Cell-cell and cell-surface interactions mediated by cellulose and a novel exopolysaccharide contribute to Pseudomonas putida biofilm formation and fitness under water-limiting conditions

Environmental Microbiology

Volumn 13, Issue 5, 2011, Pages 1342-1356

  Nielsen, Lindsey ^a   Li, Xiaohong ^b   Halverson, Larry J ^a,b  

^a Interdepartmental Graduate Program in Microbiology   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; BACTERIAL DNA; BACTERIAL POLYSACCHARIDE; CELLULOSE; GLUCURONIC ACID; HEXURONIC ACID; WATER;

ARTICLE; BIOFILM; DEHYDRATION; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; OPERON; PLANT ROOT; PSEUDOMONAS PUTIDA; RHIZOSPHERE;

ALGINATES; BIOFILMS; CELLULOSE; DEHYDRATION; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLUCURONIC ACID; HEXURONIC ACIDS; MULTIGENE FAMILY; MUTATION; OPERON; PLANT ROOTS; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS PUTIDA; RHIZOSPHERE; WATER; ZEA MAYS;

BACTERIA (MICROORGANISMS); PISUM SATIVUM; PSEUDOMONAS PUTIDA;

EID: 79955044144     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2011.02432.x     Document Type: Article

References (54)

1. Blumenkrantz, N., and Asboe-Hansen, G. (1973) New method for quantitative determination of uronic acids. Anal Biochem 54: 484-489.
2. Borlee, B.R., Goldman, A.D., Murakami, K., Samudrala, R., Wozniak, D.J., and Parsek, M.R. (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75: 827-842.
3. Byrd, M.S., Sadovskaya, I., Vinogradov, E., Lu, H., Sprinkle, A.B., Richardson, S.H., etal. (2009) Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol 73: 622-638.
4. Chang, W.-S., van de Mortel, M., Nielsen, L., Nino de Guzman, G., Li, X., and Halverson, L.J. (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol 189: 8290-8299.
5. Chang, W.-S., Li, X., and Halverson, L.J. (2009) Influence of water limitation on endogenous oxidative stress and cell death within unsaturated Pseudomonas putida biofilms. Environ Microbiol 11: 1482-1492.
6. Choi, K.-H., Choi, K.H., Schweizer, H.P., and Schweizer, H.P. (2005) An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol 5: 30.
7. Emert, G.H., Gum, J.E.K., Lang, J.A., Liu, T.H., and Brown, R.D. (1974) Cellulases. Adv Chem Ser 136: 79-100.
8. Espinosa-Urgel, M., Salido, A., and Ramos, J.-L. (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182: 2363-2369.
9. Fox, J.D., and Robyt, J.F. (1991) Miniaturization of three carbohydrate analyses using a microsample plate reader. Anal Biochem 195: 93-96.
10. Friedman, L., and Kolter, R. (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186: 4457-4465.
11. Gal, M., Preston, G.M., Massey, R.C., Spiers, A.J., and Rainey, P.B. (2003) Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces. Mol Ecol 12: 3109-3121.
12. Gjermansen, M., Nilsson, M., Yang, L., and Tolker-Nielsen, T. (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75: 815-826.
13. Gualdi, L., Tagliabue, L., Bertagnoli, S., Ierano, T., De Castro, C., and Landini, P. (2008) Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli. Microbiology 154: 2017-2024.
14. Guvener, Z.T., and Harwood, C.S. (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66: 1459-1473.
15. Heeb, S., Itoh, Y., Nishijyo, T., Schnider, U., Keel, C., Wade, J., etal. (2000) Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol Plant Microbe Interact 13: 232-237.
16. Hickman, J.W., Tifrea, D.F., and Harwood, C.S. (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102: 14422-14427.
17. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
18. Jackson, K.D., Starkey, M., Kremer, S., Parsek, M.R., and Wozniak, D.J. (2004) Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186: 4466-4475.
19. Jensen, S.E., Fecycz, I.T., and Campbell, J.N. (1980) Nutritional factors controlling exocellular protease production by Pseudomonas aeruginosa. J Bacteriol 144: 844-847.
20. Jong, W.D., Wösten, H.A.B., Dijkhuizen, L., and Claessen, D. (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73: 1128-1140.
21. Kachlany, S.C., Levery, S.B., Kim, J.S., Reuhs, B.L., Lion, L.W., and Ghiorse, W.C. (2001) Structure and carbohydrate analysis of the exopolysaccharide capsule of Pseudomonas putida G7. Environ Microbiol 3: 774-784.
22. Kader, A., Simm, R., Gerstel, U., Morr, M., and Romling, U. (2006) Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60: 602-616.
23. Lambertsen, L., Sternberg, C., and Molin, S. (2004) Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ Microbiol 6: 726-732.
24. Li, X., Nielsen, L., Nolan, C., and Halverson, L.J. (2010) Transient alginate gene expression by Pseudomonas putida biofilm residents under water-limiting conditions reflects adaptation to the local environment. Environ Microbiol 12: 1578-1590.
25. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25: 402-408.
26. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J. (2009) Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 5: e1000354.
27. Martínez-Gil, M., Yousef-Coronado, F., and Espinosa-Urgel, M. (2010) LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol Microbiol 77: 549-561.
28. Matthysse, A.G., Marry, M., Krall, L., Kaye, M., Ramey, B.E., Fuqua, C., and White, A.R. (2005) The effect of cellulose overproduction on binding and biofilm formation on roots by Agrobacterium tumefaciens. Mol Plant Microbe Interact 18: 1002-1010.
29. Matthysse, A.G., Deora, R., Mishra, M., and Torres, A.G. (2008) Polysaccharides cellulose, poly-beta-1, 6-n-acetyl-d-glucosamine, and colanic acid are required for optimal binding of Escherichia coli O157:H7 strains to alfalfa sprouts and K-12 strains to plastic but not for binding to epithelial cells. Appl Environ Microbiol 74: 2384-2390.
30. 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.
31. Merkle, R., and Poppe, I. (1994) Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol 230: 1-15.
32. Monds, R.D., Newell, P.D., Gross, R.H., and O'Toole, G.A. (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63: 656-679.
33. van de Mortel, M., and Halverson, L.J. (2004) Cell envelope components contributing to biofilm growth and survival of Pseudomonas putida in low-water-content habitats. Mol Microbiol 52: 735-750.
34. Nelson, K.E., Weinel, C., Paulsen, I.T., Dodson, R.J., Hilbert, H., Martins dos Santos, V.A., etal. (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4: 799-808.
35. Nilsson, M., Chiang, W.-C., Fazil, M., Gjermansen, M., Givskov, M., and Tolker-Nielsen, T. (2011) Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability. Environ Microbiol (in press): doi:10.1111/j.1462-2920.2011.02447.x.
36. O'Toole, G.A., and Kolter, R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449-461.
37. Priester, J.H., Olson, S.G., Webb, S.M., Neu, M.P., Hersman, L.E., and Holden, P.A. (2006) Enhanced exopolymer production and chromium stabilization in Pseudomonas putida unsaturated biofilms. Appl Environ Microbiol 72: 1988-1996.
38. Quere, B.L., and Ghigo, J.-M. (2009) BcsQ is an essential component of the Escherichia coli cellulose biosynthesis apparatus that localizes at the bacterial cell pole. Mol Microbiol 72: 724-740.
39. Ramos-Gonzalez, M.I., Campos, M.J., and Ramos, J.L. (2005) Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vitro expression technology capture and identification of root-activated promoters. J Bacteriol 187: 4033-4041.
40. Romling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62: 1234-1246.
41. Romling, U., Gomelsky, M., and Galperin, M.Y. (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57: 629-639.
42. Smibert, R.M., and Krieg, N.R. (1994) Phenotypic characterization. In Methods for General and Molecular Bacteriology. Gerhardt, P., Murray, R.G.E., Wood, W.A., and Krieg, N.R. (eds). Washington, DC, USA: American Society for Microbiology, pp. 607-654.
43. Spiers, A.J., and Rainey, P.B. (2005) The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity. Microbiology 151: 2829-2839.
44. Spiers, A.J., Bohannon, J., Gehrig, S.M., and Rainey, P.B. (2003) Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50: 15-27.
45. Starkey, M., Hickman, J.H., Ma, L., Zhang, N., De Long, S., Hinz, A., etal. (2009) Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191: 3492-3503.
46. Steinberger, R.E., and Holden, P.A. (2004) Macromolecular composition of unsaturated Pseudomonas aeruginosa biofilms with time and carbon source. Biofilms 1: 37-47.
47. Tischler, A.D., and Camilli, A. (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53: 857-869.
48. Vasseur, P., Vallet-Gely, I., Soscia, C., Genin, S., and Filloux, A. (2005) The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151: 985-997.
49. White, A.P., Gibson, D.L., Kim, W., Kay, W.W., and Surette, M.G. (2006) Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 188: 3219-3227.
50. Wozniak, D.J., Wyckoff, T.J.O., Starkey, M., Keyser, R., Azadi, P., O'Toole, G.A., and Parsek, M.R. (2003) Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci USA 100: 7907-7912.
51. York, A.G., Darvill, M., McNeil, T., Stevenson, T., and Albersheim, P. (1986) Isolation and characterization of plant-cell walls and cell-wall components. Methods Enzymol 118: 3-40.
52. Yousef-Coronado, F., Travieso, M.L., and Espinosa-Urgel, M. (2008) Different, overlapping mechanisms for colonization of abiotic and plant surfaces by Pseudomonas putida. FEMS Microbiol Lett 288: 118-124.
53. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G., and Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97: 5978-5983.
54. Zogaj, X., Nimtz, M., Rohde, M., Bokranz, W., and Romling, U. (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39: 1452-1463.