Initiation of swarming motility by Proteus mirabilis occurs in response to specific cues present in urine and requires excess L-glutamine

Journal of Bacteriology

Volumn 195, Issue 6, 2013, Pages 1305-1319

  Armbruster, Chelsie E ^a   Hodges, Steven A ^a   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLUTAMINE; HISTIDINE; MALIC ACID; ORNITHINE; PUTRESCINE;

AGAR MEDIUM; AMINO ACID METABOLISM; ARTICLE; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM CULTURE; BACTERIUM ISOLATE; BACTERIUM MUTANT; BIOSYNTHESIS; CATHETER INFECTION; GROWTH RATE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEUS MIRABILIS; SWARMING MOTILITY; URINARY TRACT INFECTION; URINE CULTURE;

CATHETER-RELATED INFECTIONS; FEMALE; GLUTAMINE; HUMANS; MOVEMENT; PROTEUS INFECTIONS; PROTEUS MIRABILIS; PUTRESCINE; SIGNAL TRANSDUCTION; UREA; URINARY CATHETERIZATION; URINARY TRACT INFECTIONS; URINE;

EID: 84874691750     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02136-12     Document Type: Article

References (54)

1. Klevens RM, Edwards JR, Richards CL, Jr, Horan TC, Gaynes RP, Pollock DA, Cardo DM. 2007. Estimating health care-associated infections and deaths in US hospitals, 2002. Public Health Rep. 122:160-166.
2. Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, Saint S, Schaeffer AJ, Tambayh PA, Tenke P, Nicolle LE. 2010. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 international clinical practice guidelines from the Infectious Diseases Society of America. Clin. Infect. Dis. 50:625-663.
3. Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME. 2008. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin. Microbiol. Rev. 21:26-59.
4. Mathur S, Sabbuba NA, Suller MT, Stickler DJ, Feneley RC. 2005. Genotyping of urinary and fecal Proteus mirabilis isolates from individuals with long-term urinary catheters. Eur. J. Clin. Microbiol. Infect. Dis. 24: 643-644.
5. Warren JW, Tenney JH, Hoopes JM, Muncie HL, Anthony WC. 1982. A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J. Infect. Dis. 146:719-723.
6. Nicolle LE. 2005. Catheter-related urinary tract infection. Drugs Aging 22:627-639.
7. Mobley HLT, Warren JW. 1987. Urease-positive bacteriuria and obstruction of long-term urinary catheters. J. Clin. Microbiol. 25:2216-2217.
8. Griffith DP, Musher DM, Itin C. 1976. Urease. The primary cause of infection-induced urinary stones. Invest. Urol. 13:346-350.
9. Li X, Zhao H, Lockatell CV, Drachenberg CB, Johnson DE, Mobley HLT. 2002. Visualization of Proteus mirabilis within the matrix of ureaseinduced bladder stones during experimental urinary tract infection. Infect. Immun. 70:389-394.
10. Hoeniger JFM. 1965. Development of flagella by Proteus mirabilis. J. Gen. Microbiol. 40:29-42.
11. Williams FD, Schwarzhoff RH. 1978. Nature of the swarming phenomenon in Proteus. Annu. Rev. Microbiol. 32:101-122.
12. Allison C, Hughes C. 1991. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci. Prog. 75:403-422.
13. Jones BV, Young R, Mahenthiralingam E, Stickler DJ. 2004. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect. Immun. 72:3941-3950.
14. Sabbuba N, Hughes G, Stickler DJ. 2002. The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int. 89:55-60.
15. Armbruster CE, Mobley HLT. 2012. Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat. Rev. Microbiol. 10:743-754.
16. Morgenstein RM, Szostek B, Rather PN. 2010. Regulation of gene expression during swarmer cell differentiation in Proteus mirabilis. FEMS Microbiol. Rev. 34:753-763.
17. Rather PN. 2005. Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol. 7:1065-1073.
18. Belas R, Suvanasuthi R. 2005. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J. Bacteriol. 187:6789-6803.
19. Cusick K, Lee YY, Youchak B, Belas R. 2012. Perturbation of FliL interferes with Proteus mirabilis swarmer cell gene expression and differentiation. J. Bacteriol. 194:437-447.
20. Morgenstein RM, Clemmer KM, Rather PN. 2010. Loss of the waaL O-antigen ligase prevents surface activation of the flagellar gene cascade in Proteus mirabilis. J. Bacteriol. 192:3213-3221.
21. Morgenstein RM, Rather PN. 2012. Role of the Umo proteins and the Rcs phosphorelay in the swarming motility of the wild type and an O-antigen (waaL) mutant of Proteus mirabilis. J. Bacteriol. 194:669-676.
22. Hatt JK, Rather PN. 2008. Characterization of a novel gene, wosA, regulating FlhDC expression in Proteus mirabilis. J. Bacteriol. 190:1946-1955.
23. Sturgill G, Rather PN. 2004. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol. Microbiol. 51:437-446.
24. Liaw S-J, Lai H-C, Wang W-B. 2004. Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect. Immun. 72:6836-6845.
25. Himpsl SD, Lockatell CV, Hebel JR, Johnson DE, Mobley HLT. 2008. Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J. Med. Microbiol. 57:1068-1078.
26. Falkinham JO, III, Hoffman PS. 1984. Unique developmental characteristics of the swarm and short cells of Proteus vulgaris and Proteus mirabilis. J. Bacteriol. 158:1037-1040.
27. Alteri CJ, Himpsl SD, Engstrom MD, Mobley HL. 2012. Anaerobic respiration using a complete oxidative TCA cycle drives multicellular swarming in Proteus mirabilis. mBio 3(6):e00365-12. doi:10.1128/mBio.00365-12.
28. Rauprich O, Matsushita M, Weijer CJ, Siegert F, Esipov SE, Shapiro JA. 1996. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178:6525-6538.
29. Jones HE, Park RW. 1967. The influence of medium composition on the growth and swarming of Proteus. J. Gen. Microbiol. 47:369-378.
30. Wilkerson ML, Niederhoffer EC. 1995. Swarming characteristics of Proteus mirabilis under anaerobic and aerobic conditions. Anaerobe 1:345-350.
31. Naylor PGD. 1964. Effect of electrolytes or carbohydrates in sodium chloride deficient medium on formation of discrete colonies of Proteus and the influence of these substances on growth in liquid culture. J. Appl. Bacteriol. 27:422-431.
32. Allison C, Lai HC, Gygi D, Hughes C. 1993. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol. 8:53-60.
33. Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, Luscombe NM, Abdellah Z, Arrosmith C, Atkin B, Chillingworth T, Hauser H, Jagels K, Moule S, Mungall K, Norbertczak H, Rabbinowitsch E, Walker D, Whithead S, Thomson NR, Rather PN, Parkhill J, Mobley HLT. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol. 190:4027-4037.
34. Vinogradov E, Perry MB. 2000. Structural analysis of the core region of lipopolysaccharides from Proteus mirabilis serotypes O6, O48 and O57. Eur. J. Biochem. 267:2439-2446.
35. Belas R, Erskine D, Flaherty D. 1991. Transposon mutagenesis in Proteus mirabilis. J. Bacteriol. 173:6289-6293.
36. Pearson MM, Mobley HLT. 2007. The type III secretion system of Proteus mirabilis HI4320 does not contribute to virulence in the mouse model of ascending urinary tract infection. J. Med. Microbiol. 56:1277-1283.
37. Kugler F, Graneis S, Schreiter PP, Stintzing FC, Carle R. 2006. Determination of free amino compounds in betalainic fruits and vegetables by gas chromatography with flame ionization and mass spectrometric detection. J. Agric. Food Chem. 54:4311-4318.
38. Lorenz MA, Burant CF, Kennedy RT. 2011. Reducing time and increasing sensitivity in sample preparation for adherent mammalian cell metabolomics. Anal. Chem. 83:3406-3414.
39. Norden AG, Sharratt P, Cutillas PR, Cramer R, Gardner SC, Unwin RJ. 2004. Quantitative amino acid and proteomic analysis: very low excretion of polypeptides _750 Da in normal urine. Kidney Int. 66:1994-2003.
40. Zaura DS, Metcoff J. 1969. Quantification of seven tricarboxylic acid cycle and related acids in human urine by gas-liquid chromatography. Anal. Chem. 41:1781-1787.
41. Markowski P, Baranowska I, Baranowski J. 2007. Simultaneous determination of L-arginine and 12 molecules participating in its metabolic cycle by gradient RP-HPLC method: application to human urine samples. Anal. Chim. Acta 605:205-217.
42. Fujihara M, Obara H, Watanabe Y, Ono HK, Sasaki J, Goryo M, Harasawa R. 2011. Acidic environments induce differentiation of Proteus mirabilis into swarmer morphotypes. Microbiol. Immunol. 55:489-493.
43. Sezonov G, Joseleau-Petit D, D'Ari R. 2007. Escherichia coli physiology in Luria-Bertani broth. J. Bacteriol. 189:8746-8749.
44. Hauser G. 1885. Ü ber Fäulnissbacterien und deren Beziehungen zur Septicämie; ein Beitrag zur Morphologie der Spaltpilze. Vogel, Leipzig, Germany.
45. Schneider R, Lockatell CV, Johnson D, Belas R. 2002. Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148:773-782.
46. Belas R, Schneider R, Melch M. 1998. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J. Bacteriol. 180:6126-6139.
47. Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S, Givskov M. 1996. Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20:127-136.
48. Kohler T, Curty LK, Barja F, van Delden C, Pechere JC. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996.
49. Bernier SP, Ha DG, Khan W, Merritt JH, O'Toole GA. 2011. Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Res. Microbiol. 162: 680-688.
50. Calvo JM, Matthews RG. 1994. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58:466-490.
51. Hay NA, Tipper DJ, Gygi D, Hughes C. 1997. A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J. Bacteriol. 179:4741-4746.
52. Hart BR, Blumenthal RM. 2011. Unexpected coregulator range for the global regulator Lrp of Escherichia coli and Proteus mirabilis. J. Bacteriol. 193:1054-1064.
53. Pearson MM, Yep A, Smith SN, Mobley HLT. 2011. Transcriptome of Proteus mirabilis in the murine urinary tract: virulence and nitrogen assimilation gene expression. Infect. Immun. 79:2619-2631.
54. Jones BD, Lockatell CV, Johnson DE, Warren JW, Mobley HL. 1990. Construction of a urease-negative mutant of Proteus mirabilis: analysis of virulence in a mouse model of ascending urinary tract infection. Infect. Immun. 58:1120-1123.