Swarming Migration by Proteus and Related Bacteria

Gillian M. Fraser; Richard B. Furness; Colin Hughes

doi:10.1128/9781555818166.ch19

Chapter 19 : Swarming Migration by Proteus and Related Bacteria

Authors: Gillian M. Fraser¹, Richard B. Furness¹, Colin Hughes¹

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Affiliations: 1: Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, United Kingdom

Content Type: Monograph

Publication Year: 2000

Category: Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555818166

Chapter DOI: 10.1128/9781555818166.ch19

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Abstract:

This chapter reviews knowledge of bacterial swarming and the likely underlying mechanisms, focusing principally on studies of Proteus mirabilis. Swarming P. mirabilis produces very large spreading colonies in which concentric zonation, or terracing, results from periodic cycles of mass migration interspersed with population growth without expansion of the colony edge. A role for bacterial motility has been demonstrated in a variety of pathogen-host interactions. Histological analysis of renal tissues from mice infected by wild-type P. mirabilis revealed that differentiated cells were the major invasive cell type. The chapter focuses on molecular analysis of swarming differentiation and migration. Environmental attractants or repellents are recognized by transmembrane receptors, the methyl-accepting chemotaxis proteins (MCPs), that transduce signals to the cytoplasmic components of the chemotaxis phosphorelay, CheWAY. The physiological status of P. mirabilis cells affects their ability to swarm, as high growth rates of vegetative cells on nutrient-rich solid medium stimulate differentiation. Cell-cell contact is stabilized by the production of cell-surface polysaccharides that form a slime capsule around groups of P. mirabilis swarm cells. The primary function of FlhDC is the control of flagella biogenesis, but in Escherichia coli, Serratia liquefaciens, and P. mirabilis FlhDC also represses cell division. The hyperexpression of the flagellar gene hierarchy in Proteus has highlighted induction and negative regulation barely evident in undifferentiated cells, and the coupling of swarming to virulence, whether through an intrinsic role in colonization or coregulation of motility and virulence genes, adds an additional level of significance.

Citation: Fraser G, Furness R, Hughes C. 2000. Swarming Migration by Proteus and Related Bacteria, p 381-401. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch19

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Swarming Migration by Proteus and Related Bacteria

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FIGURE 1

Possible mechanisms of swarming. A simple view of a swarm cell indicating putative underlying mechanisms that have been the foci of study.

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FIGURE 1

Possible mechanisms of swarming. A simple view of a swarm cell indicating putative underlying mechanisms that have been the foci of study.

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FIGURE 2

Swarming on solid growth medium by P. mirabilis. (A) Swarming of P. mirabilis inoculated in the center of a Petri plate containing complex growth medium solidified by 2% agar. V, vegetative cells from the center of the colony; S, part of a hyperflagellated swarm cell from the migrating colony edge. (B) Stages in the swarming cycle of P. mirabilis growing on solid medium. ( From Allison and Hughes, 1991a. )

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FIGURE 2

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FIGURE 3

P. mirabilis swarming-defective mutants. Wild-type P. mirabilis (WT) and transposon mutants, nonmotile nonswarming (NMNS), motile non-swarming (MNS), dendritic swarming (DS), frequent consolidation (FC), and infrequent consolidation (IC), are shown. ( From Allison and Hughes, 1991a. )

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FIGURE 3

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FIGURE 4

The enterobacterial flagellum. A representation of an enterobacterial flagellum is shown, indicating the protein components of each flagellar substructure. The flagellum crosses both the cytoplasmic membrane (CM) and the outer membrane (OM) and is stabilized in the cell envelope by three ring structures: (i) the MS ring, (ii) the Ρ ring, and (iii) the L ring. The axial substructures of the flagellum, i.e., the rod, the hook, the HAPs, and the filament, make up a helical array of polymerized proteins that form a continuous hollow tube. The substructures involved in generating rotation are associated with the CM at the base of the flagellum. The flagellar export apparatus (shaded) is thought to be loosely associated with the base of the flagellum.

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FIGURE 4

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FIGURE 5

FlhDC, a major assimilatory checkpoint. Summary of the observed relationships between known (CRP, UmoA to D, Lrp, and OmpR) and as yet-uncharacterized (X) regulators of the flagellar gene hierarchy. FlhD and FlhC together serve as a regulatory fulcrum assimilating swarm signals and mediating responses. Negative feedback to P. mirabilis flhDC, umoA, and umoD arises from defects in flagellar assembly and class 2 gene repression by the accumulation of the anti-sigma factor FlgM, which binds the flagellum-specific σ28. Arrows, positive regulation; barred lines, negative regulation.

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FIGURE 5

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FIGURE 6

Components and factors identified as involved in swarming. Studies of swarming differentiation in gram-negative organisms, including P. mirabilis, have substantiated the early view of swarming portrayed in Fig. 1 .

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FIGURE 6

References

/content/book/10.1128/9781555818166.chap19

1. Aizawa, S.-I. 1996. Flagellar assembly in Salmonella typhimurium. Mol. Microbiol. 19: 1– 5.

2. Alberti, L.,, and R. M. Harshey. 1990. Differentiation of Serratia marcescens 274 into swimmer cells and swarmer cells. J. Bacteriol. 172: 4322– 4328.

3. Allison, C.,, and C. Hughes. 1991a. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci. Prog. (Edinburgh) 75: 403– 422.

4. Allison, C.,, and C. Hughes. 1991b. Closely linked genetic loci required for swarm cell differentiation and multicellular migration by Proteus mirabilis. Mol. Microbiol. 5: 1975– 1982.

5. Allison, C.,, P. Jones,, N. Coleman,, and C. Hughes. 1992a. Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect. Immun. 60: 4740– 4746.

6. Allison, C.,, H.-C. Lai,, and C. Hughes. 1992b. Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol. Miaobiol. 6: 1583– 1591.

7. 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.

8. Allison, C.,, L. Emody,, N. Coleman,, and C. Hughes. 1994. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J. Infect. Dis. 169: 1155– 1158.

9. Armitage, J. P. 1981. Changes in metabolic activity of Proteus mirabilis during swarming. J. Gen. Microbiol. 125: 445– 450.

10. Arnosti, D. N.,, and M.J. Chamberlin. 1989. Secondary sigma factor controls transcription of flagellar and chemotaxis genes in Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 830– 834..

11. Arricau, N.,, D. Hermant,, H. Waxin,, C. Ecobichon,, P. S. Duffey,, and M. Y. Popoff. 1998. The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolality. Mol. Microbiol. 29: 835– 850.

12. Asai, T.,, M. Takanmi,, and M. Imae. 1990. The AT richness and gid transcription determine the left border of the replication origin of the E. coli chromosome. EMBOJ. 9: 4065– 4072.

13. Bainton, N. J.,, B. W. Bycroft,, S. R. Chhabra,, P. Stead,, L. Gledhill,, P. J. Hill,, C. E. D. Rees,, M. K. Winson,, G. P. C. Salmond,, G. S. A. B. Stewart,, and P. Williams. 1992. A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic synthesis in EruHnia. Gene 116: 87– 91.

14. Bartlett, D. H.,, B. B. Frantz,, and P. Matsumura. 1988. Flagellar transcriptional activators FlbB and FlaI: gene sequences and 5' consensus sequences of operons under FlbB and Flal control. J. Bacteriol. 170: 1575– 1581.

15. Belas, R. 1992. The swarming phenomenon of Proteus mirabilis. ASM News 58: 15– 22.

16. Belas, R. 1994. Expression of multiple flagellin-encoding genes of Proteus mirabilis. J. Bacteriol. 176: 7169– 7181.

17. Belas, R.,, and D. Flaherty. 1994. Sequence and genetic analysis of multiple flagellin-encoding genes from Proteus mirabilis. Gene 128: 33– 41.

18. Belas, R.,, D. Erskine,, and D. Flaherty. 1991a. Transposon mutagenesis in Proteus mirabilis. J. Bacteriol. 173: 6289– 6293.

19. Belas, R.,, D. Erskine,, and D. Flaherty. 1991b. Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J. Bacteriol. 173: 6279– 6288.

20. Belas, R.,, M. Goldman,, and K. Ashliman. 1995. Genetic analysis of Proteus mirabilis mutants defective in swarmer cell elongation. J. Bacteriol. 177: 823– 828.

21. 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.

22. Ben-Jacob, E.,, H. Shmueli,, O. Schochet,, and A. Tenenbaum. 1992. Adaptive self-organization during growth of bacterial colonies. Physica. A 187: 378– 424.

23. Ben-Jacob, E.,, A. Tenenbaum,, O. Schochet,, and O. Avidan. 1994. Holotransformations ofbacterial colonies and genomic cybernetics. Physica. A 202: 1– 47.

24. Bertin, P.,, E. Terao,, E. H. Lee,, P. Lejeune,, C. Colson,, A. Danchin,, and E. Collatz. 1994. The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J. Bacteriol. 176: 5537– 5540.

25. Bisset, K. A. 1973a. The motion of the swarm in Proteus mirabilis. J. Med. Microbiol. 6: 33– 35.

26. Bisset, K. A. 1973b. The zonation phenomenon and structure of the swarm colony in Proteus mirabilis. J. Med. Microbiol. 6: 429– 433.

27. Blair, D. E.,, and H. C. Berg. 1990. The MotA protein of E. coli is a proton conducting component of the flagellar motor. Cell 60: 439– 449.

28. Block, S. M.,, and H. C. Berg. 1984. Successive incorporation of force-generating units in the bacterial rotary motor. Nature 309: 470– 472.

29. Bowden, M. G.,, and H. B. Kaplan. 1998. The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol. Microbiol. 30: 275– 284.

30. Burkart, M.,, A. Toguchi,, and R. M. Harshey. 1998. The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc. Natl. Acad. Sci. USA 95: 2568– 2573.

31. Calvo, J. M.,, and R. G. Matthews. 1994. Leucine-responsive regulatory protein—a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58: 466– 490.

32. Chippendale, G. R., , J. W. Warren,, A. L. Trifillis,, and H. L. T. Mobley. 1994. Internalization of Proteus mirabilis by human renal epithelial cells. Infect. Immun. 62: 3115– 3121.

33. Claret, L. Unpublished data.

34. Coetzee, J. N. 1961. Lysogenic conversion in the genus Proteus. Nature 189: 946– 947.

35. Cooper, K. E.,, J. Davies,, and J. Wieseman. 1971. An investigation of an outbreak of food poisoning associated with organisms of the Proteus group. J. Pathol. Bacteriol. 52: 91– 98.

36. Cosby, W. M.,, D. Vollenbroich,, O. H. Lee,, and P. Zuber. 1998. Altered srf expression in Bacillus subtilis resulting from changes in culture pH is dependent on the Spo0K oligopeptide permease and the ComQX system of extracellular control. J. Bacteriol. 180: 1438– 1445.

37. Deighton, C. M. 1992. P blood group phenotype, Proteus antibody titres, and rheumatoid arthritis. Ann. Rheum. Dis. 51: 1242– 1244.

38. DePamphilis, M. L.,, and J. Adler. 1971. Purification of intact flagella from Escherichia coli and Bacillus subtilis. J. Bacteriol. 105: 376– 383.

39. Dienes, L. 1946. Reproductive processes in Proteus colonies. Proc. Soc. Exp. Biol. Med. 63: 265– 270.

40. Dienes, L. 1947. Further observations on the reproduction of bacilli from large bodies in Proteus cultures. Proc. Soc. Exp. Biol. Med. 66: 97– 98.

41. 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.

42. Dworkin, M. 1996. Recent advances in the social and developmental behaviour of the Myxobacteria. Microbiol. Rev. 60: 70– 102.

43. Eberl, L.,, G. Christiansen,, S. Molin,, and M. Givskov. 1996a. Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J. Bacteriol. 178: 554– 559.

44. Eberl, L.,, G. K. Winson,, C. Sternberg,, G. S. A. B. Stewart,, G. Christiansen,, S. R. Chhabra,, B. Bycroft,, P. Williams,, S. Molin,, and M. Givskov. 1996b. Involvement of N-acyl-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20: 127– 136.

45. Ebringer, A. 1985. Antibodies to Proteus in rheumatoid arthritis. Lancet i: 305– 307.

46. Esipov, S. E.,, and J. A. Shapiro. 1998. Kinetic model of Proteus mirabilis swarm colony development. J. Math. Biol. 36: 249– 268.

47. Falkinham, J. O.,, 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.

48. Fan, F.,, K. Ohnishi,, N. R. Francis,, and R. M. Macnab. 1997. The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol. Microbiol. 26: 1035– 1046.

49. Francis, N. R.,, V. M. Irikura,, S. Yamaguchi,, D. J. DeRosier,, and R. M. Macnab. 1992. Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body. Proc. Natl. Acad. Sci. USA 89: 6304– 6308.

50. Francis, N. R.,, G. E. Sosinsky,, D. Thomas,, and D.J. DeRosier. 1994. Isolation, characterisation and structure of bacterial flagellar motors containing the switch complex. J. Mol. Biol. 235: 1216– 1270.

51. Fraser, G. M. Unpublished data.

52. Fraser, G. M.,, J. C. Q. Bennett,, and C. Hughes. FlgN and FliT, substrate-specific chaperones that facilitate Salmonella flagellum assembly by binding hook-associated proteins. Submitted for publication.

53. Fraser, G. M.,, S. Gupta,, and R. B. Furness. Unpublished data.

54. Fujikawa, H.,, and M. Matsushita. 1989. Fractal growth of Bacillus subtilis on agar plates. J. Phys. Soc. Jpn. 58: 3875– 3878.

55. Furness, R. B. Unpublished data.

56. 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.

57. Gaisser, S.,, and C. Hughes. 1997. A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming defective Proteus mirabilis strain. Mol. Gen. Genet. 253: 415– 427.

58. Givskov, M.,, L. Eberl,, G. Christiansen,, M. J. Bendik,, and S. Molin. 1995a. Induction ofphospholipase and flagellar synthesis in Serratia liquefaciens is controlled by expression of the master operon flhD. Mol. Microbiol. 15: 445– 454.

59. Givskov, M.,, L. Eberl,, and S. Molin. 1995b. Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens. FEMS Microbiol. Lett. 148: 115– 122.

60. Givskov, M.,, J. Ostling,, L. Eberl,, P. W. Lindum,, A. B. Christensen,, G. Christensen,, S. Molin,, and S. Kjelleberg. 1998. Two separate regulatory systems participate in control of swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 742– 745.

61. Grabow, W. O. K. 1972. Growth inhibiting metabolites of Proteus mirabilis. J. Med. Microbiol. 5: 191– 204.

62. Gray, K. M. 1997. Intercellular communication and group behaviour in bacteria. Trends Microbiol. 5: 184– 188.

63. Grossman, A. D.,, and R. Losick. 1988. Extracellular control of spore formation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 85: 4369– 4373.

64. Guard-Petter, J. 1997. Induction of flagellation and a novel-agar-penetrating flagellar structure in Salmonella enterica grown on solid media: possible consequences for serological identification. FEMS Microbiol. Lett. 149: 173– 180.

65. Guard-Petter, J. 1998. Variants of smooth Salmonella enterica serovar enteritidis that grow to higher cell density than the wild type are more virulent. Appl. Environ. Microbiol. 64: 2166– 2172.

66. Guard-Petter, J.,, D.J. Henzler,, M. M. Rahman,, and R. W. Carlson. 1997. On-farm monitoring of mouse-invasive Salmonella enterica serovar enteritidis and a model for its association with the production of contaminated eggs. Appl. Environ. Microbiol. 63: 1588– 1593.

67. Guo, M. M. S.,, and P. V. Lin. 1965. Serological specificities of ureases of Proteus species. J. Gen. Microbiol. 38: 417– 422.

68. Gygi, D.,, and N. A. Hay. Unpublished data.

69. Gygi, D.,, M.J. Bailey,, C. Allison,, and C. Hughes. 1995a. Requirement for FlhA in flagella assembly and swarm cell differentiation by Proteus mirabilis. Mol. Microbiol. 15: 761– 769.

70. Gygi, D.,, M. M. Rahman,, H.-C. Lai,, R. Carlson,, J. Guard-Petter,, and C. Hughes. 1995b. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol. Microbiol. 17: 1167– 1175.

71. Gygi, D.,, G. Fraser,, A. Dufour,, and C. Hughes. 1997. A motile but non-swarming mutant of Proteus mirabilis lacks FlgN, a facilitator of flagella filament assembly. Mol. Microbiol. 25: 597– 604.

72. Harshey, R. M. 1994. Bees aren't the only ones: swarming in Gram-negative bacteria. Mol. Microbiol. 13: 389– 394.

73. Harshey, R. M.,, and P. Matsuyama. 1994. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface induced differentiation into hyper-flagellate swarmer cells. Proc. Natl. Acad. Sci. USA 91: 8631– 8635.

74. Hay, N. A.,, and D. J. Tipper. Unpublished data.

75. Hay, N. A.,, D. J. Tipper,, D. Gygi,, and C. Hughes. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. Submitted for publication.

76. Hay, N. A.,, D. J. Tipper,, D. Gygi,, and C. Hughes. 1997. A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J. Bacteriol. 179: 4741– 4746.

77. Henrichsen, J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36: 478– 503.

78. Hoeniger, J. F. M. 1964. Cellular changes accompanying the swarming of Proteus mirabilis. I. Observations on living cultures. Can. J. Microbiol. 10: 1– 9.

79. Hoeniger, J. F. M. 1965. Development of flagella by Proteus mirabilis. J. Gen. Microbiol. 40: 29– 42.

80. Hoeniger, J. F. M. 1966. Cellular changes accompanying the swarming of Proteus mirabilis. I. Observations of stained organisms. Can. J. Microbiol. 12: 113– 122.

81. Hughes, K. T.,, K. L. Gillen,, J. S. Melinda,, and J. E. Karlinsey. 1993. Sensing structural intermediates in bacterial flagella assembly by export of a negative regulator. Science 262: 1277– 1280.

82. Jones, H. E.,, and R. W. A. Park. 1967a. The short and long forms of Proteus. J. Gen. Microbiol. 47: 359– 367.

83. Jones, H. E.,, and R. W. A. Park. 1967. The influence of medium composition on the growth and swarming of Proteus. J. Gen. Microbiol. 47: 369– 378.

84. Kaplan, H. B.,, and L. Plamann. 1996. A Myxococcus xanthus cell density-sensing system required for multicellular development. FEMS Microbiol. Lett. 139: 89– 95.

85. Kawagashi, I.,, M. Imagawa,, Y. Imae,, L. McCarter,, and M. Homma. 1996. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol. Microbiol. 20: 693– 699.

86. Khan, S. I.,, H. Khan,, and T. S. Reese. 1991. New structural features of the flagellar base in Salmonella typhimurium revealed by rapid-freeze electron microscopy. J. Bacteriol. 173: 2888– 2896.

87. Kim, S. K.,, and D. Kaiser. 1990. Cell alignment required in differentiation of Myxococcus xanthus. Science 249: 926– 928.

88. Klienberger-Nobel, E. 1947. Morphological appearances of various stages in B. proteus and E. coli. J. Hyg. 45: 410– 412.

89. Krajden, S.,, M. Fuksa,, W. Lizewski,, L. Barton,, and A. Lee. 1984. Proteus penneri and urinary calculi formation., J. Clin. Microbiol. 19: 541– 542.

90. Kubori, T.,, N. Shimamoto,, S. Yamaguchi,, K. Namba,, and S.-I. Aizawa. 1992. Morphological pathway of flagellar assembly in Salmonella typhimurium. J. Mol. Biol. 226: 433– 446.

91. Kutsukake, K.,, and T. lino. 1994. Role of the FliA-FlgM regulatory system on the transcriptional control of the flagellar regulon and flagellar formation in Salmonella typhimurium. J. Bacteriol. 176: 3598– 3605.

92. Kutsukake, K.,, Y. Ohya,, and T. lino. 1990. Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J. Bacteriol. 172: 741– 747.

93. Lai, H.-C. 1994. Ph.D. thesis. University of Cambridge, Cambridge, United Kingdom.

94. Lai, H.-C.,, J.-C. Shu,, S. Ang,, M.-J. Lai,, B. Fruta,, S. Lin,, K.-T. Lu,, and S.-W. Ho. 1997. Effect of glucose concentration on swimming motility in Enterobacteria. Biochem. Biophys. Res. Commun. 231: 692– 695.

95. Lai, H.-C.,, D. Gygi,, G. M. Fraser,, and C. Hughes. 1998. A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology 144: 1957– 1961.

96. Lindum, P. W.,, U. Anthoni,, C. ChristofFersen,, L. Eberl,, S. Molin,, and M. Givskov. 1998. N-acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosur-factant required for swarming motility of Serratia liquefaciens MG1. J. Bacteriol. 180: 6384– 6388.

97. Liu, X.,, and P. Matsumura. 1994. The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J. Bacteriol. 176: 7345– 7351.

98. Lominski, I.,, and A. C. Lendrum. 1947. The mechanism of swarming of Proteus. J. Pathol. Bacteriol. 59: 688– 691.

99. Loomes, L. M.,, B. W. Senior,, and M. A. Kerr. 1990. A proteolytic enzyme secreted by Proteus mirabilis degrades immunoglobulins of the immunoglobulin Al (IgAl), IgA2, and IgG isotypes. Infect. Immun. 58: 1979– 1985.

100. Macnab, R. M. 1992. Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet. 26: 131– 158.

101. Macnab, R. M., 1996. Flagella and motility, p. 123– 145. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed., vol. 1. American Society for Microbiology, Washington, D.C.

102. Magnuson, R.,, J. Solomon,, and A. D. Grossman. 1994. Biochemical and genetic characterisation of a competence pheromone from B. subtilis. Cell 77: 207– 216.

103. Matsuyama, T.,, M. Sogawa,, and Y. Nakagawa. 1989. Fractal spreading growth of Serratia marcescens which produces surface active exolipids. FEMS Microbiol. Lett. 61: 243– 246.

104. Matsuyama, T.,, K. Kaneda,, Y. Nakagawa,, K. Isa,, H. Hara-Hotta,, and Y. Isuya. 1992. A novel extracellular cyclic lipopeptide which promotes flagellum-dependent and -independent spreading growth of Serratia marcescens. J. Bacteriol. 174: 1769– 1776.

105. McCarter, L.,, and M. Silverman. 1990. Surface induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol. Miaobiol. 4: 1057– 1062.

106. McCarter, L.,, M. Hilmen,, and M. Silverman. 1988. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54: 345– 351.

107. Mobley, H. L. T.,, and R. Belas. 1995. Swarming and pathogenicity of Proteus mirabilis in the urinary tract. Trends Microbiol. 3: 280– 284.

108. Mobley, H. L. T.,, G. R. Chippendale,, K. G. Swihart,, and R. A. Welch. 1991. Cytotoxicity of the HpmA hemolysin and urease of Proteus mirabilis and Proteus vulgaris against cultured human renal proximal tubular epithelial cells. Infect. Immun. 59: 2036– 2042.

109. Moltke, O. 1927. Contributions to the Characterization and Systematic Classification of Bad. Proteus vulgaris (Hauser). Levin and Munksgaard, Copenhagen, Denmark.

110. Murphy, C. A.,, and R. Belas. 1999. Genomic rearrangements in the flagellin genes of Proteus mirabilis. Mol. Miaobiol. 31: 679– 690.

111. Namba, K.,, and F. Vonderviszt. 1997. Molecular architecture of the bacterial flagellum. Q. Rev. Biophys. 30: 1– 65.

112. Naylor, P. 1964. The effect of electrolytes or carbohydrates in a sodium chloride deficient medium on the formation of discrete colonies of Proteus and the influence of these substances on growth in liquid culture. J. Appl. Bacteriol. 27: 422– 431.

113. Ohgiwari, M.,, M. Mutsushita,, and T. Matsuyama. 1992. Morphological changes in growth phenomena of bacterial colony patterns. J. Phys. Soc. Jpn. 61: 816– 822.

114. Ohnishi, K.,, K. Kutsukake,, H. Suzuki,, and T. lino. 1992. A novel transcriptional mechanism in the flagellar regulon of Salmonella typhimurium: an anti-sigma factor inhibits the activity of the flagellum-specific sigma factor ? F. Mol. Microbiol. 6: 3149– 3157.

115. Otteman, K. M.,, and J. F. Miller. 1997. Roles for motility in bacterial-host interactions. Mol. Microbiol. 24: 1109– 1117.

116. Parker, C. T.,, A. W. Kloser,, C. A. Schnaitman,, M. A. Stein,, S. Gottesman,, and B. W. Gibson. 1992. Role of the rfaG and rafP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12 . J. Bacteriol. 174: 2525– 2538.

117. Peerbooms, P. G. H.,, A. M. J. Verweij,, and D. M. MacLaren. 1984. Vero cell invasiveness of Proteus mirabilis. Infect. Immun. 43: 1068– 1071.

118. Peerbooms, P. G. H.,, A. M. J. Verweij,, and D. M. MacLaren. 1985. Uropathogenic properties of Proteus mirabilis and Proteus vulgaris. J. Med. Microbiol. 19: 55– 60.

119. Penner, J. L., 1992. The genera Proteus, Providencia, and Morganella, p. 2849– 2853. In A. Balows et al., (ed.), The Prokaryotes, vol. III. Springer-Verlag KG, Berlin, Germany.

120. Proom, H.,, and A. Woiwod. 1951. Amine production in the genus Proteus. J. Gen. Microbiol. 5: 930– 938.

121. Pruβ, B. M.,, and P. Matsumura. 1996. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J. Bacteriol. 178: 668– 674.

122. Pruβ, B. M.,, D. Maekovic,, and P. Matsumura. 1997. The Escherichia coli flagellar transcriptional activator flhD regulates cell division through induction of the acid response gene cadA. J. Bacteriol. 179: 3818– 3821.

123. Rahman, M. M.,, J. Guard-Petter,, and R. W. Carlson. 1997. A virulent isolate of Salmonella enteritidis produces a Salmonella typhi-like lipopolysaccharide. J. Bacteriol. 179: 2126– 2131.

124. 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.

125. Roberts, R. C.,, C. D. Mohr,, and L. Shapiro. 1996. Developmental programs in bacteria. Cun. Top. Dev. Biol. 34: 207– 257.

126. Rosenstein, I.J. M. 1986. Urinary calculi: microbiological and crystallographic studies. Crit. Rev. Clin. Lab. Sci. 22: 245– 277.

127. Rosenstein, I. J. M.,, J. M. Hamilton-Miller,, and W. Brumfitt. 1981. Role of urease in the formation of infection stones: comparison of ureases from different sources. Infect. Immun. 32: 32– 37.

128. Rozalski, A.,, H. Dlugonska,, and K. Kotelko. 1986. Cell invasiveness of Proteus mirabilis and Proteus vulgaris strains. Arch. Immunol. Ther. Exp. 34: 505– 511.

129. Rozalski, A.,, H. Sidorczyk,, and K. Kotelko. 1997. Potential virulence factors of Proteus bacilli. Microbiol. Mol. Biol. Rev. 61: 65– 89.

130. Rudner, D. Z.,, J. R. LeDeaux,, K. Ireton,, and A. D. Grossman. 1991. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J. Bacteriol. 173: 1388– 1398.

131. Salmond, G. P. C.,, B. W. Bycroft,, G. S. A. B. Stewart,, and P. Williams. 1995. The bacterial 'enigma': cracking the code of cell-cell communication. Mol. Microbiol. 16: 615– 624.

132. Senior, B. W. 1977. The Dienes phenomenon: identification of the determinants of compatibility. J. Med. Microbiol. 102: 235– 244.

133. Senior, B. W.,, and C. Hughes. 1987. Production and properties of haemolysins from clinical isolates of the Proteeae. J. Med. Miaobiol. 24: 17– 25.

134. Senior, B. W.,, N. C. Bradford,, and D. S. Simpson. 1980. The ureases of Proteus strains in relation to virulence for the urinary tract. J. Med. Microbiol. 13: 507– 512.

135. Shapiro, J. A. 1995. The significances of bacterial colony patterns. Bioessays 17: 597– 607.

136. Shapiro, J. A. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52: 81– 104.

137. Shapiro, L.,, and R. Losick. 1997. Protein localization and cell fate in bacteria. Science 276: 712– 717.

138. Shin, S.,, and C. Park. 1995. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J. Bacteriol. 177: 4696– 4702.

139. Silverman, M.,, and M. Simon. 1974. Characterization of Escherichia coli flagellar mutants that are insensitive to catabolite repression. J. Bacteriol. 120: 1196– 1203.

140. Skirrow, M. B. 1969. The Dienes (mutual inhibition) test in the investigation of Proteus infections. J. Med. Microbiol. 2: 471– 477.

141. Sogaard-Andersen, L.,, and D. Kaiser. 1996. C factor, a cell-surface-associated intercellular signalling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. Proc. Natl. Acad. Sci USA 93: 2675– 2679.

142. Stahl, S. J.,, K. R. Stewart,, and F. D. Williams. 1983. Extracellular slime associated with Proteus mirabilis during swarming. J. Bacteriol. 154: 930– 937.

143. Stefansson, K. 1985. Sharing of antigenic determinants between the nicotinic acetylcholine receptor and proteins in E. coli, Proteus vulgaris and Klebsiella pneumoniae: possible role in the pathogenesis of myasthenia gravis. N. Engl. J. Med. 312: 221– 225.

144. Stickler, D. J.,, J. B. King,, C. Winters,, and S. L. Morris. 1993a. Blockage of uretheral catheters by bacterial biofilms. J. Infect. 27: 133– 135.

145. Stickler, D. J.,, L. Ganderton,, J. B. King,, J. Net-tleton,, and C. Winters. 1993b. Proteus mirabilis biofilms and the encrustation of urethral catheters. Urol. Res. 21: 407– 411.

146. Stock, J. B.,, and M. Surette,. 1996. Chemotaxis, p. 1103– 1129. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, C. B. Low,, B. Maga-sanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed., vol. 1. American Society for Microbiology, Washington, DC.

147. Sturdza, S. A. 1973. La reaction d'immobilisation des filaments des Proteus sur les milieux geloses. Arch. Roum. Pathol. Exp. Microbiol. 32: 575– 580.

148. Swihart, K. G.,, and R. A. Welch. 1990. Cytotoxic activity of the Proteus hemolysin HpmA. Infect. Immun. 58: 1861– 1869.

149. Uphoff, T. S.,, and R. A. Welch. 1990. Nucleotide sequencing of the Proteus mirabilis calcium-independent hemolysin genes (hpmA and hpmB) reveals sequence similarity with Serratia marcescens hemolysin genes (shlA and shlB). J. Bacteriol. 172: 1206– 1216.

150. von Meyenburg, K.,, B. Jorgensen,, J. Neilson,, and F. Hansen. 1982. Promoters of the atp operon coding for the membrane-bound ATP-synthase of Escherichia coli mapped by ?n 10 insertion mutations. Mol. Gen. Genet. 188: 240– 248.

151. Warren, J. W.,, D. Damron,, J. H. Tenney,, J. M. Hoopes,, B. Deforge,, and H.J. Muncie. 1987. Fever, bacteremia and death as complications of bacteriuria in women with long-term urethral catheters J. Infect. Dis. 155: 1151– 1158.

152. Wassif, C.,, D. Cheek,, and R. Belas. 1995. Molecular analysis of metalloprotease from Proteus mirabilis. J. Bacteriol. 177: 5790– 5798.

153. Willey, J.,, J. Schwedock,, and R. Losick. 1993. Multiple extracellular signals govern the production of a morphogenetic protein involved in ariel mycelium formation by Streptomyces coelicolor. Genes Dev. 7: 895– 903.

154. Williams, F. D.,, and R. H. Schwarzhoff. 1978. Nature of the swarming phenomenon in Proteus. Annu. Rev. Microbiol. 32: 101– 122.

155. 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.

156. Zhao, H.,, R. B. Thompson,, V. Lockatell,, D. E. Johnson,, and H. L. T. Mobley. 1998. Use of green fluorescent protein to assess urease gene expression by uropathogenic Proteus mirabilis during experimental ascending urinary tract infection. Infect. Immun. 66: 330– 335.