant of Mycobacterium tuberculosis resulting from disruption of the mce1 operon. Proc Natl Acad Sci U S A 2003;100:15918-23.
61. Jin Q, Yuan Z, Xu J, et al. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. NucleicAcids Res 2002;30:4432-41.
62. Pupo GM, Lan R, Reeves PR. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. ProcNatl Acad Sci USA 2000;97:10567-72.
63. Hale TL. Genetic basis of virulence in Shigella species. Microbiol Rev 1991;55:206-24.
64. Maurelli AT, Fernandez RE, Bloch CA, et al. ̀̀Black holes'' and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci U S A 1998;95: 3943-8.
65. Silva RM, Toledo MR, Trabulsi LR. Biochemical and cultural characteristics of invasive Escherichia coli. JClinMicrobiol 1980;11:441-4.
66. Bliven KA, Maurelli AT. Antivirulence genes: insights into pathogen evolution through gene loss. Infect Immun 2012; 80:4061-70.
67. Maurelli AT. Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMSMicrobiol Lett 2007;267:1-8.
68. Sokurenko EV, Hasty DL, Dykhuizen DE. Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol 1999;7:191-5.
69. Raoult D, Mouffok N, Bitam I, et al. Plague: history and contemporary analysis. J. Infect 2013;66:18-26.
70. Titball RW, Hill J, Lawton DG, et al. Yersinia pestis and plague. Biochem SocTrans 2003;31:104-7.
71. Achtman M, Zurth K, Morelli G, et al. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 1999;96: 14043-8.
72. Deng W, Burland V, Plunkett G, et al. Genome sequence of Yersinia pestis KIM. J Bacteriol 2002;184:4601-11.
73. Parkhill J, Wren BW, Thomson NR, et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 2001;413:523-7.
74. Gehring AM, DeMoll E, Fetherston JD, et al. Iron acquisition in plague: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis. Chem Biol 1998;5: 573-86.
75. Perry RD, Straley SC, Fetherston JD, et al. DNA sequencing and analysis of the low-Ca2P-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun 1998;66:4611-23.
76. Brubaker RR. Factors promoting acute and chronic diseases caused by Yersiniae. Clin Microbiol Rev 1991;4: 309-24.
77. Zhou D, Yang R. Molecular Darwinian evolution of virulence in Yersinia pestis. Infect Immun 2009;77:2242-50.
78. Tong Z, Zhou D, Song Y, et al. Pseudogene accumulation might promote the adaptive microevolution of Yersinia pestis. JMedMicrobiol 2005;54:259-68.
79. Erickson DL, Jarrett CO, Callison JA, et al. Loss of a biofilm- inhibiting glycosyl hydrolase during the emergence of Yersinia pestis. J Bacteriol 2008;190:8163-70.
80. Sun YC, Hinnebusch BJ, Darby C. Experimental evidence for negative selection in the evolution of a Yersinia pestis pseudogene. Proc Natl Acad Sci U S A 2008; 105:8097-101.
81. Montminy SW, Khan N, McGrath S, et al. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat Immunol 2006;7:1066-73.
82. Merhej V, Royer-Carenzi M, Pontarotti P, et al. Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct 2009;4:13.
83. Georgiades K, Raoult D. Comparative genomics evidence that only protein toxins are tagging bad bugs. FrontCell Infect Microbiol 2011;1:7.
84. Pappenheimer AM, Jr, Murphy JR. Studies on the molecular epidemiology of diphtheria. Lancet 1983;2:923-6.
85. Cook TM, Protheroe RT, Handel JM. Tetanus: a review of the literature. BrJAnaesth 2001;87:477-87.
86. Gill DM. Bacterial toxins: a table of lethal amounts. Microbiol Rev 1982;46:86-94.
87. Schiavo G, Matteoli M, Montecucco C. Neurotoxins affecting neuroexocytosis. Physiol Rev 2000;80:717-66.
88. Huttner WB. Cell biology. Snappy exocytoxins. Nature 1993;365:104-5.
89. Georgiades K, Raoult D. Genomes of the most dangerous epidemic bacteria have a virulence repertoire characterized by fewer genes but more toxin-antitoxin modules. PLoS One 2011;6:e17962.
90. Gerdes K, Rasmussen PB, Molin S. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. ProcNatlAcad SciUSA 1986;83:3116-20.
91. Gerdes K, Christensen SK, Lobner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat RevMicrobiol 2005; 3:371-82.
92. Goulard C, Langrand S, Carniel E, et al. The Yersinia pestis chromosome encodes active addiction toxins. J Bacteriol 2010;192:3669-77.
93. Gerdes K, Maisonneuve E. Bacterial persistence and toxin- antitoxin loci. Annu RevMicrobiol 2012;66:103-23.
94. Audoly G, Vincentelli R, Edouard S, et al. Effect of rickettsial toxin VapC on its eukaryotic host. PLoS One 2011;6: e26528.
95. Scolovschi C, Audoly G, Raoult D. Connection of toxinantitoxin modules to inoculation eschar and arthropod vertical transmission in Rickettsiales. Comp Immunol Microbiol Infect Dis 2013;36:199-209.