Swarming motility

Current Opinion in Microbiology

Volumn 2, Issue 6, 1999, Pages 630-635

  Fraser, Gillian M ^a   Hughes, Colin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DENSITY; CELL DIFFERENTIATION; CELL MIGRATION; CILIARY MOTILITY; FLAGELLUM; NONHUMAN; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 0032740147     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(99)00033-8     Document Type: Review

References (62)

1. Allison C., Hughes C. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci Progress Edinburgh. 75:1991;403-422.
2. Harshey R.M. Bees aren't the only ones: swarming in Gram-negative bacteria. Mol Microbiol. 13:1994;389-394.
3. Fraser G.M., Furness R.B., Hughes C. Swarming migration by Proteus and related bacteria. Brun Y., Shimkets L. Prokaryotic Development. 1999;American Society for Microbiology, Washington, DC. in press.
4. Rauprich O., Matsushita M., Weijer C.J., Siegert F., Esipov S.E., Shapiro J.A. Periodic phenomena in Proteus mirabilis swarm colony development. J Bacteriol. 178:1996;6525-6538.
5. McCarter L.L. The multiple identities of Vibrio parahaemolyticus. J Mol Microbiol Biotechnol. 1:1999;51-57. A review describing the adaptation of V. parahaemolyticus to diverse environments. The author discusses signals, such as surface contact and iron limitation, that trigger differentiation of swimmer cells to hyper-flagellated swarmer cells.
6. Eberl L., Molin S., Givskov M. Surface motility of Serratia liquefaciens MG1. J Bacteriol. 181:1999;1703-1712. A review of the molecular mechanisms suggested to underlie S. liquefaciens swarming, and the ecological relevance of population migration.
7. Otteman K.M., Miller J.F. Roles for motility in bacterial-host interactions. Mol Microbiol. 24:1997;1109-1117.
8. Guard-Petter J. 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. 149:1997;173-180.
9. Young G.M., Smith M.J., Minnich M.J., Miller V.L. The Yersinia enterocolitica motility master regulatory operon, flhDC, is required for flagellin production, swimming motility, and swarming motility. J Bacteriol. 181:1999;2823-2833. Swarming of Y. enterocolitica on growth media containing 0.6% agar is demonstrated. A number of flagellar genes are required for swarming and, as in other enterobacteria, the flhDC flagellar master operon regulates flagella biogenesis and swarming motility.
10. Allison C., Emody L., Coleman N., Hughes C. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J Infect Dis. 169:1994;1155-1158.
11. Stickler D., Morris N., Moreno M.C., Sabbuba N. Studies on the formation of crystalline bacterial biofilms on urethral catheters. Eur J Microbiol Infect Dis. 17:1998;649-652.
12. Murphy C.A., Belas R. Genomic rearrangements in the flagellin genes of Proteus mirabilis. Mol Microbiol. 31:1999;679-690. P. mirabilis carries three flagellin genes, termed flaABC: flaA and flaB are adjacent, and flaC is not closely linked. Normally, only flaA is expressed, but in non-motile flaA mutant populations motile revertants are found at a low frequency. Reversion is the result of flaA-flaB gene conversion. Rearrangement of the flaA-flaB genes occurs at any one of nine homologous domains. Analysis of vegetative cells, swarm cells, and cells isolated from a urinary tract infection identified six classes of flaA-flaB rearrangement that occur with different frequencies and distributions, depending on environmental conditions.
13. Allison C., Lai H.-C., Hughes C. Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol Microbiol. 6:1992;1583-1591.
14. Rozalski A., Sidorczyk Z., Kotelko K. Potential virulence factors of Proteus bacilli. Microbiol Mol Biol Rev. 61:1997;65-89.
15. Walker K.E., Moghaddame-Jafari S., Lockatell C.V., Johnson D., Belas R. ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol Microbiol. 32:1999;825-836. Expression of the zapA IgA protease gene increases at least 20-fold during the swarming cycle, with maximal expression occurring in swarm cells just prior to consolidation. ZapA is not required for swarming differentiation and migration, but a zapA mutant is attenuated for virulence in a mouse model of ascending urinary tract infection. The zapA gene is part of a locus encoding a second metalloprotease, ZapE, and an ABC transporter system, ZapBCD.
16. Givskov M., Eberl L., Christiansen G., Bendik M.J., Molin S. Induction of phospholipase and flagellar synthesis in Serratia liquefaciens is controlled by expression of the master operon flhD. Mol Microbiol. 15:1995;445-454.
17. Young G.M., Schmiel D.H., Miller V.L.A. new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein secretion system. Proc Natl Acad Sci USA. 96:1999;6456-6461.
18. Latta R.K., Grondin A., Jarrell H.C., Nicholls G.R., Berube L.R. Differential expression of nonagglutinating fimbriae and MR/P pili in swarming colonies of Proteus mirabilis. J Bacteriol. 181:1999;3220-3225.
19. Belas R., Schneider R., Melch M. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriol. 180:1998;6126-6139. Transposon insertions in the rsbA and rcsC genes, encoding membrane sensor kinases of the two-component regulator family, result in constitutive differentiation and precocious swarming. The rsbA mutant does not require signals such as surface contact and amino acids to stimulate differentiation, and it initiates migration at cell densities 100-fold lower than wild-type. Overexpression of RsbA in the wild-type also results in precocious swarming, indicating that this protein might function as both a positive and negative regulator of swarming.
20. Guard-Petter J. Variants of smooth Salmonella enterica serovar enteritidis that grow to higher cell-density than the wild type are more virulent. Appl Environ Microbiol. 64:1998;2166-2172.
21. •]).
22. McCarter L.L. OpaR, a homolog of Vibrio harveyi LuxR, controls opacity of Vibrio parahaemolyticus. J Bacteriol. 180:1998;3166-3173.
23. Allison C., Lai H.-C., Gygi D., Hughes C. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol Microbiol. 8:1993;53-60.
24. Zhao H., Li X., Johnson D.E., Mobley H.L.T. Identification of protease and rpoN-associated genes of of uropathogenic Proteus mirabilis by negative selection in a mouse model of ascending urinary tract infection. Microbiology. 145:1999;185-195.
25. Gaisser S., Hughes C. A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming defective Proteus mirabilis strain. Mol Gen Genet. 253:1997;415-427.
26. Magnuson R., Solomon J., Grossman A.D. Biochemical and genetic characterisation of a competence pheremone from B. subtilis. Cell. 77:1994;207-216.
27. Stock JB, Surette M: Chemotaxis. In Escherichia coli and Salmonella Typhimurium: Cellular and Molecular Biology, vol 1, edn 2. Edited by Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB et al. Washington DC: American Society for Microbiology; 1996:1103-1129.
28. Belas R., Erskine D., Flaherty D. Proteus mirabilis mutants defective in swarmer cell differentiaton and multicellular behaviour. J Bacteriol. 173:1991;6279-6288.
29. O'Rear J., Alberti L., Harshey R.M. Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function. J Bacteriol. 174:1992;6125-6137.
30. Sar N., McCarter L., Simon M., Silverman M. Chemotactic control of the two flagellar systems of Vibrio parahaemolyticus. J Bacteriol. 172:1990;334-341.
31. Jiang Z.-Y., Gest H., Bauer C.E. Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J Bacteriol. 179:1997;5720-5727.
32. Jiang Z.-Y., Rushing B.G., Bai Y., Gest H., Bauer C.E. Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol. 180:1998;1248-1255.
33. Harshey R.M., Matsuyama P. Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci USA. 91:1994;8631-8635.
34. Burkart M., Toguchi A., Harshey R.M. The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc Natl Acad Sci USA. 95:1998;2568-2573. The Tsr and Tar chemoreceptors can individually support swarming, although saturation or disruption of chemoattractant binding does not affect differentiation or migration. Similarly, non-chemotactic flagellar switch mutants can still swarm. Although chemotactic behaviour is not required, signalling through the CheWAY phosphorelay is essential for swarming differentiation.
35. Rudner R., Martsinkevich O., Leung W., Jarvis E.D. Classification and genetic characterization of pattern forming Bacilli. Mol Microbiol. 27:1998;687-703.
36. Hay N.A., Tipper D.J., Gygi D., Hughes C. A non-swarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J Bacteriol. 179:1997;4741-4746.
37. Calvo J.M., Matthews R.G. Leucine-responsive regulatory protein - a global regulator of metabolism in Escherichia coli. Microbiol Rev. 58:1994;466-490.
38. Belas R., Goldman M., Ashliman K. Genetic analysis of Proteus mirabilis mutants defective in swarmer cell elongation. J Bacteriol. 177:1995;823-828.
39. Rao N.N., Liu S., Kornberg A. Inorganic polyphosphate in Escherichia coli: the phosphate regulon and the stringent response. J Bacteriol. 180:1998;2186-2193.
40. Lai H.-C., Gygi D., Fraser G.M., Hughes C. A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology. 144:1998;1957-1961.
41. McCarter L.L., Hilmen M., Silverman M. Flagellar dynamometer controls swarmer cell diffferentiation of V. parahaemolyticus. Cell. 54:1988;345-351.
42. Kawagashi I., Imagawa M., Imae Y., McCarter L.L., Homma M. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol Microbiol. 20:1996;693-699.
43. Jaques S., Kim Y.-K., McCarter L.L. Mutations conferring resistance to phenamil and amiloride, inhibitors of sodium-driven motility of Vibrio parahaemolyticus. Proc Natl Acad Sci USA. 96:1999;5740-5745.
44. Gygi D., Bailey M.J., Allison C., Hughes C. Requirement for FlhA in flagella assembly and swarm cell differentiation by Proteus mirabilis. Mol Microbiol. 15:1995;761-769.
45. Gygi D., Fraser G., Dufour A., Hughes C. A motile but non-swarming mutant of Proteus mirabilis lacks FlgN, a facilitator of flagella filament assembly. Mol Microbiol. 25:1997;597-604.
46. Eberl L., Christiansen G., Molin S., Givskov M. Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J Bacteriol. 178:1996;554-559.
47. Furness R.B., Fraser G.M., Hay N.A., Hughes C. Negative feedback from a Proteus Class II flagellum export defect to the flhDC master operon controlling cell division and flagellum assembly. J Bacteriol. 179:1997;5585-5588.
48. Hay N.A., Tipper D.J., Gygi D., Hughes C. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J Bacteriol. 181:1999;2008-2016. A transposon insertion in the novel ccmA gene abolishes swarming and causes differentiated P. mirabilis cells to have a curved morphology. Two forms of the wild-type CcmA protein are present in the cytosolic membrane: a full-length integral membrane protein and an amino-terminally truncated peripheral membrane protein. In the ccmA transposon mutant, wild-type levels of carboxy-terminally truncated versions of both proteins are present. A ccmA null mutant swarms slowly, and elongated cells are less misshapen than those of the transposon mutant. The CcmA protein might function to maintain linearity of elongated swarm cells.
49. Gygi D., Hughes C. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol Microbiol. 17:1995;1167-1175.
50. Rahman M.M., Guard-Petter J., Asokan K., Hughes C., Carlson R.W. The structure of the colony migration factor from pathogenic Proteus mirabilis: a capsular polysaccharide that facilitates swarming. J Biol Chem. 274:1999;22993-22998. P. mirabilis produces an acidic capsular polysaccharide (Cmf-CPS) that facilitates swarming migration. The structure of Cmf-CPS is determined by glycosyl composition and linkage analysis, and 1D and 2D NMR spectroscopy. The Cmf-CPS structures of two P. mirabilis isolates and a P. vulgaris isolate are compared. All three are acidic, and contain at least one uronosyl residue and aminosugars.
51. •]). The migration defect of swrA and swrI mutants can be complemented by addition of surfactants to the growth media, suggesting that swrA is the only swarming-specific gene that is controlled as part of the SwrI quorum sensing regulon.
52. Cosby W.M., Vollenbroich D., Lee O.H., Zuber P. Altered srf expression in Bacillus subtilis resulting from changes in culture pH is dependent on the SpoOK oligopeptide permease and the ComQX system of extracellular control. J Bacteriol. 180:1998;1438-1445.
53. Esipov S.E., Shapiro J.A. Kinetic model of Proteus mirabilis swarm colony development. J Math Biol. 36:1998;249-268. Presents a mathematical model describing the swarm cell differentiation/de-differentiation cycle and the spatial evolution of swimmer and swarmer cells during swarm colony development. Central to this model are the age dependence of swarm cell behaviour, and cell density thresholds for population migration.
54. Fraser G.M., Bennett J.C.Q., Hughes C. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol. 32:1999;569-580. The motile P. mirabilis flgN mutant cannot hyperflagellate or swarm. Loss of FlgN results in decreased export of the flagellar hook-associated proteins (HAPs) FlgK and FlgL, thus reducing efficiency of flagellum assembly. Studies in S. typhimurium show that FlgN binds to the carboxy-terminal helices of FlgK and FlgL, and that the similar FliT protein binds to the carboxyl terminus of the flagellar cap protein, FliD (HAP2). The data indicate that FlgN and FliT are substrate-specific chaperones that facilitate HAP export.
55. Macnab RM: Flagella and motility. In Escherichia coli and Salmonella Typhimurium: Cellular and Molecular Biology, vol 1, edn 2. Edited by Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB et al. Washington, DC: American Society for Microbiology; 1996:123-145.
56. Pruß B.M., Matsumura P. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J Bacteriol. 178:1996;668-674.
57. Pruß B.M., Maekovic D., Matsumura P. The Escherichia coli flagellar transcriptional activator flhD regulates cell division through induction of the acid response gene cadA. J Bacteriol. 179:1997;3818-3821.
58. Gottesman S. Regulation by proteolysis: developmental switches. Curr Opin Microbiol. 2:1999;142-147.
59. Stewart B.L., Enos-Berlage J.L., McCarter L. The lonS gene regulates swarmer cell differentiation of Vibrio parahaemolyticus. J Bacteriol. 179:1997;107-114.
60. Dufour A., Furness R.B., Hughes C. Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol Microbiol. 29:1998;741-751. This paper reports the isolation and characterisation of the P. mirabilis umoA, umoB, umoC and umoD genes, which upregulate expression of the flhDC flagellar master operon when present in trans and multicopy. Mutations in the chromosomal umo genes reduce swarming differentiation and decrease expression of flhDC. The umoB and umoC transcripts are rare, but umoA and umoD are upregulated during differentiation in parallel with flhDC. UmoB and UmoD are similar to the predicted products of the E. coli uncharacterised open reading frames yrfF and ycfJ, respectively; UmoA and UmoC have no known homologues. All four Umo proteins are predicted to localise to the cell envelope.
61. Whitfield C., Roberts I.S. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol Microbiol. 31:1999;1307-1319.
62. Taylor B.L., Zhulin I.B. In search of higher energy: metabolism-dependent behaviour in bacteria. Mol Microbiol. 28:1998;683-690.