More than motility: Salmonella flagella contribute to overriding friction and facilitating colony hydration during swarming

Journal of Bacteriology

Volumn 195, Issue 5, 2013, Pages 919-929

  Partridge, Jonathan D ^a   Harshey, Rasika M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; AMPICILLIN; BACTERIAL PROTEIN; CHLORAMPHENICOL; KANAMYCIN; MOTAB PROTEIN; UNCLASSIFIED DRUG; WATER;

ANTIBIOTIC RESISTANCE; ARTICLE; CHEMOTAXIS; FLAGELLUM; FRICTION; GENE EXPRESSION; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; SALMONELLA; SURFACE PROPERTY;

AGAR; BACTERIAL PROTEINS; CELL DIVISION; CHEMOTACTIC FACTORS; CHEMOTAXIS; DNA, BACTERIAL; FLAGELLA; FRICTION; MEMBRANE PROTEINS; MUTATION; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION;

EID: 84873541778     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02064-12     Document Type: Article

References (64)

1. Harshey RM. 2003. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57:249-273.
2. Kearns DB. 2010. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8:634-644.
3. Partridge JD, Harshey RM. 2013. Swarming: flexible roaming plans. J. Bacteriol. 195:909-918.
4. McCarter LL. 2004. Dual flagellar systems enable motility under different circumstances. J. Mol. Microbiol. Biotechnol. 7:18-29.
5. Allison C, Hughes C. 1991. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci. Prog. 75:403-422.
6. Rather PN. 2005. Swarmer cell differentiation in Proteus mirabilis. Environ. Microbiol. 7:1065-1073.
7. Pearson MM, Rasko DA, Smith SN, Mobley HL. 2010. Transcriptome of swarming Proteus mirabilis. Infect. Immun. 78:2834-2845.
8. Gode-Potratz CJ, Kustusch RJ, Breheny PJ, Weiss DS, McCarter LL. 2011. Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol. Microbiol. 79:240-263.
9. Gode-Potratz CJ, McCarter LL. 2011. Quorum sensing and silencing in Vibrio parahaemolyticus. J. Bacteriol. 193:4224-4237.
10. Trimble MJ, McCarter LL. 2011. Bis-(3'-5')-cyclic dimeric GMP-linked quorum sensing controls swarming in Vibrio parahaemolyticus. Proc. Natl. Acad. Sci. U. S. A. 108:18079-18084.
11. Belas R, Simon M, Silverman M. 1986. Regulation of lateral flagellar gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 167:210-218.
12. McCarter L, Hilmen M, Silverman M. 1988. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54:345-351.
13. Kawagishi I, Imagawa M, Imae Y, McCarter L, Homma M. 1996. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol. Microbiol. 20:693-699.
14. Kearns DB, Losick R. 2003. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49:581-590.
15. Salvetti S, Faegri K, Ghelardi E, Kolsto AB, Senesi S. 2011. Global gene expression profile for swarming Bacillus cereus bacteria. Appl. Environ. Microbiol. 77:5149-5156.
16. Patrick JE, Kearns DB. 2012. Swarming motility and the control of master regulators of flagellar biosynthesis. Mol. Microbiol. 83:14-23.
17. 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.
18. Hsueh YH, Cozy LM, Sham LT, Calvo RA, Gutu AD, Winkler ME, Kearns DB. 2011. DegU-phosphate activates expression of the anti-sigma factor FlgM in Bacillus subtilis. Mol. Microbiol. 81:1092-1108.
19. Calvio C, Osera C, Amati G, Galizzi A. 2008. Autoregulation of swrAA and motility in Bacillus subtilis. J. Bacteriol. 190:5720-5728.
20. Tolker-Nielsen T, Christensen AB, Holmstrom K, Eberl L, Rasmussen TB, Sternberg C, Heydorn A, Molin S, Givskov M. 2000. Assessment of flhDC mRNA levels in Serratia liquefaciens swarm cells. J. Bacteriol. 182: 2680-2686.
21. Wang Q, Frye JG, McClelland M, Harshey RM. 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.
22. Overhage J, Bains M, Brazas MD, Hancock RE. 2008. Swarming ofPseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J. Bacteriol. 190: 2671-2679.
23. Tremblay J, Deziel E. 2010. Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 11:587. doi:10.1186/1471-2164-11-587.
24. Alberti L, Harshey RM. 1990. Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J. Bacteriol. 172:4322-4328.
25. Harshey RM, Matsuyama T. 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.
26. Chen BG, Turner L, Berg HC. 2007. The wetting agent required for swarming in Salmonella enterica serovar Typhimurium is not a surfactant. J. Bacteriol. 189:8750-8753.
27. Be'er A, Harshey RM. 2011. Collective motion of surfactant-producing bacteria imparts superdiffusivity to their upper surface. Biophys. J. 101: 1017-1024.
28. Toguchi A, Siano M, Burkart M, Harshey RM. 2000. Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
29. Harshey RM. 2010. Swarming adventures, p 163-172. In Maloy SM, Casadesus J, Hughes K (ed), The lure of bacterial genetics: a tribute to John Roth. American Society for Microbiology, Washington, DC.
30. Attmannspacher U, Scharf BE, Harshey RM. 2008. FliL is essential for swarming: motor rotation in absence of FliL fractures the flagellar rod in swarmer cells of Salmonella enterica. Mol. Microbiol. 68:328-341.
31. Motaleb MA, Pitzer JE, Sultan SZ, Liu J. 2011. A novel gene inactivation system reveals altered periplasmic flagellar orientation in a Borrelia burgdorferi fliL mutant. J. Bacteriol. 193:3324-3331.
32. Suaste-Olmos F, Domenzain C, Mireles-Rodriguez JC, Poggio S, Osorio A, Dreyfus G, Camarena L. 2010. The flagellar protein FliL is essential for swimming in Rhodobacter sphaeroides. J. Bacteriol. 192:6230-6239.
33. Wang Q, Suzuki A, Mariconda S, Porwollik S, Harshey RM. 2005. Sensing wetness: a new role for the bacterial flagellum. EMBO J. 24:2034-2042.
34. Burkart M, Toguchi A, Harshey RM. 1998. The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 95:2568-2573.
35. Manson MD. 1992. Bacterial motility and chemotaxis. Adv. Microb. Physiol. 33:277-346.
36. Mariconda S, Wang Q, Harshey RM. 2006. A mechanical role for the chemotaxis system in swarming motility. Mol. Microbiol. 60:1590-1602.
37. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, New York, NY.
38. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
39. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
40. Singer HM, Erhardt M, Steiner AM, Zhang MM, Yoshikami D, Bulaj G, Olivera BM, Hughes KT. 2012. Selective purification of recombinant neuroactive peptides using the flagellar type III secretion system. mBio. 3(3):e00115-12. doi:10.1128/mBio.00115-12.
41. Rosu V, Hughes KT. 2006. σ28-dependent transcription in Salmonella enterica is independent of flagellar shearing. J. Bacteriol. 188:5196-5203.
42. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465.
43. Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP. 2006. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355-358.
44. Walker JS. 2003. Physics: an introduction, 2nd ed. Prentice-Hall Inc., Upper Saddle River, NJ.
45. Henrichsen J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36:478-503.
46. Pruss BM, Matsumura P. 1996. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J. Bacteriol. 178:668-674.
47. Pruss BM, Markovic D, Matsumura P. 1997. The Escherichia coli flagellar transcriptional activator flhD regulates cell division through induction of the acid response gene cadA. J. Bacteriol. 179:3818-3821.
48. Akbulut M, Belman N, Golan Y, Israelachvili J. 2006. Frictional properties of confined nanorods. Adv. Mater. 18:2589-2592.
49. Darnton NC, Turner L, Rojevsky S, Berg HC. 2010. Dynamics of bacterial swarming. Biophys. J. 98:2082-2090.
50. Hosking ER, Vogt C, Bakker EP, Manson MD. 2006. The Escherichia coli MotAB proton channel unplugged. J. Mol. Biol. 364:921-937.
51. Tuson HH, Copeland MF, Carey S, Sacotte R, Weibel DB. 2013. Flagellum density regulates Proteus mirabilis swarmer cell motility in viscous environments. J. Bacteriol. 195:368-377.
52. Banaha M, Daerr A, Limat L. 2009. Spreading of liquid drops on agar gels. Eur. Phys. J. Spec. Top. 166:185-188.
53. Gygi D, Rahman MM, Lai HC, Carlson R, Guard-Petter J, Hughes C. 1995. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol. Microbiol. 17:1167-1175.
54. Lahaye E, Aubry T, Fleury V, Sire O. 2007. Does water activity rule P. mirabilis periodic swarming? II. Viscoelasticity and water balance during swarming. Biomacromolecules 8:1228-1235.
55. 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.
56. Stahl SJ, Stewart KR, Williams FD. 1983. Extracellular slime associated with Proteus mirabilis during swarming. J. Bacteriol. 154:930-937.
57. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, Fuqua C, Brun YV. 2012. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol. Microbiol. 83:41-51.
58. Pruss BM, Liu X, Hendrickson W, Matsumura P. 2001. FlhD/FlhCregulated promoters analyzed by gene array and lacZ gene fusions. FEMS Microbiol. Lett. 197:91-97.
59. Chubiz JE, Golubeva YA, Lin D, Miller LD, Slauch JM. 2010. FliZ regulates expression of the Salmonella pathogenicity island 1 invasion locus by controlling HilD protein activity in Salmonella enterica serovar Typhimurium. J. Bacteriol. 192:6261-6270.
60. Watrous J, Roach P, Alexandrov T, Heath BS, Yang JY, Kersten RD, van der Voort M, Pogliano K, Gross H, Raaijmakers JM, Moore BS, Laskin J, Bandeira N, Dorrestein PC. 2012. Mass spectral molecular networking of living microbial colonies. Proc. Natl. Acad. Sci. U. S. A. 109:E1743-E1752.
61. Hoefler BC, Gorzelnik KV, Yang JY, Hendricks N, Dorrestein PC, Straight PD. 2012. Enzymatic resistance to the lipopeptide surfactin as identified through imaging mass spectrometry of bacterial competition. Proc. Natl. Acad. Sci. U. S. A. 109:13082-13087.
62. Turner L, Zhang R, Darnton NC, Berg HC. 2010. Visualization of flagella during bacterial swarming. J. Bacteriol. 192:3259-3267.
63. Berg HC. 2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19-54.
64. Wang Q, Zhao Y, McClelland M, Harshey RM. 2007. The RcsCDB signaling system and swarming motility in Salmonella enterica serovar Typhimurium: dual regulation of flagellar and SPI-2 virulence genes. J. Bacteriol. 189:8447-8457.