The adhesive and cohesive properties of a bacterial polysaccharide adhesin are modulated by a deacetylase

Molecular Microbiology

Volumn 88, Issue 3, 2013, Pages 486-500

  Wan, Zhe ^a   Brown, Pamela J B ^a,b   Elliott, Ellen N ^a,c   Brun, Yves V ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL ENZYME; BACTERIAL POLYSACCHARIDE; EXOPOLYSACCHARIDE; HOLDFAST; POLYSACCHARIDE DEACETYLASE; UNCLASSIFIED DRUG;

ALPHAPROTEOBACTERIA; ARTICLE; ASTICCACAULIS BIPROSTHECUM; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOFILM; CARBOHYDRATE SYNTHESIS; CAULOBACTER CRESCENTUS; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENE DISRUPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SITE DIRECTED MUTAGENESIS; SUPERNATANT;

ADHESINS, BACTERIAL; AMIDOHYDROLASES; BACTERIAL ADHESION; BIOFILMS; BLOTTING, WESTERN; CAULOBACTER CRESCENTUS; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; PLASMIDS; POLYSACCHARIDES, BACTERIAL; SEQUENCE DELETION;

ASTICCACAULIS BIPROSTHECIUM; BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES;

EID: 84876699602     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12199     Document Type: Article

References (48)

1. Berne, C., Kysela, D.T., and Brun, Y.V. (2010) A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Mol Microbiol 77: 815-829.
2. Blair, D.E., and van Aalten, D.M.F. (2004) Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetyl-glucosamine. FEBS Lett 570: 13-19.
3. Blair, D.E., Schuttelkopf, A.W., MacRae, J.I., and van Aalten, D.M.F. (2005) Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proc Natl Acad Sci USA 102: 15429-15434.
4. Blair, D.E., Hekmat, O., Schuttelkopf, A.W., Shrestha, B., Tokuyasu, K., Withers, S.G., and van Aalten, D.M. (2006) Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry 45: 9416-9426.
5. Bodenmiller, D., Toh, E., and Brun, Y.V. (2004) Development of surface adhesion in Caulobacter crescentus. J Bacteriol 186: 1438-1447.
6. Brown, P.J., Hardy, G.G., Trimble, M.J., and Brun, Y.V. (2009) Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv Microb Physiol 54: 1-101
7. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
8. Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-D238.
9. Caufrier, F., Martinou, A., Dupont, C., and Bouriotis, V. (2003) Carbohydrate esterase family 4 enzymes: substrate specificity. Carbohydr Res 338: 687-692.
10. Cerca, N., Jefferson, K.K., Maira-Litran, T., Pier, D.B., Kelly-Quintos, C., Goldmann, D.A., etal. (2007) Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun 75: 3406-3413.
11. Chertkov, O., Brown, P.J., Kysela, D.T., de Pedro, M.A., Lucas, S., Copeland, A., etal. (2011) Complete genome sequence of Hirschia baltica type strain (IFAM 1418(T)). Stand Genomic Sci 5: 287-297.
12. Cole, J.L., Hardy, G.G., Bodenmiller, D., Toh, E., Hinz, A., and Brun, Y.V. (2003) The HfaB and HfaD adhesion proteins of Caulobacter crescentus are localized in the stalk. Mol Microbiol 49: 1671-1683.
13. Cuthbertson, L., Mainprize, I.L., Naismith, J.H., and Whitfield, C. (2009) Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol Mol Biol Rev 73: 155-177.
14. Donlan, R.M. (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8: 881-890.
15. Dunne, W.M. (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155-166.
16. Ely, B. (1979) Transfer of drug resistance factors to the dimorphic bacterium Caulobacter crescentus. Genetics 91: 371-380.
17. Ely, B. (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204: 372-384.
18. Entcheva-Dimitrov, P., and Spormann, A.M. (2004) Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. J Bacteriol 186: 8254-8266.
19. Haag, A.P. (2006) Mechanical Properties of Bacterial Exopolymeric Adhesives and Their Commercial Development Biological Adhesives. Smith, A.M., and Callow, J.A. (eds). Heidelberg, Germany: Springer-Verlag, pp. 1-19.
20. Hardy, G.G., Allen, R.C., Toh, E., Long, M., Brown, P.J.B., Cole-Tobian, J.L., and Brun, Y.V. (2010) A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol Microbiol 76: 409-427.
21. Hassan, S., and Hugouvieux-Cotte-Pattat, N. (2011) Identification of two feruloyl esterases in Dickeya dadantii 3937 and induction of the major feruloyl esterase and of pectate lyases by ferulic acid. J Bacteriol 193: 963-970.
22. Heilmann, C., Schweitzer, O., Gerke, C., Vanittanakom, N., Mack, D., and Gotz, F. (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20: 1083-1091.
23. Itoh, Y., Rice, J.D., Goller, C., Pannuri, A., Taylor, J., Meisner, J., etal. (2008) Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1, 6-N-acetyl-D-glucosamine. J Bacteriol 190: 3670-3680.
24. Kurtz, J.D., Jr, and Smith, J. (1994) The Caulobacter crescentus holdfast: identification of holdfast attachment complex genes. FEMS Microbiol Lett 116: 175-182.
25. Larson, R.J., and Pate, J.L. (1975) Growth and morphology of Asticcacaulis biprosthecum in defined media. Arch Microbiol 106: 147-157.
26. Levano-Garcia, J., Verjovski-Almeida, S., and da Silva, A.C. (2005) Mapping transposon insertion sites by touchdown PCR and hybrid degenerate primers. Biotechniques 38: 225-229.
27. Levi, A., and Jenal, U. (2006) Holdfast formation in motile swarmer cells optimizes surface attachment during Caulobacter crescentus development. J Bacteriol 188: 5315-5318.
28. Li, G., Smith, C.S., Brun, Y.V., and Tang, J.X. (2005) The elastic properties of the Caulobacter crescentus adhesive holdfast are dependent on oligomers of N-acetylglucosamine. J Bacteriol 187: 257-265.
29. Li, G., Brown, P.J.B., Tang, J.X., Xu, J., Quardokus, E.M., Fuqua, C., and Brun, Y.V. (2012) Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol 83: 41-51.
30. Merker, R.I., and Smit, J. (1988) Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl Environ Microbiol 54: 2078-2085.
31. Neu, T.R. (1992) Microbial 'footprints' and the general ability of microorganisms to label interfaces. Can J Microbiol 38: 1005-1008.
32. Notredame, C., Higgins, D.G., and Heringa, J. (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
33. Poindexter, J.S. (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28: 231-295.
34. Ridout, M.J., Brownsey, G.J., York, G.M., Walker, G.C., and Morris, V.J. (1997) Effect of o-acyl substituents on the functional behaviour of Rhizobium meliloti succinoglycan. Int J Biol Macromol 20: 1-7.
35. Rinaudo, M. (2004) Role of substituents on the properties of some polysaccharides. Biomacromolecules 5: 1155-1165.
36. Rubin, E.J., Akerley, B.J., Novik, V.N., Lampe, D.J., Husson, R.N., and Mekalanos, J.J. (1999) In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc Natl Acad Sci USA 96: 1645-1650.
37. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
38. Smith, C.S., Hinz, A., Bodenmiller, D., Larson, D.E., and Brun, Y.V. (2003) Identification of genes required for synthesis of the adhesive holdfast in Caulobacter crescentus. J Bacteriol 185: 1432-1442.
39. Sorlier, P., Denuzière, A., Viton, C., and Domard, A. (2001) Relation between the degree of acetylation and the electrostatic properties of chitin and chitosan. Biomacromolecules 2: 765-772.
40. Tielen, P., Strathmann, M., Jaeger, K.-E., Flemming, H.-C., and Wingender, J. (2005) Alginate acetylation influences initial surface colonization by mucoid Pseudomonas aeruginosa. Microbiol Res 160: 165-176.
41. Toh, E., Kurtz, H.D., and Brun, Y.V. (2008) Characterization of the Caulobacter crescentus holdfast polysaccharide biosynthesis pathway reveals significant redundancy in the initiating glycosyltransferase and polymerase steps. J Bacteriol 190: 7219-7231.
42. Tsang, P.H., Li, G., Brun, Y.V., Freund, L.B., and Tang, J.X. (2006) Adhesion of single bacterial cells in the micronewton range. Proc Natl Acad Sci USA 103: 5764-5768.
43. Vigeant, M.A., Ford, R.M., Wagner, M., and Tamm, L.K. (2002) Reversible and irreversible adhesion of motile Escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy. Appl Environ Microbiol 68: 2794-2801.
44. Villain-Simonnet, A., Milas, M., and Rinaudo, M. (2000) A new bacterial polysaccharide (YAS34). I. Characterization of the conformations and conformational transition. Int J Biol Macromol 27: 65-75.
45. Viollier, P.H., Sternheim, N., and Shapiro, L. (2002) A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J 21: 4420-4428.
46. Vuong, C., Kocianova, S., Voyich, J.M., Yao, Y., Fischer, E.R., DeLeo, F.R., and Otto, M. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279: 54881-54886.
47. Waters, D.M., Murray, P.G., Miki, Y., Martínez, A.T., Tuohy, M.G., and Faulds, C.B. (2012) Cloning, overexpression in Escherichia coli, and characterization of a thermostable fungal acetylxylan esterase from Talaromyces emersonii. Appl Environ Microbiol 78: 3759-3762.
48. Zhao, Y., Park, R.D., and Muzzarelli, R.A. (2010) Chitin deacetylases: properties and applications. Mar Drugs 8: 24-46.