Chemoreceptor VfcA mediates amino acid chemotaxis in Vibrio fischeri

Applied and Environmental Microbiology

Volumn 79, Issue 6, 2013, Pages 1889-1896

  Brennan, Caitlin A ^a   DeLoney Marino, Cindy R ^b   Mandel, Mark J ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF SOUTHERN INDIANA   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIRECTED MUTAGENESIS; ENVIRONMENTAL STIMULI; FLAGELLAR MOTILITY; ISOLATED MUTANTS; VIBRIO FISCHERI; WILD TYPES;

BIOCHEMISTRY; GENES; MUTAGENESIS; PHYSIOLOGY;

AMINO ACIDS;

AMINO ACID; BACTERIAL PROTEIN;

AMINO ACID; BACTERIUM; CEPHALOPOD; CHEMOTAXIS; COLONIZATION; ENVIRONMENTAL CUE; MOTILITY; MUTUALISM; PLASMID;

ALIIVIBRIO FISCHERI; ARTICLE; CHEMOTAXIS; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; LOCOMOTION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSPOSON;

ALIIVIBRIO FISCHERI; AMINO ACIDS; BACTERIAL PROTEINS; CHEMOTAXIS; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; LOCOMOTION; MUTAGENESIS, INSERTIONAL; SIGNAL TRANSDUCTION;

EID: 84874806459     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03794-12     Document Type: Article

References (55)

1. Henrichsen J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol. Rev. 36:478 -503.
2. Adler J. 1966. Chemotaxis in bacteria. Science 153:708 -716.
3. Larsen SH, Reader RW, Kort EN, Tso WW, Adler J. 1974. Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature 249:74 -77.
4. Stock JB, Surette MG. 1996. Chemotaxis, p 1103-1129. In Neidhart FC, Ingraham JI, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella, 2nd ed. ASM Press, Washington, DC.
5. Bibikov SI, Biran R, Rudd KE, Parkinson JS. 1997. A signal transducer for aerotaxis in Escherichia coli. J. Bacteriol. 179:4075- 4079.
6. Hazelbauer GL, Mesibov RE, Adler J. 1969. Escherichia coli mutants defective in chemotaxis toward specific chemicals. Proc. Natl. Acad. Sci. U. S. A. 64:1300 -1307.
7. Springer MS, Goy MF, Adler J. 1977. Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins. Proc. Natl. Acad. Sci. U. S. A. 74:3312-3316.
8. Manson MD, Blank V, Brade G, Higgins CF. 1986. Peptide chemotaxis in Escherichia coli involves the Tap signal transducer and the dipeptide permease. Nature 321:253-256.
9. Kondoh H, Ball CB, Adler J. 1979. Identification of a methyl-accepting chemotaxis protein for the ribose and galactose chemoreceptors of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 76:260 -264.
10. Porter SL, Wadhams GH, Armitage JP. 2008. Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol. 16:251-260.
11. Zusman DR, Scott AE, Yang Z, Kirby JR. 2007. Chemosensory pathways, motility and development in Myxococcus xanthus. Nat. Rev. Microbiol. 5:862- 872.
12. Lacal J, Garcia-Fontana C, Munoz-Martinez F, Ramos JL, Krell T. 2010. Sensing of environmental signals: classification of chemoreceptors according to the size of their ligand binding regions. Environ. Microbiol. 12:2873-2884.
13. Krell T, Lacal J, Munoz-Martinez F, Reyes-Darias JA, Cadirci BH, Garcia-Fontana C, Ramos JL. 2011. Diversity at its best: bacterial taxis. Environ. Microbiol. 13:1115-1124.
14. Miller LD, Russell MH, Alexandre G. 2009. Diversity in bacterial chemotactic responses and niche adaptation. Adv. Appl. Microbiol. 66:53-75.
15. Alvarez-Ortega C, Harwood CS. 2007. Identification of a malate chemoreceptor in Pseudomonas aeruginosa by screening for chemotaxis defects in an energy taxis-deficient mutant. Appl. Environ. Microbiol. 73:7793- 7795.
16. Kato J, Kim HE, Takiguchi N, Kuroda A, Ohtake H. 2008. Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. J. Biosci. Bioeng. 106:1-7.
17. Taguchi K, Fukutomi H, Kuroda A, Kato J, Ohtake H. 1997. Genetic identification of chemotactic transducers for amino acids in Pseudomonas aeruginosa. Microbiology 143:3223-3229.
18. Kim HE, Shitashiro M, Kuroda A, Takiguchi N, Ohtake H, Kato J. 2006. Identification and characterization of the chemotactic transducer in Pseudomonas aeruginosa PAO1 for positive chemotaxis to trichloroethylene. J. Bacteriol. 188:6700-6702.
19. Boin MA, Hase CC. 2007. Characterization of Vibrio cholerae aerotaxis. FEMS Microbiol. Lett. 276:193-201.
20. Meibom KL, Li XB, Nielsen AT, Wu CY, Roseman S, Schoolnik GK. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. U. S. A. 101:2524 -2529.
21. Nishiyama S, Suzuki D, Itoh Y, Suzuki K, Tajima H, Hyakutake A, Homma M, Butler-Wu SM, Camilli A, Kawagishi I. 2012. Mlp24 (McpX) of Vibrio cholerae implicated in pathogenicity functions as a chemoreceptor for multiple amino acids. Infect. Immun. 80:3170 - 3178.
22. Ruby EG, Urbanowski M, Campbell J, Dunn A, Faini M, Gunsalus R, Lostroh P, Lupp C, McCann J, Millikan D, Schaefer A, Stabb E, Stevens A, Visick K, Whistler C, Greenberg EP. 2005. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Natl. Acad. Sci. U. S. A. 102:3004 -3009.
23. Mandel MJ, Stabb EV, Ruby EG. 2008. Comparative genomics-based investigation of resequencing targets in Vibrio fischeri: focus on point miscalls and artifactual expansions. BMC Genomics 9:138. doi:10.1186/1471 -2164-9-138.
24. DeLoney-Marino CR, Visick KL. 2012. Role for cheR of Vibrio fischeri in the Vibrio-squid symbiosis. Can. J. Microbiol. 58:29 -38.
25. Hussa EA, O-Shea TM, Darnell CL, Ruby EG, Visick KL. 2007. Twocomponent response regulators of Vibrio fischeri: identification, mutagenesis, and characterization. J. Bacteriol. 189:5825-5838.
26. Graf J, Dunlap PV, Ruby EG. 1994. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176:6986-6991.
27. Millikan DS, Ruby EG. 2003. FlrA, a 54-dependent transcriptional activator in Vibrio fischeri, is required for motility and symbiotic light-organ colonization. J. Bacteriol. 185:3547-3557.
28. Mandel MJ, Schaefer AL, Brennan CA, Heath-Heckman EA, DeLoney- Marino CR, McFall-Ngai MJ, Ruby EG. 2012. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78:4620-4626.
29. DeLoney-Marino CR, Wolfe AJ, Visick KL. 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.
30. Boettcher KJ, Ruby EG. 1990. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172: 3701-3706.
31. Studer SV, Mandel MJ, Ruby EG. 2008. AinS quorum sensing regulates the Vibrio fischeri acetate switch. J. Bacteriol. 190:5915-5923.
32. Dunn AK, Martin MO, Stabb EV. 2005. Characterization of pES213, a small mobilizable plasmid from Vibrio fischeri. Plasmid 54:114 -134.
33. Stabb EV, Ruby EG. 2002. RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol. 358: 413-426.
34. Caetano-Anolles G. 1993. Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl. 3:85-94.
35. O-Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R. 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310:91- 109.
36. Ruby EG, Nealson KH. 1976. Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica; a model of symbiosis based on bacterial studies. Biol. Bull. 151:574 -586.
37. Dunn AK, Millikan DS, Adin DM, Bose JL, Stabb EV. 2006. New rfpand pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl. Environ. Microbiol. 72:802- 810.
38. Naughton LM, Mandel MJ. 2012. Colonization of Euprymna scolopes squid by Vibrio fischeri. J. Vis. Exp. 61:e3758.
39. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. 2008. NCBI BLAST: a better web interface. Nucleic Acids Res. 36:W5-W9.
40. Lupp C, Ruby EG. 2005. Vibrio fischeri uses two quorum-sensing systems for the regulation of early and late colonization factors. J. Bacteriol. 187: 3620-3629.
41. Wolfe AJ, Berg HC. 1989. Migration of bacteria in semisolid agar. Proc. Natl. Acad. Sci. U. S. A. 86:6973- 6977.
42. Parales RE, Harwood CS. 2002. Bacterial chemotaxis to pollutants and plant-derived aromatic molecules. Curr. Opin. Microbiol. 5:266 -273.
43. Graf J, Ruby EG. 1998. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc. Natl. Acad. Sci. U. S. A. 95:1818 -1822.
44. Levit MN, Grebe TW, Stock JB. 2002. Organization of the receptorkinase signaling array that regulates Escherichia coli chemotaxis. J. Biol. Chem. 277:36748 -36754.
45. Zhao K, Liu M, Burgess RR. 2007. Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in Escherichia coli. Nucleic Acids Res. 35:4441- 4452.
46. Parales RE, Ditty JL, Harwood CS. 2000. Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl. Environ. Microbiol. 66:4098-4104.
47. Sonnhammer EL, Eddy SR, Durbin R. 1997. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405- 420.
48. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
49. Hanlon DW, Marquez-Magana LM, Carpenter PB, Chamberlin MJ, Ordal GW. 1992. Sequence and characterization of Bacillus subtilis CheW. J. Biol. Chem. 267:12055-12060.
50. Aravind L, Ponting CP. 1999. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176:111- 116.
51. Anantharaman V, Aravind L. 2000. Cache: a signaling domain common to animal Ca2-channel subunits and a class of prokaryotic chemotaxis receptors. Trends Biochem. Sci. 25:535-537.
52. Ulrich LE, Zhulin IB. 2005. Four-helix bundle: a ubiquitous sensory module in prokaryotic signal transduction. Bioinformatics 21(Suppl 3): iii45-iii48.
53. Shu CJ, Ulrich LE, Zhulin IB. 2003. The NIT domain: a predicted nitrate-responsive module in bacterial sensory receptors. Trends Biochem. Sci. 28:121-124.
54. Zhulin IB, Taylor BL, Dixon R. 1997. PAS domain S-boxes in Archaea, Bacteria, and sensors for oxygen and redox. Trends Biochem. Sci. 22:331- 333.
55. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.