Reduced set of virulence genes allows high accuracy prediction of bacterial pathogenicity in humans

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Iraola, Gregorio ^a,b   Vazquez, Gustavo ^c   Spangenberg, Lucía ^a   Naya, Hugo ^a,b  

^a INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CLASSIFICATION; COMPUTER PROGRAM; EXTERNAL VALIDITY; PHENOTYPE; PREDICTION; PROBABILITY; STATISTICAL MODEL; TAXONOMY;

BACTERIA; GENES, BACTERIAL; HUMANS; VIRULENCE;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); FIRMICUTES; GAMMAPROTEOBACTERIA;

EID: 84864710511     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042144     Document Type: Article

References (81)

1. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, et al. ((1995)) Whole-genome random sequencing and assembly of Haemophilus inuenzae Rd. Science 269:496-512.
2. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, et al. ((1995)) The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
3. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, et al. ((1997)) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
4. Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, et al. ((2001)) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
5. Perna NT, Plunkett G, Burland V, Mau B, Glasner JD, et al. ((2001)) Genome sequence of entero-haemorrhagic Escherichia coli O157:H7. Nature 409:529-533.
6. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. ((2005)) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
7. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. ((2008)) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:53-59.
8. Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, et al. ((1998)) Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci USA 95:8922-8926.
9. Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P, ((2007)) A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 inuenza A viruses contributes to increased virulence. PLoS Pathog 3:1414-1421.
10. Marjuki H, Scholtissek C, Franks J, Negovetich NJ, Aldridge JR, et al. ((2010)) Three amino acid changes in PB1-F2 of highly pathogenic H5N1 avian inuenza virus affect pathogenicity in mallard ducks. Arch Virol 155:925-934.
11. Spangenberg L, Battke F, Grana M, Nieselt K, Naya H, ((2011)) Identifying associations between amino acid changes and meta information in alignments. Bioinformatics 27:2782-2789.
12. Oswald E, Nougayrede JP, Taieb F, Sugai M, ((2005)) Bacterial toxins that modulate host cell-cycle progression. Curr Opin Microbiol 8:83-91.
13. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, et al. ((2007)) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189:38-51.
14. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K, ((2008)) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190:300-310.
15. Ho Sui SJ, Fedynak A, Hsiao WW, Langille MG, Brinkman FS, ((2009)) The association of virulence factors with genomic islands. PLoS ONE 4:e8094.
16. Andreatta M, Nielsen M, Moller Aarestrup F, Lund O, ((2010)) In silico prediction of human pathogenicity in the-proteobacteria. PLoS ONE 5:e13680.
17. Rees DC, Johnson E, Lewinson O, ((2009)) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218-227.
18. Rohmer L, Hocquet D, Miller SI, ((2011)) Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19:341-348.
19. West SA, Buckling A, ((2003)) Cooperation, virulence and siderophore production in bacterial parasites. Proc Biol Sci 270:37-44.
20. Moran NA, ((2002)) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
21. Stock AM, Robinson VL, Goudreau PN, ((2000)) Two-component signal transduction. Annu Rev Biochem 69:183-215.
22. Shikuma NJ, Yildiz FH, ((2009)) Identification and characterization of OscR, a transcriptional regulator involved in osmolarity adaptation in Vibrio cholerae. J Bacteriol 191:4082-4096.
23. Dubrac S, Boneca IG, Poupel O, Msadek T, ((2007)) New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189:8257-8269.
24. Senadheera MD, Guggenheim B, Spatafora GA, Huang YC, Choi J, et al. ((2005)) A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187:4064-4076.
25. Sperandio V, Torres AG, Kaper JB, ((2002)) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of agella and motility by quorum sensing in E. coli. Mol Microbiol 43:809-821.
26. Josenhans C, Suerbaum S, ((2002)) The role of motility as a virulence factor in bacteria. Int J Med Microbiol 291:605-614.
27. Kehl-Fie TE, Porsch EA, Miller SE, St Geme JW, ((2009)) Expression of Kingella kingae type IV pili is regulated by sigma54, PilS, and PilR. J Bacteriol 191:4976-4986.
28. Whitehouse CA, Balbo PB, Pesci EC, Cottle DL, Mirabito PM, et al. ((1998)) Campylobacter jejuni cytolethal distending toxin causes a G2-phase cell cycle block. Infect Immun 66:1934-1940.
29. Marches O, Ledger TN, Boury M, Ohara M, Tu X, et al. ((2003)) Enteropathogenic and enterohaem-orrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 50:1553-1567.
30. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R, ((2003)) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301:1099-1102.
31. Billington SJ, Jost BH, Songer JG, ((2000)) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol Lett 182:197-205.
32. Alouf JE, ((1980)) Streptococcal toxins (streptolysin O, streptolysin S, erythrogenic toxin). Pharmacol Ther 11:661-717.
33. Sinev MA, Budarina ZhI, Gavrilenko IV, Tomashevski AIu, Kuz'min NP, ((1993)) [Evidence of the existence of hemolysin II from Bacillus cereus: cloning the genetic determinant of hemolysin II]. Mol Biol (Mosk) 27:1218-1229.
34. Budarina ZI, Sinev MA, Mayorov SG, Tomashevski AY, Shmelev IV, et al. ((1994)) Hemolysin II is more characteristic of Bacillus thuringiensis than Bacillus cereus. Arch Microbiol 161:252-257.
35. Zhang XH, Austin B, ((2005)) Haemolysins in Vibrio species. J Appl Microbiol 98:1011-1019.
36. Ja_e AB, Hall A, ((2005)) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269.
37. Ridley AJ, ((2001)) Rho proteins: linking signaling with membrane trafficking. Traffic 2:303-310.
38. Yamamoto M, Sato S, Hemmi H, Uematsu S, Hoshino K, et al. ((2003)) TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 4:1144-1150.
39. Raetz CR, Guan Z, Ingram BO, Six DA, Song F, et al. ((2009)) Discovery of new biosynthetic pathways: the lipid A story. J Lipid Res 50 Suppl: S103-108.
40. Poon KK, Westman EL, Vinogradov E, Jin S, Lam JS, ((2008)) Functional characterization of MigA and WapR: putative rhamnosyltransferases involved in outer core oligosaccharide biosynthesis of Pseudomonas aeruginosa. J Bacteriol 190:1857-1865.
41. Murray GL, Attridge SR, Morona R, ((2006)) Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J Bacteriol 188:2735-2739.
42. Al-Dabbagh B, Mengin-Lecreulx D, Bouhss A, ((2008)) Purification and characterization of the bacterial UDP-GlcNAc:undecaprenyl-phosphate GlcNAc-1-phosphate transferase WecA. J Bacteriol 190:7141-7146.
43. Hibbing ME, Fuqua C, Parsek MR, Peterson SB, ((2010)) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15-25.
44. Yim L, Betancor L, Martinez A, Bryant C, Maskell D, et al. (2011) Naturally occurring motility-defective mutants of Salmonella enterica serovar Enteritidis isolated preferentially from non-human rather than human sources. Appl Environ Microbiol.
45. O'Toole GA, Kolter R, ((1998)) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295-304.
46. Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J, ((2006)) Motility inuences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72:361-367.
47. Starnbach MN, Lory S, ((1992)) The iA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for agellin synthesis. Mol Microbiol 6:459-469.
48. Tasteyre A, Barc MC, Collignon A, Boureau H, Karjalainen T, ((2001)) Role of FliC and FliD agellar proteins of Clostridium difficile in adherence and gut colonization. Infect Immun 69:7937-7940.
49. Schoenhals GJ, Macnab RM, ((1999)) FliL is a membrane-associated component of the agellar basal body of Salmonella. Microbiology (Reading, Engl) 145 (Pt 7):1769-1775.
50. Waters RC, O'Toole PW, Ryan KA, ((2007)) The FliK protein and agellar hook-length control. Protein Sci 16:769-780.
51. Titz B, Rajagopala SV, Ester C, Hauser R, Uetz P, ((2006)) Novel conserved assembly factor of the bacterial agellum. J Bacteriol 188:7700-7706.
52. Liu J, Lin T, Botkin DJ, McCrum E, Winkler H, et al. ((2009)) Intact agellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly exion. J Bacteriol 191:5026-5036.
53. Soto GE, Hultgren SJ, ((1999)) Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181:1059-1071.
54. Aprikian P, Interlandi G, Kidd BA, Le Trong I, Tchesnokova V, et al. ((2011)) The bacterial fimbrial tip acts as a mechanical force sensor. PLoS Biol 9:e1000617.
55. Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, et al. ((1995)) FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci USA 92:2081-2085.
56. Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, et al. ((2002)) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323:845-857.
57. Valenski ML, Harris SL, Spears PA, Horton JR, Orndorff PE, ((2003)) The Product of the fimI gene is necessary for Escherichia coli type 1 pilus biosynthesis. J Bacteriol 185:5007-5011.
58. Craig L, Li J, ((2008)) Type IV pili: paradoxes in form and function. Curr Opin Struct Biol 18:267-277.
59. Schulein R, Dehio C, ((2002)) The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol Microbiol 46:1053-1067.
60. Robinson C, Bolhuis A, ((2001)) Protein targeting by the twin-arginine translocation pathway. Nat Rev Mol Cell Biol 2:350-356.
61. Mori H, Ito K, ((2001)) The Sec protein-translocation pathway. Trends Microbiol 9:494-500.
62. Muller M, ((2005)) Twin-arginine-specific protein export in Escherichia coli. Res Microbiol 156:131-136.
63. Dilks K, Rose RW, Hartmann E, Pohlschroder M, ((2003)) Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol 185:1478-1483.
64. Cornelis GR, Van Gijsegem F, ((2000)) Assembly and function of type III secretory systems. Annu Rev Microbiol 54:735-774.
65. Sansonetti PJ, ((2001)) Microbes and microbial toxins: paradigms for microbial-mucosal interactions III. Shigellosis: from symptoms to molecular pathogenesis. Am J Physiol Gastrointest Liver Physiol 280:G319-323.
66. Celli J, Deng W, Finlay BB, ((2000)) Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell Microbiol 2:1-9.
67. Farizo KM, Huang T, Burns DL, ((2000)) Importance of holotoxin assembly in Ptl-mediated secretion of pertussis toxin from Bordetella pertussis. Infect Immun 68:4049-4054.
68. Zink SD, Pedersen L, Cianciotto NP, Abu-Kwaik Y, ((2002)) The Dot/Icm type IV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect Immun 70:1657-1663.
69. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, et al. ((2002)) Type IV secretion and Brucella virulence. Vet Microbiol 90:341-348.
70. Backert S, Churin Y, Meyer TF, ((2002)) Helicobacter pylori type IV secretion, host cell signaling and vaccine development. Keio J Med 51 Suppl 2: 6-14.
71. Schroder G, Dehio C, ((2005)) Virulence-associated type IV secretion systems of Bartonella. Trends Microbiol 13:336-342.
72. Bingle LE, Bailey CM, Pallen MJ, ((2008)) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11:3-8.
73. Potvin E, Lehoux DE, Kukavica-Ibrulj I, Richard KL, Sanschagrin F, et al. ((2003)) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5:1294-1308.
74. Persson OP, Pinhassi J, Riemann L, Marklund BI, Rhen M, et al. ((2009)) High abundance of virulence gene homologues in marine bacteria. Environ Microbiol 11:1348-1357.
75. Pallen MJ, Wren BW, ((2007)) Bacterial pathogenomics. Nature 449:835-842.
76. Gross R, Guzman CA, Sebaihia M, dos Santos VA, Pieper DH, et al. ((2008)) The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 9:449.
77. Fry NK, Duncan J, Malnick H, Warner M, Smith AJ, et al. ((2005)) Bordetella petrii clinical isolate. Emerging Infect Dis 11:1131-1133.
78. Stark D, Riley LA, Harkness J, Marriott D, ((2007)) Bordetella petrii from a clinical sample in Australia: isolation and molecular identification. J Med Microbiol 56:435-437.
79. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, ((1990)) Basic local alignment search tool. J Mol Biol 215:403-410.
80. Frank E, Hall M, Trigg L, Holmes G, Witten IH, ((2004)) Data mining in bioinformatics using Weka. Bioinformatics 20:2479-2481.
81. Dearden JC, Cronin MT, Kaiser KL, ((2009)) How not to develop a quantitative structure-activity or structure-property relationship (QSAR/QSPR). SAR QSAR Environ Res 20:241-266.