GacA Regulates Symbiotic Colonization Traits of Vibrio fischeri and Facilitates a Beneficial Association with an Animal Host

Journal of Bacteriology

Volumn 185, Issue 24, 2003, Pages 7202-7212

  Whistler, Cheryl A ^a   Ruby, Edward G ^a  

^a UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CATALASE; HOMOSERINE; LACTONE; PROTEIN GACA; PROTEIN GACS; SEA WATER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIOLUMINESCENCE; ENZYME ACTIVITY; GENE MUTATION; LIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SQUID; SYMBIOSIS; VIBRIO FISCHERI; WILD TYPE;

4-BUTYROLACTONE; ALDEHYDES; AMINO ACIDS; ANIMALS; BACTERIAL PROTEINS; CHEMILUMINESCENT MEASUREMENTS; CLONING, MOLECULAR; DECAPODIFORMES; GENETIC COMPLEMENTATION TEST; MICROBIOLOGICAL TECHNIQUES; MUTAGENESIS; SYMBIOSIS; VIBRIO;

ANIMALIA; BACTERIA (MICROORGANISMS); CEPHALOPODA; EUPRYMNA; EUPRYMNA SCOLOPES; HAWAIIA; NEGIBACTERIA; PHOTOBACTERIUM; SCOLOPES; SEPIOLIDAE; UNCULTURED MARINE BACTERIUM; VIBRIO; VIBRIO FISCHERI;

EID: 0345097572     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.24.7202-7212.2003     Document Type: Article

References (59)

1. Aarons, S., A. Abbas, C. Adams, A. Fenton, and F. O'Gara. 2000. A regulatory RNA (prrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J. Bacteriol. 182:3913-3919.
2. Altschul, S., T. Madden, A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Ausubel, F., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1990. Current protocols in molecular biology. Wiley and Sons, Inc., New York, N.Y.
4. Beers, R. F., Jr., and I. W. Sizer. 1952. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195:133-140.
5. Blumer, C., S. Heeb, B. Pessi, and D. Haas. 1999. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc. Natl. Acad. Sci. USA 96: 14073-14078.
6. Boettcher, K. J., and E. G. Ruby. 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172: 1053-1058.
7. Boettcher, K. J., and E. G. Ruby. 1995. Detection and quantification of Vibrio fischeri autoinducer from symbiotic squid light organs. J. Bacteriol. 177: 1053-1058.
8. Castaneda, M., J. Sanchez, S. Moreno, C. Nunez, and G. Espin. 2001. The global regulators GacA and sigma S form part of a cascade that controls alginate production in Azotobacter vinelandii. J. Bacteriol. 183:6787-6793.
9. Chancey, S. T., D. W. Wood, and L. S. Pierson III. 1999. Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens. Appl. Environ. Microbiol. 65:2294-2299.
10. Chancey, S. T., D. W. Wood, E. A. Pierson, and L. S. Pierson III. 2002. Survival of GacS/GacA mutants of the biological control bacterium Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. Appl. Environ. Microbiol. 68:3308-3314.
11. Corbell, N. A., and J. E. Loper. 1995. A global regulator of secondary metabolite production in Pseudomonas fluorescens Pf-5. J. Bacteriol. 177: 6230-6236.
12. Cui, Y., A. Chatterjee, and A. K. Chatterjee. 2001. Effects of the two-component system comprising GacA and GacS of Erwinia carotovora subsp. carotovora on the production of global regulatory rsmB RNA, extracellular enzymes, and HarpinEcc. Mol. Plant Microbe Interact. 14:516-526.
13. DeLoney-Marino, C. R., C. R. Wolfe, and K. L. Visick. Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl. Environ. Microbiol., in press.
14. Duffy, V. K., and G. Defago. 2000. Controlling instability in gacS-gacA regulatory genes during inoculate production of Pseudomonas fluorescens biocontrol strains. Mol. Plant Microbe Interact. 66:3142-3150.
15. Eriksson, A. R. B., R. A. Andersson, M. Pirhonen, and E. T. Palva. 1998. Two-component regulators involved in the global control of virulence in Erwinia carotovora subsp. carotovora. Mol. Plant Microbe Interact. 8:743-752.
16. Flavier, A. B., L. M. Ganova-Raeva, M. A. Schell, and T. P. Denny. 1997. Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179:7089-7097.
17. Goodier, R. I., and B. M. M. Ahmer. 2001. SirA orthologs affect both motility and virulence. J. Bacteriol. 183:2249-2258.
18. 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.
19. Graf, J., and E. G. Ruby. 2000. Novel effects of a transposon insertion in the Vibrio fischeri gInD gene: defects in iron uptake and symbiotic persistence in addition to nitrogen utilization. Mol. Microbiol. 37:168-179.
20. Graf, J., and E. G. Ruby. 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl. Acad. Sci. USA 95:1818-1822.
21. Hammer, B. K., E. S. Tateda, and M. S. Swanson. 2002. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 44:107-118.
22. Heeb, S., and D. Haas. 2001. Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol. Plant Microbe Interact. 14:1351-1363.
23. Heeb, S., C. Blumer, and D. Haas. 2002. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHAO. J. Bacteriol. 184:1046-1056.
24. Herrero, M., V. de Lorenzo, and K. N. Timmis. 1990. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
25. Hyytiainen, H., M. Montesano, and E. T. Palva. 2001. Global regulators ExpA (GacA) and KdgR modulate extracellular enzyme gene expression through the RsmA-RsmB system in Erwinia carotovora subsp. carotovora. Mol. Plant Microbe Interact. 14:931-938.
26. Kinscherf, T. G., and D. K. Willis. 1999. Swarming by Pseudomonas syringea B728a requires gacS (lemA) and gacA but not the acyl-homoserine lactone biosynthetic gene ahll. J. Bacteriol. 181:4133-4136.
27. Lawhon, S. D., R. Maurer, M. Suyemoto, and C. Altier. 2002. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46:1451-1464.
28. Lee, K. H., and E. G. Ruby. 1994. Competition between Vibrio fischeri strains during initiation and maintenance of a light organ symbiosis. J. Bacteriol. 176:1985-1991.
29. Lee, K. H., and E. G. Ruby. 1994. Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl. Environ. Microbiol. 60:1565-1571.
30. Lee, K. H., and E. G. Ruby. 1995. Symbiotic role of the viable but nonculturable state of Vibrio fischeri in Hawaiian coastal seawater. Appl. Environ. Microbiol. 61:278-283.
31. Lund, A. H., M. Dutch, and F. S. Pedersen. 1996. Increased cloning efficiency by temperature-cycle ligation. Nucleic Acids Res. 24:800-801.
32. Lupp, C., M. Urbanowski, E. P. Greenberg, and E. G. Ruby. 2003. The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol. Microbiol. 50:319-331.
33. McCann, J., E. V. Stabb, D. S. Millikan, and E. G. Ruby. 2003. Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl. Environ. Microbiol. 69:5928-5934.
34. Meighen, E. A., and P. V. Dunlap. 1993. Physiological, biochemical and genetic control of bacterial bioluminescence. Adv. Microb. Physiol. 34:1-67.
35. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
36. 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.
37. Mukhopadhyay, S., J. P. Audia, R. N. Roy, and H. E. Schellhorn. 2000. Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol. Microbiol. 37:371-381.
38. Nyholm, S. V., B. Deplancke, H. R. Gaskins, M. A. Apicella, and M. J. McFall-Ngai. 2002. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68:5113-5122.
39. Pearson, J. P., K. M. Gray, L. Passador, K. D. Tucker, A. Eberhard, B. H. Iglewski, and E. P. Greenberg. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91:197-201.
40. Pernestig, A. K., S. J. Normark, D. M. Georgellis, and O. Melefors. 2000. The role of the AirS two-component system in uropathogenic Escherichia coli. Adv. Exp. Med. Biol. 485:137-142.
41. Pernestig, A.-K., D. Georgellis, T. Romeo, K. Suzuki, H. Tomenius, S. Normark, and O. Melefors. 2003. The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J. Bacteriol. 185:843-853.
42. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
43. Reimmann, C., M. Beyeler, M. Latifi, H. Winteler, M. Foglino, A. Lazdunski, and D. Hass. 1997. The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol. Microbiol. 24:309-319.
44. Ruby, E. G., and L. M. Asato. 1993. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbioses. Arch. Microbiol. 159:160-167.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
46. Schaefer, A. L., B. L. Hanselka, M. R. Parsek, and E. P. Greenberg. 2000. Detection, purification, and structural elucidation of the acylhomoserine lactone inducer of Vibrio fischeri luminescence and other related molecules. Methods Enzymol. 305:288-301.
47. 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.
48. Stewart, B. J., and L. L. McCarter. 2003. Lateral flagellar gene systems of Vibrio parahaemolyticus. J. Bacteriol. 185:4508-4518.
49. Suzuki, K., X. Wang, T. Weilbacher, A.-K. Pernestig, O. Melefors, D. Georgellis, P. Babitzke, and T. Romeo. 2002. Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J. Bacteriol. 184: 5130-5140.
50. Visick, K. L., and E. G. Ruby. 1997. New genetic tools for use in the marine bioluminescent bacterium Vibrio fischeri, p. 119-122. In J. W. Hastings, L. J. Kricka, and P. E. Stanley (ed.), Bioluminescence and chemiluminescence. John Wiley & Sons, New York, N.Y.
51. Visick, K. L., and E. G. Ruby. TnluxAB insertion mutants of Vibrio fischeri with symbiosis-regulated phenotypes. Nova Acta Leopold., in press.
52. Visick, K. L., J. Foster, J. Doino, M. McFall-Ngai, and E. G. Ruby. 2000. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182:4578-4586.
53. Visick, K. L., and M. J. McFall-Ngai. 2000. An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J. Bacteriol. 182:1779-1787.
54. Visick, K. L., and E. G. Ruby. 1998. The periplasmic group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and by approach to stationary phase. J. Bacteriol. 180:2087-2092.
55. s and the stress response in Pseudomonas fluorescens Pf-5. J. Bacteriol. 180:6635-6641.
56. Wong, S. M., P. A. Carroll, L. G. Rahme, F. M. Ausubel, and S. B. Calderwood. 1998. Modulation of expression of the ToxR regulon in Vibrio cholerae by a member of the two-component family of response regulators. Infect. Immun. 66:5854-5861.
57. Zambrano, M. M., and R. Kolter. 1996. GASPing for life in stationary phase. Cell 86:181-184.
58. Zambrano, M. M., D. A. Siegele, M. Almiron, A. Tormo, and R. Kolter. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760.
59. Zinser, E. R., and R. Kolter. 1999. Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J. Bacteriol. 181:5800-5807.