Genetic analysis of agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch

Molecular Microbiology

Volumn 89, Issue 5, 2013, Pages 929-948

  Xu, Jing ^a   Kim, Jinwoo ^b   Koestler, Benjamin J ^c   Choi, Jeong Hyeon ^a,d   Waters, Christopher M ^c   Fuqua, Clay ^a  

^a INDIANA UNIVERSITY   (United States)

^b Gyeongsang National University   (South Korea)

^c Michigan State University ^*  (United States)

^d AUGUSTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CONGO RED; CYCLIC DIGUANOSINE MONOPHOSPHATE; CYCLIC GMP; EXOPOLYSACCHARIDE; GUANYLATE CYCLASE; POLYSACCHARIDE; PROTEIN DIGUANYLATE CYCLASEA; PROTEIN DIGUANYLATE CYCLASEB; PROTEIN DIGUANYLATE CYCLASEC; UNCLASSIFIED DRUG; UNIPOLAR POLYSACCHARIDE;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CELL MOTILITY; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE ISOLATION; GENE MUTATION; GENE PRODUCT; GENETIC ANALYSIS; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RHIZOBIUM RADIOBACTER; SESSILE SPECIES; TRANSCRIPTION REGULATION; TRANSPOSON; VISN GENE; VISR GENE;

AGROBACTERIUM TUMEFACIENS;

ADHESINS, BACTERIAL; AGROBACTERIUM TUMEFACIENS; BACTERIAL ADHESION; CONGO RED; CYCLIC GMP; DNA TRANSPOSABLE ELEMENTS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LOCOMOTION; MUTAGENESIS, INSERTIONAL; POLYSACCHARIDES, BACTERIAL; STAINING AND LABELING;

EID: 84883149886     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12321     Document Type: Article

References (59)

1. Abel, S., Chien, P., Wassmann, P., Schirmer, T., Kaever, V., Laub, M.T., etal. (2011) Regulatory cohesion of cell cycle and cell differentiation through Inter linked phosphorylation and second messenger networks. Mol Cell 43: 550-560.
2. Aldridge, P., Paul, R., Goymer, P., Rainey, P., and Jenal, U. (2003) Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol Microbiol 47: 1695-1708.
3. Amikam, D., and Benziman, M. (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 171: 6649-6675.
4. Berk, V., Fong, J.C., Dempsey, G.T., Develioglu, O.N., Zhuang, X., Liphardt, J., etal. (2012) Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337: 236-239.
5. Blair, K.M., Turner, L., Winkelman, J.T., Berg, H.C., and Kearns, D.B. (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320: 1636-1638.
6. Branda, S.S., Vik, S., Friedman, L., and Kolter, R. (2005) Biofilms: the matrix revisited. Trends Microbiol 13: 20-26.
7. 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.
8. Brown, P.J., de Pedro, M.A., Kysela, D.T., Van der Henst, C., Kim, J., De Bolle, X., etal. (2012) Polar growth in the Alphaproteobacterial order Rhizobiales. Proc Natl Acad Sci USA 109: 1697-1701.
9. Cogan, N.G., and Keener, J.P. (2004) The role of the biofilm matrix in structural development. Math Med Biol 21: 147-166.
10. Colvin, K.M., Irie, Y., Tart, C.S., Urbano, R., Whitney, J.C., Ryder, C., etal. (2012) The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 14: 1913-1928.
11. D'Argenio, D.A., and Miller, S.I. (2004) Cyclic di-GMP as a bacterial second messenger. Microbiology 150: 2497-2502.
12. Danhorn, T., and Fuqua, C. (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61: 401-422.
13. Douglas, C.J., Halperin, W., and Nester, E.W. (1982) Agrobacterium tumefaciens mutants affected for attachment to plant cells. J Bacteriol 152: 1265-1275.
14. Duerig, A., Abel, S., Folcher, M., Nicollier, M., Schwede, T., Amiot, N., etal. (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23: 93-104.
15. Goodner, B., Hinkle, G., Gattung, S., Miller, N., Blanchard, M., Qurollo, B., etal. (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294: 2323-2328.
16. Hall-Stoodley, L., Costerton, J.W., and Stoodley, P. (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95-108.
17. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
18. Hibbing, M.E., and Fuqua, C. (2011) Antiparallel and interlinked control of cellular iron levels by the Irr and RirA regulators of Agrobacterium tumefaciens. J Bacteriol 193: 3461-3472.
19. Hickman, J.W., and Harwood, C.S. (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389.
20. Howie, A.J., and Brewer, D.B. (2009) Optical properties of amyloid stained by Congo red: history and mechanisms. Micron 40: 285-301.
21. Khan, S.R., Gaines, J., Roop, R.M., and Farrand, S.K. (2008) Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl Environ Microbiol 74: 5053-5062.
22. Kim, J., Heindl, J.E., and Fuqua, C. (2013) Coordination of division and development influences complex multicellular behavior in Agrobacterium tumefaciens. PLoS ONE 10: 1371.
23. Kolter, R., and Greenberg, E.P. (2006) Microbial sciences: the superficial life of microbes. Nature 441: 300-302.
24. Krasteva, P.V., Fong, J.C., Shikuma, N.J., Beyhan, S., Navarro, M.V., Yildiz, F.H., and Sondermann, H. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
25. Lampe, D.J., Akerley, B.J., Rubin, E.J., Mekalanos, J.J., and Robertson, H.M. (1999) Hyperactive transposase mutants of the Himar1 mariner transposon. Proc Natl Acad Sci USA 96: 11428-11433.
26. Lee, V.T., Matewish, J.M., Kessler, J.L., Hyodo, M., Hayakawa, Y., and Lory, S. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474-1484.
27. Li, G., Brown, P.J., 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.
28. McCarter, L., and Silverman, M. (1990) Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol Microbiol 4: 1057-1062.
29. McCarter, L., Hilmen, M., and Silverman, M. (1988) Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54: 345-351.
30. Mah, T.F., Pitts, B., Pellock, B., Walker, G.C., Stewart, P.S., and O'Toole, G.A. (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426: 306-310.
31. Massie, J.P., Reynolds, E.L., Koestler, B.J., Cong, J.P., Agostoni, M., and Waters, C.M. (2012) Quantification of high-specificity cyclic diguanylate signaling. Proc Natl Acad Sci USA 109: 12746-12751.
32. Matthysse, A.G. (1986) Initial interactions of Agrobacterium tumefaciens with plant host cells. CRC Critical Reviews in Microbiology. O'Leary, W.M. (ed). Boca Raton: CRC Press, pp. 281-307.
33. Matthysse, A.G., White, S., and Lightfoot, R. (1995) Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 177: 1069-1075.
34. Mayfield, C.I., and Inniss, W.E. (1977) A rapid, simple method for staining bacterial flagella. Can J Microbiol 23: 1311-1313.
35. Merighi, M., Lee, V.T., Hyodo, M., Hayakawa, Y., and Lory, S. (2007) The second messenger bis-(3'-5')-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65: 876-895.
36. Merritt, J.H., Ha, D.G., Cowles, K.N., Lu, W., Morales, D.K., Rabinowitz, J., etal. (2010) ) Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases. mBio 19: e00183-00181.
37. Merritt, P.M., Danhorn, T., and Fuqua, C. (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189: 8005-8014.
38. O'Toole, G.A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
39. Paul, R., Weiser, S., Amiot, N.C., Chan, C., Schirmer, T., Giese, B., and Jenal, U. (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18: 715-727.
40. Pratt, L.A., and Kolter, R. (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285-293.
41. Romling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62: 1234-1246.
42. Rotter, C., Muhlbacher, S., Salamon, D., Schmitt, R., and Scharf, B. (2006) Rem, a new transcriptional activator of motility and chemotaxis in Sinorhizobium meliloti. J Bacteriol 188: 6932-6942.
43. Ryan, R.P., Fouhy, Y., Lucey, J.F., Crossman, L.C., Spiro, S., He, Y.W., etal. (2006) Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci USA 103: 6712-6717.
44. Schirmer, T., and Jenal, U. (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735.
45. Shikuma, N.J., Fong, J.C., and Yildiz, F.H. (2012) Cellular levels and binding of c-di-GMP control subcellular localization and activity of the Vibrio cholerae transcriptional regulator VpsT. PLoS Pathog 8: e1002719.
46. Simm, R., Morr, M., Kader, A., Nimtz, M., and Römling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
47. Slater, S.C., Goldman, B.S., Goodner, B., Setubal, J.C., Farrand, S.K., Nester, E.W., etal. (2009) Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 191: 2501-2511.
48. Sondermann, H., Shikuma, N.J., and Yildiz, F.H. (2012) You've come a long way: c-di-GMP signaling. Curr Opin Microbiol 15: 140-146.
49. Sourjik, V., Muschler, P., Scharf, B., and Schmitt, R. (2000) VisN and VisR are global regulators of chemotaxis, flagellar, and motility genes in Sinorhizobium (Rhizobium) meliloti. J Bacteriol 182: 782-788.
50. Steiner, S., Lori, C., Boehm, A., and Jenal, U. (2012) Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. EMBO J 32: 354-368.
51. Sudarsan, N., Lee, E.R., Weinberg, Z., Moy, R.H., Kim, J.N., Link, K.H., and Breaker, R.R. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413.
52. Tamayo, R., Pratt, J.T., and Camilli, A. (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61: 131-148.
53. Tempe, J., Petit, A., Holsters, M., Montagu, M., and Schell, J. (1977) Thermosensitive step associated with transfer of the Ti plasmid during conjugation: possible relation to transformation in crown gall. Proc Natl Acad Sci USA 74: 2848-2849.
54. Tuckerman, J.R., Gonzalez, G., Sousa, E.H., Wan, X., Saito, J.A., Alam, M., and Gilles-Gonzalez, M.A. (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48: 9764-9774.
55. Van Larebeke, N., Engler, G., Holsters, M., Van den Elsacker, S., Zaenen, I., Schilperoort, R.A., and Schell, J. (1974) Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature 252: 169-170.
56. Watson, B., Currier, T.C., Gordon, M.P., Chilton, M.D., and Nester, E.W. (1975) Plasmid required for virulence of Agrobacterium tumefaciens. J Bacteriol 123: 255-264.
57. Weinhouse, H., Sapir, S., Amikam, D., Shilo, Y., Volman, G., Ohana, P., and Benziman, M. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-211.
58. Wu, C.F., Lin, J.S., Shaw, G.C., and Lai, E.M. (2012) Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog 8: e1002938.
59. Xu, J., Kim, J., Danhorn, T., Merritt, P.M., and Fuqua, C. (2012) Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesin biosynthesis. Res Microbiol 163: 674-684.