Genetic determinants of swimming motility in the squid light-organ symbiont Vibrio fischeri

MicrobiologyOpen

Volumn 2, Issue 4, 2013, Pages 576-594

  Brennan, Caitlin A ^a   Mandel, Mark J ^a   Gyllborg, Mattias C ^a   Thomasgard, Krista A ^a   Ruby, Edward G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Chemotaxis; Euprymna scolopes; Flagellar motility; Symbiosis

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIUM IDENTIFICATION; BACTERIUM MUTANT; CELL DIVISION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; EUPRYMNA SCOLOPES; FLIL1 GENE; FLIL2 GENE; FLRA GENE; GENE CONTROL; GENE EXPRESSION; GENE INSERTION; GENETIC IDENTIFICATION; GENETIC SCREENING; GENETIC TRANSCRIPTION; JUVENILE ANIMAL; MOTA1 GENE; MOTA2 GENE; MOTB1 GENE; MOTB2 GENE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; REGULON; SQUID; SWIMMING; SYMBIONT; TRANSPOSON; VIBRIO FISCHERI;

CHEMOTAXIS; EUPRYMNA SCOLOPES; FLAGELLAR MOTILITY; SYMBIOSIS;

ALIIVIBRIO FISCHERI; ANIMAL STRUCTURES; ANIMALS; BACTERIOLOGICAL TECHNIQUES; CHEMOTAXIS; CULTURE MEDIA; DECAPODIFORMES; FLAGELLA; GENES, BACTERIAL; LOCOMOTION; MUTAGENESIS, INSERTIONAL; MUTATION; SYMBIOSIS;

BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA SCOLOPES; SEPIOLIDAE; VIBRIO FISCHERI;

EID: 84897108716     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.96     Document Type: Article

References (86)

1. Adler, J. 1966. Chemotaxis in bacteria. Science 153:708-716.
2. Allen, R. D., and P. Baumann . 1971. Structure and arrangement of flagella in species of the genus Beneckea and Photobacterium fischeri. J. Bacteriol. 107:295-302.
3. Arnosti, D. N., and M. J. Chamberlin . 1989. Secondary σ factor controls transcription of flagellar and chemotaxis genes in Escherichia coli. Proc. Natl Acad. Sci. USA 86:830-834.
4. Baldi, P., and A. D. Long . 2001. A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics 17:509-519.
5. Boettcher, K. J., and E. G. Ruby . 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172:3701-3706.
6. Brennan, C. A., C. R. DeLoney-Marino, and M. J. Mandel . 2013. Chemoreceptor VfcA mediates amino acid chemotaxis in Vibrio fischeri. Appl. Environ. Microbiol. 79:1889-1896.
7. Butler, S. M., and A. Camilli . 2004. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl Acad. Sci. USA 101:5018-5023.
8. Caetano-Anolles, G. 1993. Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl. 3:85-94.
9. Cameron, D. E., J. M. Urbach, and J. J. Mekalanos . 2008. A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae. Proc. Natl Acad. Sci. USA 105:8736-8741.
10. Case, R. B., Y. P. Chang, S. B. Smith, J. Gore, N. R. Cozzarelli, and C. Bustamante . 2004. The bacterial condensing MukBEF compacts DNA into a repetitive, stable structure. Science 305:222-227.
11. Correa, N. E., F. Peng, and K. E. Klose . 2005. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J. Bacteriol. 187:6324-6332.
12. Cullen, T. W., and M. S. Trent . 2010. A link between the assembly of flagella and lipooligosaccharide of the Gram-negative bacterium Campylobacter jejuni. Proc. Natl Acad. Sci. USA 107:5160-5165.
13. Dam, P., V. Olman, K. Harris, Z. Su, and Y. Xu . 2007. Operon prediction using both genome-specific and general genomic information. Nucleic Acids Res. 35:288-298.
14. DeLoney-Marino, C. R., and K. L. Visick . 2012. Role for cheR of Vibrio fischeri in the Vibrio-squid symbiosis. Can. J. Microbiol. 58:29-38.
15. DeLoney-Marino, C. R., A. J. Wolfe, and K. L. Visick . 2003. Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl. Environ. Microbiol. 69:7527-7530.
16. Dunn, A. K., and E. V. Stabb . 2008. Genetic analysis of trimethylamine N-oxide reductases in the light organ symbiont Vibrio fischeri ES114. J. Bacteriol. 190:5814-5823.
17. Dunn, A. K., M. O. Martin, and E. V. Stabb . 2005. Characterization of pES213, a small mobilizable plasmid from Vibrio fischeri. Plasmid 54:114-134.
18. Dunn, A. K., D. S. Millikan, D. M. Adin, J. L. Bose, and E. V. Stabb . 2006. New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl. Environ. Microbiol. 72:802-810.
19. Freter, R., B. Allweiss, P. C. O'Brien, S. A. Halstead, and M. S. Macsai . 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vitro studies. Infect. Immun. 34:241-249.
20. Frye, J., J. E. Karlinsey, H. R. Felise, B. Marzolf, N. Dowidar, M. McClelland, et al. 2006. Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:2233-2243.
21. Gage, D. J., T. Bobo, and S. R. Long . 1996. Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J. Bacteriol. 178:7159-7166.
22. Girgis, H. S., Y. Liu, W. S. Ryu, and S. Tavazoie . 2007. A comprehensive genetic characterization of bacterial motility. PLoS Genet. 3:1644-1660.
23. Graf, J., P. V. Dunlap, and E. G. Ruby . 1994. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176:6986-6991.
24. Hayashi, F., K. D. Smith, A. Ozinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, et al. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103.
25. Henrichsen, J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36:478-503.
26. Hussa, E. A., T. M. O'Shea, C. L. Darnell, E. G. Ruby, and K. L. Visick . 2007. Two-component response regulators of Vibrio fischeri: identification, mutagenesis, and characterization. J. Bacteriol. 189:5825-5838.
27. Iino, T., Y. Komeda, K. Kutsukake, R. M. Macnab, P. Matsumura, J. S. Parkinson, et al. 1988. New unified nomenclature for the flagellar genes of Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 52:533-535.
28. Kapatral, V., J. W. Campbell, S. A. Minnich, N. R. Thomson, P. Matsumura, and B. M. Pruss . 2004. Gene array analysis of Yersinia enterocolitica FlhD and FlhC: regulation of enzymes affecting synthesis and degradation of carbamoylphosphate. Microbiology 150(Pt 7):2289-2300.
29. Kim, Y. K., and L. L. McCarter . 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182:3693-3704.
30. Klose, K. E., and J. J. Mekalanos . 1998a. Differential regulation of multiple flagellins in Vibrio cholerae. J. Bacteriol. 180:303-316.
31. Klose, K. E., and J. J. Mekalanos . 1998b. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28:501-520.
32. Lane, M. C., V. Lockatell, G. Monterosso, D. Lamphier, J. Weinert, J. R. Hebel, et al. 2005. Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect. Immun. 73:7644-7656.
33. Lemon, K. P., D. E. Higgins, and R. Kolter . 2007. Flagellar motility is critical for Listeria monocytogenes biofilm formation. J. Bacteriol. 189:4418-4424.
34. Letunic, I., T. Doerks, and P. Bork . 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:302-305.
35. Liu, Z., T. Miyashiro, A. Tsou, A. Hsiao, M. Goulian, and J. Zhu . 2008. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc. Natl Acad. Sci. USA 105:9769-9774.
36. Lyell, N. L., A. K. Dunn, J. L. Bose, S. L. Vescovi, and E. V. Stabb . 2008. Effective mutagenesis of Vibrio fischeri by using hyperactive mini-Tn5 derivatives. Appl. Environ. Microbiol. 74:7059-7063.
37. Macnab, R. M. 1996. Flagella and motility. Pp. 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 andH. E. Umbarger eds. Escherichia coli and Salmonella typhimurium. ASM Press, Washington, D.C.
38. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
39. Mandel, M. J., E. V. Stabb, and E. G. Ruby . 2008. Comparative genomics-based investigation of resequencing targets in Vibrio fischeri: focus on point miscalls and artefactual expansions. BMC Genomics 9:138.
40. Mandel, M. J., A. L. Schaefer, C. A. Brennan, E. A. Heath-Heckman, C. R. Deloney-Marino, M. J. McFall-Ngai, et al. 2012. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78:4620-4626.
41. Martinez, R. M., M. N. Dharmasena, T. J. Kirn, and R. K. Taylor . 2009. Characterization of two outer membrane proteins, FlgO and FlgP, that influence Vibrio cholerae motility. J. Bacteriol. 191:5669-5679.
42. McCarter, L. L. 1995. Genetic and molecular characterization of the polar flagellum of Vibrio parahaemolyticus. J. Bacteriol. 177:1595-1609.
43. McCarter, L. 2006. Motility and chemotaxis. Pp. 115-132 in F. L. Thompson, B. Austin and J. Swings, eds. The biology of Vibrios. ASM Press, Washington, D.C.
44. McCarter, L., and M. Silverman . 1990. Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol. Microbiol. 4:1057-1062.
45. Miller, L. D., M. H. Russell, and G. Alexandre . 2009. Diversity in bacterial chemotactic responses and niche adaptation. Adv. Appl. Microbiol. 66:53-75.
46. Millikan, D. S., and E. G. Ruby . 2002. Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects. Appl. Environ. Microbiol. 68:2519-2528.
47. 54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J. Bacteriol. 185:3547-3557.
48. Millikan, D. S., and E. G. Ruby . 2004. Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization. J. Bacteriol. 186:4315-4325.
49. Milton, D. L., R. O'Toole, P. Horstedt, and H. Wolf-Watz . 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
50. Moisi, M., C. Jenul, S. M. Butler, A. New, S. Tutz, J. Reidl, et al. 2009. A novel regulatory protein involved in motility of Vibrio cholerae. J. Bacteriol. 191:7027-7038.
51. Morris, D. C., F. Peng, J. R. Barker, and K. E. Klose . 2008. Lipidation of an FlrC-dependent protein is required for enhanced intestinal colonization by Vibrio cholerae. J. Bacteriol. 190:231-239.
52. Naughton, L. M., and M. J. Mandel . 2012. Colonization of Euprymna scolopes squid by Vibrio fischeri. J. Vis. Exp. 61:e3758.
53. Nyholm, S. V., and M. J. McFall-Ngai . 2004. The winnowing: establishing the squid-vibrio symbiosis. Nat. Rev. Microbiol. 2:632-642.
54. Nyholm, S. V., E. V. Stabb, E. G. Ruby, and M. J. McFall-Ngai . 2000. Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl Acad. Sci. USA 97:10231-10235.
55. O'Toole, G. A., L. A. Pratt, P. I. Watnick, D. K. Newman, V. B. Weaver, and R. Kolter . 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310:91-109.
56. Overhage, J., S. Lewenza, A. K. Marr, and R. E. Hancock . 2007. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J. Bacteriol. 189:2164-2169.
57. Peterson, J. D., L. A. Umayam, T. Dickinson, E. K. Hickey, and O. White . 2001. The comprehensive microbial resource. Nucleic Acids Res. 29:123-125.
58. Post, D. M., L. Yu, B. C. Krasity, B. Choudhury, M. J. Mandel, C. A. Brennan, et al. 2012. O-antigen and core carbohydrate of Vibrio fischeri lipopolysaccharide: composition and analysis of their role in Euprymna scolopes light organ colonization. J. Biol. Chem. 287:8515-8530.
59. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
60. Pruss, B. M., J. W. Campbell, T. K. Van Dyk, C. Zhu, Y. Kogan, and P. Matsumura . 2003. FlhD/FlhC is a regulator of anaerobic respiration and the Entner-Doudoroff pathway through induction of the methyl-accepting chemotaxis protein Aer. J. Bacteriol. 185:534-543.
61. Punta, M., P. C. Coggill, R. Y. Eberhardt, J. Mistry, J. Tate, C. Boursnell, et al. 2012. The Pfam protein families database. Nucleic Acids Res. 40:290-301.
62. Rashid, M. H., C. Rajanna, A. Ali, and D. K. Karaolis . 2003. Identification of genes involved in the switch between the smooth and rugose phenotypes of Vibrio cholerae. FEMS Microbiol. Lett. 227:113-119.
63. Rawls, J. F., M. A. Mahowald, A. L. Goodman, C. M. Trent, and J. I. Gordon . 2007. In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc. Natl Acad. Sci. USA 104:7622-7627.
64. Richardson, K. 1991. Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect. Immun. 59:2727-2736.
65. Rolig, A. S., J. Shanks, J. E. Carter, and K. M. Ottemann . 2012. Helicobacter pylori requires TlpD-driven chemotaxis to proliferate in the antrum. Infect. Immun. 80:3713-3720.
66. Ruby, E. G., and L. M. Asato . 1993. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch. Microbiol. 159:160-167.
67. Ruby, E. G., M. Urbanowski, J. Campbell, A. Dunn, M. Faini, R. Gunsalus, et al. 2005. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Natl Acad. Sci. USA 102:3004-3009.
68. Sanders, D. A., B. Mendez, and D. E., Jr. Koshland . 1989. Role of the CheW protein in bacterial chemotaxis: overexpression is equivalent to absence. J. Bacteriol. 171:6271-6278.
69. Sassetti, C. M., D. H. Boyd, and E. J. Rubin . 2001. Comprehensive identification of conditionally essential genes in mycobacteria. Proc. Natl Acad. Sci. USA 98:12712-12717.
70. Shinoda, S., and K. Okamoto . 1977. Formation and function of Vibrio parahaemolyticus lateral flagella. J. Bacteriol. 129:1266-1271.
71. Slauch, J. M., and T. J. Silhavy . 1991. cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J. Bacteriol. 173:4039-4048.
72. Sommerlad, S. M., and D. R. Hendrixson . 2007. Analysis of the roles of FlgP and FlgQ in flagellar motility of Campylobacter jejuni. J. Bacteriol. 189:179-186.
73. Stabb, E. V., and E. G. Ruby . 2002. RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol. 358:413-426.
74. Studer, S. V., M. J. Mandel, and E. G. Ruby . 2008. AinS quorum sensing regulates the Vibrio fischeri acetate switch. J. Bacteriol. 190:5915-5923.
75. Syed, K. A., S. Beyhan, N. Correa, J. Queen, J. Liu, F. Peng, et al. 2009. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J. Bacteriol. 191:6555-6570.
76. Uehara, T., K. R. Parzych, T. Dinh, and T. G. Bernhardt . 2010. Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J. 29:1412-1422.
77. Visick, K. L., and E. G. Ruby . 2006. Vibrio fischeri and its host: it takes two to tango. Curr. Opin. Microbiol. 9:632-638.
78. Wang, Y., Y. S. Dufour, H. K. Carlson, T. J. Donohue, M. A. Marletta, and E. G. Ruby . 2010. H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc. Natl Acad. Sci. USA 107:8375-8380.
79. Wier, A. M., S. V. Nyholm, M. J. Mandel, R. P. Massengo-Tiasse, A. L. Schaefer, I. Koroleva, et al. 2010. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Natl Acad. Sci. USA 107:2259-2264.
80. Wilhelms, M., S. Vilches, R. Molero, J. G. Shaw, J. M. Tomas, and S. Merino . 2009. Two redundant sodium-driven stator motor proteins are involved in Aeromonas hydrophila polar flagellum rotation. J. Bacteriol. 191:2206-2217.
81. Wolfe, A. J., and H. C. Berg . 1989. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. USA 86:6973-6977.
82. 54 controls motility, biofilm formation, luminescence, and colonization. Appl. Environ. Microbiol. 70:2520-2524.
83. Wright, K. J., P. C. Seed, and S. J. Hultgren . 2005. Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect. Immun. 73:7657-7668.
84. Yamazoe, M., T. Onogi, Y. Sunako, H. Niki, K. Yamanaka, T. Ichimura, et al. 1999. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J. 18:5873-5884.
85. Young, G. M., D. H. Schmiel, and V. L. Miller . 1999. 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 96:6456-6461.
86. Zhao, K., M. Liu, and R. R. Burgess . 2007. Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli. Nucleic Acids Res. 35:4441-4452.