Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae

mBio

Volumn 5, Issue 1, 2014, Pages

  Dalia, Ankur B ^a,b   Lazinski, David W ^a,b   Camilli, Andrew ^a,b  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; MEMBRANE PROTEIN; PROTEIN TFOS; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BINDING AFFINITY; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; UPREGULATION; VIBRIO CHOLERAE;

CHITIN; DNA TRANSFORMATION COMPETENCE; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN BINDING; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE;

EID: 84903367769     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01028-13     Document Type: Article

References (31)

1. Redfield RJ. 1993. Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J. Hered. 84:400-404.
2. Chen Y, Dai J, Morris JG, Jr, Johnson JA. 2010. Genetic analysis of the capsule polysaccharide (K antigen) and exopolysaccharide genes in pandemic Vibrio parahaemolyticus O3:K6. BMC Microbiol. 10:274. http:// dx.doi.org/10.1186/1471-2180-10-274.
3. Gulig PA, Tucker MS, Thiaville PC, Joseph JL, Brown RN. 2009. User friendly cloning coupled with chitin-based natural transformation enables rapid mutagenesis of Vibrio vulnificus. Appl. Environ. Microbiol. 75:4936-4949. http://dx.doi.org/10.1128/AEM.02564-08.
4. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK. 2005. Chitin induces natural competence in Vibrio cholerae. Science 310: 1824-1827. http://dx.doi.org/10.1126/science.1120096.
5. Pollack-Berti A, Wollenberg MS, Ruby EG. 2010. Natural transformation of Vibrio fischeri requires tfoX and tfoY. Environ. Microbiol. 12: 2302-2311. http://dx.doi.org/10.1111/j.1462-2920.2010.02250.x.
6. Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR. 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45:275-283.
7. Nahar S, Sultana M, Naser MN, Nair GB, Watanabe H, Ohnishi M, Yamamoto S, Endtz H, Cravioto A, Sack RB, Hasan NA, Sadique A, Huq A, Colwell RR, Alam M. 2011. Role of shrimp chitin in the ecology of toxigenic Vibrio cholerae and cholera transmission. Front. Microbiol. 2:260. http://dx.doi.org/10.3389/fmicb.2011.00260.
8. Li X, Roseman S. 2004. The chitinolytic cascade in vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/ kinase. Proc. Natl. Acad. Sci. U. S. A. 101:627-631. http://dx.doi.org/ 10.1073/pnas.0307645100.
9. 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. http://dx.doi.org/10.1073/pnas.0308707101.
10. Antonova ES, Bernardy EE, Hammer BK. 2012. Natural competence in Vibrio cholerae is controlled by a nucleoside scavenging response that requires CytR-dependent anti-activation. Mol. Microbiol. 86:1215-1231. http://dx.doi.org/10.1111/mmi.12054.
11. Lo Scrudato M, Blokesch M. 2012. The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 8:e1002778. http://dx.doi.org/10.1371/journal.pgen.1002778.
12. Lo Scrudato M, Blokesch M. 2013. A transcriptional regulator linking quorum sensing and chitin induction to render Vibrio cholerae naturally transformable. Nucleic Acids Res. 41:3644-3658. http://dx.doi.org/ 10.1093/nar/gkt041.
13. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82. http://dx.doi.org/10.1016/j.cell.2004.06.009.
14. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 99:3129-3134. http:// dx.doi.org/10.1073/pnas.052694299.
15. van Opijnen T, Bodi KL, Camilli A. 2009. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat. Methods 6:767-772. http://dx.doi.org/10.1038/ nmeth.1377.
16. Yamamoto S, Mitobe J, Ishikawa T, Wai SN, Ohnishi M, Watanabe H, Izumiya H. 2013. Regulation of natural competence by the orphan twocomponent system sensor kinase ChiS involves a non-canonical transmembrane regulator in Vibrio cholerae. Mol. Microbiol., in press. http:// dx.doi.org/10.1111/mmi.12462.
17. Seitz P, Blokesch M. 2013. DNA-uptake machinery of naturally competent Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 110:17987-17992. http://dx.doi.org/10.1073/pnas.1315647110.
18. Yamamoto S, Izumiya H, Mitobe J, Morita M, Arakawa E, Ohnishi M, Watanabe H. 2011. Identification of a chitin-induced small RNA that regulates translation of the tfoX gene, encoding a positive regulator of natural competence in Vibrio cholerae. J. Bacteriol. 193:1953-1965. http:// dx.doi.org/10.1128/JB.01340-10.
19. Maru Y, Afar DE, Witte ON, Shibuya M. 1996. The dimerization property of glutathione S-transferase partially reactivates bcr-abl lacking the oligomerization domain. J. Biol. Chem. 271:15353-15357. http:// dx.doi.org/10.1074/jbc.271.26.15353.
20. Keyhani NO, Roseman S. 1997. Wild-type Escherichia coli grows on the chitin disaccharide, N, N=-diacetylchitobiose, by expressing the cel operon. Proc. Natl. Acad. Sci. U. S. A. 94:14367-14371. http://dx.doi.org/ 10.1073/pnas.94.26.14367.
21. Hunt DE, Gevers D, Vahora NM, Polz MF. 2008. Conservation of the chitin utilization pathway in the Vibrionaceae. Appl. Environ. Microbiol. 74:44-51. http://dx.doi.org/10.1128/AEM.01412-07.
22. Chen CY, Wu KM, Chang YC, Chang CH, Tsai HC, Liao TL, Liu YM, Chen HJ, Shen AB, Li JC, Su TL, Shao CP, Lee CT, Hor LI, Tsai SF. 2003. Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res. 13:2577-2587. http://dx.doi.org/10.1101/gr.1295503.
23. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet 361:743-749. http://dx.doi.org/10.1016/ S0140-6736(03)12659-1.
24. 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. http://dx.doi.org/ 10.1073/pnas.0409900102.
25. Yamamoto S, Morita M, Izumiya H, Watanabe H. 2010. Chitin disaccharide (GlcNAc)2 induces natural competence in Vibrio cholerae through transcriptional and translational activation of a positive regulatory gene tfoXVC. Gene 457:42-49. http://dx.doi.org/10.1016/j.gene.2010.03.003.
26. Klein BA, Tenorio EL, Lazinski DW, Camilli A, Duncan MJ, Hu LT. 2012. Identification of essential genes of the periodontal pathogen Porphyromonas gingivalis. BMC Genomics 13:578. http://dx.doi.org/10.1186/ 1471-2164-13-578.
27. Dalia AB, Lazinski DW, Camilli A. 2013. Characterization of undermethylated sites in Vibrio cholerae. J. Bacteriol. 195:2389-2399. http:// dx.doi.org/10.1128/JB.02112-12.
28. De Souza Silva O, Blokesch M. 2010. Genetic manipulation of Vibrio cholerae by combining natural transformation with FLP recombination. Plasmid 64:186-195. http://dx.doi.org/10.1016/j.plasmid.2010.08.001.
29. 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. http://dx.doi.org/10.1073/pnas.120163297.
30. Pratt JT, Ismail AM, Camilli A. 2010. PhoB regulates both environmental and virulence gene expression in Vibrio cholerae. Mol. Microbiol. 77: 1595-1605. http://dx.doi.org/10.1111/j.1365-2958.2010.07310.x.
31. Nickels BE. 2009. Genetic assays to define and characterize proteinprotein interactions involved in gene regulation. Methods 47:53-62. http://dx.doi.org/10.1016/j.ymeth.2008.10.011.