Metabolism and fitness of urinary tract pathogens

Microbiology Spectrum

Volumn 3, Issue 3, 2015, Pages

  Alteri, Christopher J ^a   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON; IRON; VIRULENCE FACTOR;

ECONOMICS; ENERGY METABOLISM; ESCHERICHIA COLI INFECTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; URINARY TRACT; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

AMINO ACIDS; CARBON; ENERGY METABOLISM; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; INTESTINAL MUCOSA; IRON; URINARY TRACT; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI; VIRULENCE FACTORS;

EID: 84959038386     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MBP-0016-2015     Document Type: Article

References (83)

1. Foxman B, Barlow R, D'Arcy H, Gillespie B, Sobel JD. 2000. Urinary tract infection: self-reported incidence and associated costs. Ann Epidemiol 10:509-515.
2. Litwin MS, Saigal CS, Yano EM, Avila C, Geschwind SA, Hanley JM, Joyce GF, Madison R, Pace J, Polich SM, Wang M. 2005. Urologic diseases in America Project: analytical methods and principal findings. J Urol 173:933-937.
3. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat Rev Microbiol 2:123-140.
4. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguenec C, Lescat M, Mangenot S, Martinez-Jehanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Medigue C, Rocha EP, Denamur E. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5:e1000344. doi:10.1371/journal.ppat.1000344
5. Land M, Hauser L, Jun SR, Nookaew I, Leuze MR, Ahn TH, Karpinets T, Lund O, Kora G, Wassenaar T, Poudel S, Ussery DW. 2015. Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics 15:141-161.
6. Croxen MA, Finlay BB. 2010. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8:26-38.
7. Johnson JR, Kuskowski MA, Gajewski A, Soto S, Horcajada JP, Jimenez de Anta MT, Vila J. 2005. Extended virulence genotypes and phylogenetic background of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J Infect Dis 191:46-50.
8. Johnson JR, Russo TA. 2005. Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli. Int J Med Microbiol 295:383-404.
9. Russo TA, Johnson JR. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 5:449-456.
10. Chen SL, Hung CS, Pinkner JS, Walker JN, Cusumano CK, Li Z, Bouckaert J, Gordon JI, Hultgren SJ. 2009. Positive selection identifies an in vivo role for FimH during urinary tract infection in addition to mannose binding. Proc Natl Acad Sci U S A 106:22439-22444.
11. Hommais F, Gouriou S, Amorin C, Bui H, Rahimy MC, Picard B, Denamur E. 2003. The FimH A27V mutation is pathoadaptive for urovirulence in Escherichia coli B2 phylogenetic group isolates. Infect Immun 71:3619-3622.
12. Johnson JR, Russo TA. 2002. Extraintestinal pathogenic Escherichia coli: "the other bad E. coli". J Lab Clin Med 139:155-162.
13. Alteri CJ, Mobley HL. 2012. Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15:3-9.
14. Hacker J, Blum-Oehler G, Mühldorfer I, Tschäpe H. 1997. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23:1089-1097.
15. Lloyd AL, Rasko DA, Mobley HL. 2007. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189:3532-3546.
16. Le Gall T, Clermont O, Gouriou S, Picard B, Nassif X, Denamur E, Tenaillon O. 2007. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol Biol Evol 24:2373-2384.
17. Diard M, Garry L, Selva M, Mosser T, Denamur E, Matic I. 2010. Pathogenicity-associated islands in extraintestinal pathogenic Escherichia coli are fitness elements involved in intestinal colonization. J Bacteriol 192:4885-4893.
18. Alteri CJ, Smith SN, Mobley HL. 2009. Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5:e1000448. doi:10.1371/journal.ppat.1000448
19. Moller AK, Leatham MP, Conway T, Nuijten PJ, de Haan LA, Krogfelt KA, Cohen PS. 2003. An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infect Immun 71:2142-2152.
20. Meador JP, Caldwell ME, Cohen PS, Conway T. 2014. Escherichia coli pathotypes occupy distinct niches in the mouse intestine. Infect Immun 82:1931-1938.
21. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, Stevenson SJ, Anderson AB, Grissom JE, Laux DC, Cohen PS, Conway T. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101:7427-7432.
22. Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue JW, Hightower GA, Smith JT, Autieri SM, Leatham MP, Lins JJ, Allen RL, Laux DC, Cohen PS, Conway T. 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76:1143-1152.
23. Martens EC, Roth R, Heuser JE, Gordon JI. 2009. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284:18445-18457.
24. Peekhaus N, Conway T. 1998. What's for dinner?: Entner-Doudoroffmetabolism in Escherichia coli. J Bacteriol 180:3495-3502.
25. Bonafonte MA, Solano C, Sesma B, Alvarez M, Montuenga L, Garcia-Ros D, Gamazo C. 2000. The relationship between glycogen synthesis, biofilm formation and virulence in Salmonella enteritidis. FEMS Microbiol Lett 191:31-36.
26. Jones SA, Jorgensen M, Chowdhury FZ, Rodgers R, Hartline J, Leatham MP, Struve C, Krogfelt KA, Cohen PS, Conway T. 2008. Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine. Infect Immun 76:2531-2540.
27. Miranda RL, Conway T, Leatham MP, Chang DE, Norris WE, Allen JH, Stevenson SJ, Laux DC, Cohen PS. 2004. Glycolytic and gluconeogenic growth of Escherichia coli O157:H7 (EDL933) and E. coli K-12 (MG1655) in the mouse intestine. Infect Immun 72:1666-1676.
28. Nowrouzian FL, Wold AE, Adlerberth I. 2005. Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 191:1078-1083.
29. Nowrouzian FL, Adlerberth I, Wold AE. 2006. Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells. Microbes Infect 8:834-840.
30. Schouler C, Taki A, Chouikha I, Moulin-Schouleur M, Gilot P. 2009. A genomic island of an extraintestinal pathogenic Escherichia coli strain enables the metabolism of fructooligosaccharides, which improves intestinal colonization. J Bacteriol 191:388-393.
31. Porcheron G, Kut E, Canepa S, Maurel MC, Schouler C. 2011. Regulation of fructooligosaccharide metabolism in an extra-intestinal pathogenic Escherichia coli strain. Mol Microbiol 81:717-733.
32. Rouquet G, Porcheron G, Barra C, Répérant M, Chanteloup NK, Schouler C, Gilot P. 2009. A metabolic operon in extraintestinal pathogenic Escherichia coli promotes fitness under stressful conditions and invasion of eukaryotic cells. J Bacteriol 191:4427-4440.
33. Hagberg L, Engberg I, Freter R, Lam J, Olling S, Svanborg Edén C. 1983. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect Immun 40:273-283.
34. Alteri CJ, Mobley HL. 2007. Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect Immun 75:2679-2688.
35. Asscher AW, Sussman M, Waters WE, Davis RH, Chick S. 1966. Urine as a medium for bacterial growth. Lancet 2:1037-1041.
36. Russo TA, Jodush ST, Brown JJ, Johnson JR. 1996. Identification of two previously unrecognized genes (guaA and argC) important for uropathogenesis. Mol Microbiol 22:217-229.
37. Brooks T, Keevil CW. 1997. A simple artificial urine for the growth of urinary pathogens. Lett Appl Microbiol 24:203-206.
38. Aubron C, Glodt J, Matar C, Huet O, Borderie D, Dobrindt U, Duranteau J, Denamur E, Conti M, Bouvet O. 2012. Variation in endogenous oxidative stress in Escherichia coli natural isolates during growth in urine. BMC Microbiol 12:120.
39. Snyder JA, Haugen BJ, Buckles EL, Lockatell CV, Johnson DE, Donnenberg MS, Welch RA, Mobley HL. 2004. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72:6373-6381.
40. Hancock V, Vejborg RM, Klemm P. 2010. Functional genomics of probiotic Escherichia coli Nissle 1917 and 83972, and UPEC strain CFT073: comparison of transcriptomes, growth and biofilm formation. Mol Genet Genomics 284:437-454.
41. Vejborg RM, de Evgrafov MR, Phan MD, Totsika M, Schembri MA, Hancock V. 2012. Identification of genes important for growth of asymptomatic bacteriuria Escherichia coli in urine. Infect Immun 80:3179-3188.
42. Alteri CJ, Hagan EC, Sivick KE, Smith SN, MobleyHL. 2009. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog 5:e1000586. doi:10.1371/journal.ppat.1000586
43. Alteri CJ, Himpsl SD, Mobley HL. 2015. Preferential use of central metabolism in vivo reveals a nutritional basis for polymicrobial infection. PLoS Pathog 11:e1004601. doi:10.1371/journal.ppat.1004601
44. Roesch PL, Redford P, Batchelet S, Moritz RL, Pellett S, Haugen BJ, Blattner FR, Welch RA. 2003. Uropathogenic Escherichia coli use d-serine deaminase to modulate infection of the murine urinary tract. Mol Microbiol 49:55-67.
45. Bahrani-Mougeot FK, Buckles EL, Lockatell CV, Hebel JR, Johnson DE, Tang CM, Donnenberg MS. 2002. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol Microbiol 45:1079-1093.
46. Hagan EC, Lloyd AL, Rasko DA, Faerber GJ, Mobley HL. 2010. Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 6:e1001187. doi:10.1371/journal.ppat.1001187
47. Bielecki P, Muthukumarasamy U, Eckweiler D, Bielecka A, Pohl S, Schanz A, Niemeyer U, Oumeraci T, von NeuhoffN, Ghigo JM, Häussler S. 2014. In vivo mRNA profiling of uropathogenic Escherichia coli from diverse phylogroups reveals common and group-specific gene expression profiles. MBio 5:e01075-01014. doi:10.1128/mBio.01075-14
48. Subashchandrabose S, Hazen TH, Brumbaugh AR, Himpsl SD, Smith SN, Ernst RD, Rasko DA, Mobley HL. 2014. Host-specific induction of Escherichia coli fitness genes during human urinary tract infection. Proc Natl Acad Sci U S A 111:18327-18332.
49. Wandersman C, Delepelaire P. 2004. Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611-647.
50. Kammler M, Schön C, Hantke K. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175:6212-6219.
51. Torres AG, Redford P, Welch RA, Payne SM. 2001. TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 69:6179-6185.
52. Welch RA, Burland V, Plunkett G III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020-17024.
53. Hagan EC, Mobley HL. 2009. Haem acquisition is facilitated by a novel receptor Hma and required by uropathogenic Escherichia coli for kidney infection. Mol Microbiol 71:79-91.
54. Johnson JR, Jelacic S, Schoening LM, Clabots C, Shaikh N, Mobley HL, Tarr PI. 2005. The IrgA homologue adhesin Iha is an Escherichia coli virulence factor in murine urinary tract infection. Infect Immun 73:965-971.
55. Russo TA, Carlino UB, Johnson JR. 2001. Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coli. Infect Immun 69:6209-6216.
56. Russo TA, McFadden CD, Carlino-MacDonald UB, Beanan JM, Barnard TJ, Johnson JR. 2002. IroN functions as a siderophore receptor and is a urovirulence factor in an extraintestinal pathogenic isolate of Escherichia coli. Infect Immun 70:7156-7160.
57. Watts RE, Totsika M, Challinor VL, Mabbett AN, Ulett GC, De Voss JJ, Schembri MA. 2012. Contribution of siderophore systems to growth and urinary tract colonization of asymptomatic bacteriuria Escherichia coli. Infect Immun 80:333-344.
58. Carbonetti NH, Boonchai S, Parry SH, Väisänen-Rhen V, Korhonen TK, Williams PH. 1986. Aerobactin-mediated iron uptake by Escherichia coli isolates from human extraintestinal infections. Infect Immun 51:966-968.
59. Johnson JR, Moseley SL, Roberts PL, Stamm WE. 1988. Aerobactin and other virulence factor genes among strains of Escherichia coli causing urosepsis: association with patient characteristics. Infect Immun 56:405-412.
60. Vigil PD, Stapleton AE, Johnson JR, Hooton TM, Hodges AP, He Y, Mobley HL. 2011. Presence of putative repeat-in-toxin gene tosA in Escherichia coli predicts successful colonization of the urinary tract. MBio 2:e00066-00011. doi:10.1128/mBio.00066-11
61. Henderson JP, Crowley JR, Pinkner JS, Walker JN, Tsukayama P, Stamm WE, Hooton TM, Hultgren SJ. 2009. Quantitative metabolomics reveals an epigenetic blueprint for iron acquisition in uropathogenic Escherichia coli. PLoS Pathog 5:e1000305. doi:10.1371/journal.ppat.1000305
62. Melican K, Sandoval RM, Kader A, Josefsson L, Tanner GA, Molitoris BA, Richter-Dahlfors A. 2011. Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog 7:e1001298. doi:10.1371/journal.ppat.1001298
63. Anfora AT, Halladin DK, Haugen BJ, Welch RA. 2008. Uropathogenic Escherichia coli CFT073 is adapted to acetatogenic growth but does not require acetate during murine urinary tract infection. Infect Immun 76: 5760-5767.
64. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D, Voigt B, Grönberg-Hernandez J, Ragnarsdottir B, Hecker M, Ron EZ, Daniel R, Gottschalk G, Hacker J, Svanborg C, Dobrindt U. 2010. Host imprints on bacterial genomes-rapid, divergent evolution in individual patients. PLoS Pathog 6:e1001078. doi:10.1371/journal.ppat.1001078
65. Hadjifrangiskou M, Kostakioti M, Chen SL, Henderson JP, Greene SE, Hultgren SJ. 2011. A central metabolic circuit controlled by QseC in pathogenic Escherichia coli. Mol Microbiol 80:1516-1529.
66. Park SJ, Gunsalus RP. 1995. Oxygen, iron, carbon, and superoxide control of the fumarase fumA and fumC genes of Escherichia coli: role of the arcA, fnr, and soxR gene products. J Bacteriol 177:6255-6262.
67. Unden G, Bongaerts J. 1997. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217-234.
68. Jones SA, Chowdhury FZ, Fabich AJ, Anderson A, Schreiner DM, House AL, Autieri SM, Leatham MP, Lins JJ, Jorgensen M, Cohen PS, Conway T. 2007. Respiration of Escherichia coli in the mouse intestine. Infect Immun 75:4891-4899.
69. Shepherd M, Sanguinetti G, Cook GM, Poole RK. 2010. Compensations for diminished terminal oxidase activity in Escherichia coli: cytochrome bd-II-mediated respiration and glutamate metabolism. J Biol Chem 285:18464-18472.
70. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE. 2011. Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333:345-348.
71. Allison KR, Brynildsen MP, Collins JJ. 2011. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473:216-220.
72. Bergsten G, Samuelsson M, Wullt B, Leijonhufvud I, Fischer H, Svanborg C. 2004. PapG-dependent adherence breaks mucosal inertia and triggers the innate host response. J Infect Dis 189:1734-1742.
73. Godaly G, Bergsten G, Hang L, Fischer H, Frendéus B, Lundstedt AC, Samuelsson M, Samuelsson P, Svanborg C. 2001. Neutrophil recruitment, chemokine receptors, and resistance to mucosal infection. J Leukoc Biol 69:899-906.
74. Chromek M, Slamová Z, Bergman P, Kovács L, Podracká L, Ehrén I, Hökfelt T, Gudmundsson GH, Gallo RL, Agerberth B, Brauner A. 2006. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12:636-641.
75. Alteri CJ, Lindner JR, Reiss DJ, Smith SN, Mobley HL. 2011. The broadly conserved regulator PhoP links pathogen virulence and membrane potential in Escherichia coli. Mol Microbiol 82:145-163.
76. Anfora AT, Haugen BJ, Roesch P, Redford P, Welch RA. 2007. Roles of serine accumulation and catabolism in the colonization of the murine urinary tract by Escherichia coli CFT073. Infect Immun 75:5298-5304.
77. Haugen BJ, Pellett S, Redford P, Hamilton HL, Roesch PL, Welch RA. 2007. In vivo gene expression analysis identifies genes required for enhanced colonization of the mouse urinary tract by uropathogenic Escherichia coli strain CFT073 dsdA. Infect Immun 75:278-289.
78. Cai W, Wannemuehler Y, Dell'anna G, Nicholson B, Barbieri NL, Kariyawasam S, Feng Y, Logue CM, Nolan LK, Li G. 2013. A novel twocomponent signaling system facilitates uropathogenic Escherichia coli's ability to exploit abundant host metabolites. PLoS Pathog 9:e1003428. doi:10.1371/journal.ppat.1003428
79. Barbieri NL, Nicholson B, Hussein A, Cai W, Wannemuehler YM, Dell'Anna G, Logue CM, Horn F, Nolan LK, Li G. 2014. FNR regulates expression of important virulence factors contributing to pathogenicity of uropathogenic Escherichia coli. Infect Immun 82:5086-5098.
80. Sohanpal BK, El-Labany S, Lahooti M, Plumbridge JA, Blomfield IC. 2004. Integrated regulatory responses of fimB to N-acetylneuraminic (sialic) acid and GlcNAc in Escherichia coli K-12. Proc Natl Acad Sci U S A 101:16322-16327.
81. Bernier SP, Létoffé S, Delepierre M, Ghigo JM. 2011. Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol Microbiol 81:705-716.
82. Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, Palm F, Mounier J, Prévost MC, Sansonetti P, Tang CM. 2010. Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465: 355-358.
83. Spurbeck RR, Stapleton AE, Johnson JR, Walk ST, Hooton TM, Mobley HL. 2011. Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of ygi and yad fimbriae. Infect Immun 79:4753-4763.