Transcriptome of swarming Proteus mirabilis

Infection and Immunity

Volumn 78, Issue 6, 2010, Pages 2834-2845

  Pearson, Melanie M ^a   Rasko, David A ^b   Smith, Sara N ^a   Mobley, Harry L T ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; ALPHA HEMOLYSIN; BACTERIAL PROTEIN; CHLORAMPHENICOL; COLD SHOCK PROTEIN; CYSJ PROTEIN; DPPA PROTEIN; FLAGELLIN; HEMOLYSIN; HEXA PROTEIN; LRHA PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; OPPB PROTEIN; OUTER MEMBRANE PROTEIN A; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SULFITE REDUCTASE (NADPH); TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIUM CULTURE; CELL DIVISION; CELL MOTILITY; COMPLEX I DEFICIENCY; DOWN REGULATION; GENE EXPRESSION; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEUS MIRABILIS; UPREGULATION; URINARY TRACT INFECTION;

ANIMALS; DOWN-REGULATION; FEMALE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LOCOMOTION; MICE; MICE, INBRED CBA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEUS INFECTIONS; PROTEUS MIRABILIS; UP-REGULATION; URINARY TRACT INFECTIONS; VIRULENCE;

EID: 77952702307     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01222-09     Document Type: Article

References (66)

1. Allison, C., N. Coleman, P. L. Jones, and C. Hughes. 1992. Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect. Immun. 60:4740-4746.
2. Allison, C., and C. Hughes. 1991. Closely linked genetic loci required for swarm cell differentiation and multicellular migration by Proteus mirabilis. Mol. Microbiol. 5:1975-1982. (Pubitemid 21896227)
3. Allison, C., H. C. Lai, D. Gygi, and C. Hughes. 1993. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol. 8:53-60.
4. Allison, C., H. C. Lai, and C. Hughes. 1992. Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol. Microbiol. 6:1583-1591.
5. Alteri, C. J., S. N. Smith, and H. L. Mobley. 2009. Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog. 5:e1000448.
6. Altman, P. L. 1961. Physical properties and chemical composition of urine: mammals. Part 1: man, p. 363-369. In D. L. Dittmer (ed.), Blood and other bodily fluids. Federation of American Societies for Experimental Biology, Washington, DC.
7. Armitage, J. P. 1981. Changes in metabolic activity of Proteus mirabilis during swarming. J. Gen. Microbiol. 125:445-450.
8. Belas, R., D. Erskine, and D. Flaherty. 1991. Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J. Bacteriol. 173:6279-6288.
9. Belas, R., D. Erskine, and D. Flaherty. 1991. Transposon mutagenesis in Proteus mirabilis. J. Bacteriol. 173:6289-6293.
10. Belas, R., M. Goldman, and K. Ashliman. 1995. Genetic analysis of Proteus mirabilis mutants defective in swarmer cell elongation. J. Bacteriol. 177:823-828.
11. Belas, R., R. Schneider, and M. Melch. 1998. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J. Bacteriol. 180:6126-6139.
12. Burall, L. S., J. M. Harro, X. Li, C. V. Lockatell, S. D. Himpsl, J. R. Hebel, D. E. Johnson, and H. L. Mobley. 2004. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect. Immun. 72:2922-2938.
13. Claret, L., and C. Hughes. 2000. Rapid turnover of FlhD and FlhC, the flagellar regulon transcriptional activator proteins, during Proteus swarming. J. Bacteriol. 182:833-836. (Pubitemid 30054020)
14. Clemmer, K. M., and P. N. Rather. 2008. The Lon protease regulates swarming motility and virulence gene expression in Proteus mirabilis. J. Med. Microbiol. 57:931-937.
15. Clemmer, K. M., and P. N. Rather. 2007. Regulation of flhDC expression in Proteus mirabilis. Res. Microbiol. 158:295-302.
16. Coker, C., C. A. Poore, X. Li, and H. L. Mobley. 2000. Pathogenesis of Proteus mirabilis urinary tract infection. Microbes Infect. 2:1497-1505.
17. D'Agata, E. M. 2004. Rapidly rising prevalence of nosocomial multidrug-resistant, Gram-negative bacilli: a 9-year surveillance study. Infect. Control Hosp. Epidemiol. 25:842-846.
18. de Boer, P. A., R. E. Crossley, and L. I. Rothfield. 1989. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641-649.
19. Derouaux, A., B. Wolf, C. Fraipont, E. Breukink, M. Nguyen-Disteche, and M. Terrak. 2008. The monofunctional glycosyltransferase of Escherichia coli localizes to the cell division site and interacts with penicillin-binding protein 3, FtsW, and FtsN. J. Bacteriol. 190:1831-1834.
20. Dufour, A., R. B. Furness, and C. Hughes. 1998. Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol. Microbiol. 29:741-751.
21. Falkinham, J. O., III, and P. S. Hoffman. 1984. Unique developmental characteristics of the swarm and short cells of Proteus vulgaris and Proteus mirabilis. J. Bacteriol. 158:1037-1040.
22. Fraser, G. M., and C. Hughes. 1999. Swarming motility. Curr. Opin. Microbiol. 2:630-635.
23. Furness, R. B., G. M. Fraser, N. A. Hay, and C. Hughes. 1997. Negative feedback from a Proteus class II flagellum export defect to the flhDC master operon controlling cell division and flagellum assembly. J. Bacteriol. 179: 5585-5588.
24. Ghelardi, E., F. Celandroni, S. Salvetti, M. Ceragioli, D. J. Beecher, S. Senesi, and A. C. Wong. 2007. Swarming behavior of and hemolysin BL secretion by Bacillus cereus. Appl. Environ. Microbiol. 73:4089-4093.
25. Griffith, D. P., D. M. Musher, and C. Itin. 1976. Urease. The primary cause of infection-induced urinary stones. Invest. Urol. 13:346-350.
26. Gygi, D., M. M. Rahman, H. C. Lai, R. Carlson, J. Guard-Petter, and C. Hughes. 1995. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol. Microbiol. 17:1167-1175.
27. Hagberg, L., I. Engberg, R. Freter, J. Lam, S. Olling, and C. Svanborg Eden. 1983. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect. Immun. 40:273-283.
28. Harshey, R. M. 1994. Bees aren't the only ones: swarming in gram-negative bacteria. Mol. Microbiol. 13:389-394.
29. Harshey, R. M., and T. Matsuyama. 1994. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl. Acad. Sci. U. S. A. 91:8631-8635.
30. Hatt, J. K., and P. N. Rather. 2008. Characterization of a novel gene, wosA, regulating FlhDC expression in Proteus mirabilis. J. Bacteriol. 190:1946-1955.
31. Hay, N. A., D. J. Tipper, D. Gygi, and C. Hughes. 1999. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J. Bacteriol. 181:2008-2016.
32. Inoue, T., R. Shingaki, S. Hirose, K. Waki, H. Mori, and K. Fukui. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J. Bacteriol. 189:950-957.
33. Jansen, A. M., C. V. Lockatell, D. E. Johnson, and H. L. Mobley. 2003. Visualization of Proteus mirabilis morphotypes in the urinary tract: the elongated swarmer cell is rarely observed in ascending urinary tract infection. Infect. Immun. 71:3607-3613.
34. Johnson, D. E., C. V. Lockatell, M. Hall-Craigs, H. L. Mobley, and J. W. Warren. 1987. Uropathogenicity in rats and mice of Providencia stuartii from long-term catheterized patients. J. Urol. 138:632-635.
35. Jones, B. V., R. Young, E. Mahenthiralingam, and D. J. Stickler. 2004. Ultrastructure of Proteus mirabilis swarmer cell rafts and role of swarming in catheter-associated urinary tract infection. Infect. Immun. 72:3941-3950.
36. Jones, H. E., and R. W. Park. 1967. The short forms and long forms of Proteus. J. Gen. Microbiol. 47:359-367.
37. Kim, W., and M. G. Surette. 2004. Metabolic differentiation in actively swarming Salmonella. Mol. Microbiol. 54:702-714.
38. Li, X., D. E. Johnson, and H. L. Mobley. 1999. Requirement of MrpH for mannose-resistant Proteus-like fimbria-mediated hemagglutination by Proteus mirabilis. Infect. Immun. 67:2822-2833. (Pubitemid 29244696)
39. Li, X., H. Zhao, C. V. Lockatell, C. B. Drachenberg, D. E. Johnson, and H. L. Mobley. 2002. Visualization of Proteus mirabilis within the matrix of urease-induced bladder stones during experimental urinary tract infection. Infect. Immun. 70:389-394.
40. Liaw, S. J., H. C. Lai, and W. B. Wang. 2004. Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect. Immun. 72:6836-6845.
41. Liu, Q., M. Z. Li, D. Leibham, D. Cortez, and S. J. Elledge. 1998. The univector plasmid-fusion system, a method for rapid construction of recombinant DNA without restriction enzymes. Curr. Biol. 8:1300-1309.
42. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402.
43. Marr, A. K., J. Overhage, M. Bains, and R. E. Hancock. 2007. The Lon protease of Pseudomonas aeruginosa is induced by aminoglycosides and is involved in biofilm formation and motility. Microbiology 153:474-482.
44. Matsuyama, T., Y. Takagi, Y. Nakagawa, H. Itoh, J. Wakita, and M. Matsushita. 2000. Dynamic aspects of the structured cell population in a swarming colony of Proteus mirabilis. J. Bacteriol. 182:385-393. (Pubitemid 30030122)
45. Mobley, H. L., and J. W. Warren. 1987. Urease-positive bacteriuria and obstruction of long-term urinary catheters. J. Clin. Microbiol. 25:2216-2217.
46. Niki, H., A. Jaffe, R. Imamura, T. Ogura, and S. Hiraga. 1991. The new gene mukB codes for a 177 kD protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 10:183-193. (Pubitemid 21905281)
47. O'Fallon, E., S. Gautam, and E. M. D'Agata. 2009. Colonization with multidrug-resistant gram-negative bacteria: prolonged duration and frequent cocolonization. Clin. Infect. Dis. 48:1375-1381.
48. Osborn, M. J., and L. Rothfield. 2007. Cell shape determination in Escherichia coli. Curr. Opin. Microbiol. 10:606-610.
49. Overhage, J., M. Bains, M. D. Brazas, and R. E. Hancock. 2008. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J. Bacteriol. 190: 2671-2679.
50. Pearson, M. M., and H. L. Mobley. 2008. Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis. Mol. Microbiol. 69:548-558.
51. Pearson, M. M., and H. L. Mobley. 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.
52. Pearson, M. M., M. Sebaihia, C. Churcher, M. A. Quail, A. S. Seshasayee, N. M. Luscombe, Z. Abdellah, C. Arrosmith, B. Atkin, T. Chillingworth, H. Hauser, K. Jagels, S. Moule, K. Mungall, H. Norbertczak, E. Rabbinowitsch, D. Walker, S. Whithead, N. R. Thomson, P. N. Rather, J. Parkhill, and H. L. Mobley. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J. Bacteriol. 190:4027-4037.
53. Rauprich, O., M. Matsushita, C. J. Weijer, F. Siegert, S. E. Esipov, and J. A. Shapiro. 1996. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178:6525-6538.
54. Sabbuba, N., G. Hughes, and D. J. Stickler. 2002. The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int. 89:55-60.
55. Schild, S., R. Tamayo, E. J. Nelson, F. Qadri, S. B. Calderwood, and A. Camilli. 2007. Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2:264-277.
56. Schneider, R., C. V. Lockatell, D. Johnson, and R. Belas. 2002. Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148:773-782.
57. Stahl, S. J., K. R. Stewart, and F. D. Williams. 1983. Extracellular slime associated with Proteus mirabilis during swarming. J. Bacteriol. 154:930-937.
58. Stevenson, L. G., and P. N. Rather. 2006. A novel gene involved in regulating the flagellar gene cascade in Proteus mirabilis. J. Bacteriol. 188:7830-7839.
59. Sturgill, G., and P. N. Rather. 2004. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol. Microbiol. 51:437-446. (Pubitemid 38142132)
60. Turnbull, A. L., and M. G. Surette. 2008. D-Cysteine is required for induced antibiotic resistance in actively swarming Salmonella enterica serovar Typhimurium. Microbiology 154:3410-3419.
61. Verstraeten, N., K. Braeken, B. Debkumari, M. Fauvart, J. Fransaer, J. Vermant, and J. Michiels. 2008. Living on a surface: swarming and biofilm formation. Trends Microbiol. 16:496-506.
62. Walker, K. E., S. Moghaddame-Jafari, C. V. Lockatell, D. Johnson, and R. Belas. 1999. ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol. Microbiol. 32:825-836.
63. Wang, Q., J. G. Frye, M. McClelland, and R. M. Harshey. 2004. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol. Microbiol. 52:169-187.
64. Williams, F. D., D. M. Anderson, P. S. Hoffman, R. H. Schwarzhoff, and S. Leonard. 1976. Evidence against the involvement of chemotaxis in swarming of Proteus mirabilis. J. Bacteriol. 127:237-248.
65. Williams, F. D., and R. H. Schwarzhoff. 1978. Nature of the swarming phenomenon in Proteus. Annu. Rev. Microbiol. 32:101-122.
66. Yamanaka, K., T. Ogura, H. Niki, and S. Hiraga. 1996. Identification of two new genes, mukE and mukF, involved in chromosome partitioning in Escherichia coli. Mol. Gen. Genet. 250:241-251. (Pubitemid 126423709)