Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Robledo, M ^a,e   Rivera, L ^a   Jiménez Zurdo, Jose I ^b   Rivas, R ^a   Dazzo, F ^c   Velázquez, E ^a   Martínez Molina, E ^a   Hirsch, Ann M ^d   Mateos, Pedro F ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b CSIC   (Spain)

^c Michigan State University ^*  (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Biofilm; Cellulases; Cellulose biosynthesis; Rhizobium; Symbiosis

Indexed keywords

CELC2 CELLULASE; CELLULASE; CELLULOSE; GLUCAN SYNTHASE; UNCLASSIFIED DRUG;

ABIOTIC STRESS; ARTICLE; BACTERIUM CULTURE; BIOFILM; CARBOHYDRATE SYNTHESIS; CELL ADHESION; CELL AGGREGATION; FIBER; FLOCCULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PLANT ROOT; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM; ROOT HAIR; SYMBIOSIS;

BACTERIAL PROTEINS; BIOFILMS; CELLULASE; CELLULOSE; MUTATION; PLANT ROOTS; RHIZOBIUM LEGUMINOSARUM; SYMBIOSIS; TRIFOLIUM;

RHIZOBIACEAE; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM;

EID: 84866050915     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-125     Document Type: Article

References (57)

1. Dazzo FB, Truchet GL, Sherwood JE, Hrabak EM, Abe M, Pankratz SH. Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Appl Environ Microbiol 1984, 48:1140-1150. 241700, 6393874.
2. Ausmees N, Jacobsson K, Lindberg M. A unipolarly located, cell-surface-associated agglutinin, RapA, belongs to a family of Rhizobium-adhering proteins (Rap) in Rhizobium leguminosarum bv. trifolii. Microbiology 2001, 147:549-559.
3. Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM. Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 2006, 56:195-206. 10.1111/j.1574-6941.2005.00044.x, 16629750.
4. Sherwood JE, Vasse JM, Dazzo FB, Truchet GL. Development and trifoliin A-binding ability of the capsule of Rhizobium trifolii. J Bacteriol 1984, 159:145-152. 215605, 6376470.
5. Davey ME, O'Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 2000, 64:847-867. 10.1128/MMBR.64.4.847-867.2000, 99016, 11104821.
6. Dazzo FB, Brill WJ. Bacterial polysaccharide which binds Rhizobium trifolii to clover root hairs. J Bacteriol 1979, 137:1362-1373. 218321, 86535.
7. Smit G, Swart S, Lugtenberg BJ, Kijne JW. Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 1992, 6:2897-2903. 10.1111/j.1365-2958.1992.tb01748.x, 1479881.
8. Mateos PF, Baker B, Philip-Hollingsworth S, Squartini A, Peruffo A, Nuti M, Dazzo F. Direct in situ identification of cellulose micro fibrils associated with Rhizobium leguminosarum biovar. trifolii attached to the root epidermis of white clover. Can J Microbiol 1995, 41:202-207.
9. Dazzo FB, Napoli CA, Hubbell DH. Adsorption of bacteria to roots as related to host specificity in the Rhizobium-clover symbiosis. Appl Environ Microbiol 1976, 32:166-171. 170022, 970936.
10. Dazzo FB, Brill WJ. Receptor site on clover and alfalfa roots for Rhizobium. Appl Environ Microbiol 1977, 33:132-136. 170604, 16345183.
11. Dazzo FB, Brill WJ. Regulation by fixed nitrogen of host-symbiont recognition in the Rhizobium-clover symbiosis. Plant Physiol 1978, 62:18-21. 10.1104/pp.62.1.18, 1092046, 16660460.
12. De Hoff PL, Brill LM, Hirsch AM. Plant lectins: the ties that bind in root symbiosis and plant defense. Mol Genet Genomics 2009, 282:1-15. 10.1007/s00438-009-0460-8, 2695554, 19488786.
13. Webb JS, Givskov M, Kjelleberg S. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol 2003, 6:578-585. 10.1016/j.mib.2003.10.014, 14662353.
14. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ. Bacterial biofilms in nature and disease. Annu Rev Microbiol 1987, 41:435-464. 10.1146/annurev.mi.41.100187.002251, 3318676.
15. Napoli C, Dazzo F, Hubbell D. Production of cellulose micro fibrils by Rhizobium. Appl Microbiol 1975, 30:123-131. 187130, 1096821.
16. Ausmees N, Jonsson H, Hoglund S, Ljunggren H, Lindberg M. Structural and putative regulatory genes involved in cellulose synthesis in Rhizobium leguminosarum bv. trifolii. Microbiology 1999, 145(Pt 5):1253-1262.
17. Laus MC, van Brussel AA, Kijne JW. Role of cellulose fibrils and exopolysaccharides of Rhizobium leguminosarum in attachment to and infection of Vicia sativa root hairs. Mol Plant Microbe Interact 2005, 18:533-538. 10.1094/MPMI-18-0533, 15986922.
18. Williams A, Wilkinson A, Krehenbrink M, Russo DM, Zorreguieta A, Downie JA. Glucomannan-mediated attachment of Rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. J Bacteriol 2008, 190:4706-4715. 10.1128/JB.01694-07, 2446804, 18441060.
19. Matthysse AG, White S, Lightfoot R. Genes required for cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 1995, 177:1069-1075. 176703, 7860585.
20. Matthysse AG, Deschet K, Williams M, Marry M, White AR, Smith WC. A functional cellulose synthase from ascidian epidermis. Proc Natl Acad Sci USA 2004, 101:986-991. 10.1073/pnas.0303623101, 327129, 14722352.
21. Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH, Benziman M. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 1987, 325:279-281. 10.1038/325279a0, 18990795.
22. Deinema MH, Zevenhuizen LP. Formation of cellulose fibrils by Gram-negative bacteria and their role in bacterial flocculation. Arch Mikrobiol 1971, 78:42-51. 10.1007/BF00409087, 5095074.
23. Ross P, Mayer R, Benziman M. Cellulose biosynthesis and function in bacteria. Microbiol Rev 1991, 55:35-58. 372800, 2030672.
24. Nobles DR, Romanovicz DK, Brown RM. Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase?. Plant Physiol 2001, 127:529-542. 10.1104/pp.010557, 125088, 11598227.
25. Lasa I, Penades JR. Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 2006, 157:99-107. 10.1016/j.resmic.2005.11.003, 16427771.
26. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP. Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 2002, 43:1407-1420. 10.1093/pcp/pcf164, 12514238.
27. Wong HC, Fear AL, Calhoon RD, Eichinger GH, Mayer R, Amikam D, Benziman M, Gelfand DH, Meade JH, Emerick AW, et al. Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci USA 1990, 87:8130-8134. 10.1073/pnas.87.20.8130, 54906, 2146681.
28. Robledo M, Jiménez-Zurdo JI, Velázquez E, Trujillo ME, Zurdo-Piñeiro JL, Ramírez-Bahena MH, Ramos B, Díaz-Minguez JM, Dazzo F, Martínez-Molina E, Mateos PF. Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc Natl Acad Sci USA 2008, 105:7064-7069. 10.1073/pnas.0802547105, 2383954, 18458328.
29. Lin FC, Brown RM, Drake RR, Haley BE. Identification of the uridine 5'-diphosphoglucose (UDP-Glc) binding subunit of cellulose synthase in Acetobacter xylinum using the photoaffinity probe 5-azido-UDP-Glc. J Biol Chem 1990, 265:4782-4784.
30. Romling U. Molecular biology of cellulose production in bacteria. Res Microbiol 2002, 153:205-212. 10.1016/S0923-2508(02)01316-5, 12066891.
31. Saxena IM, Kudlicka K, Okuda K, Brown RM. Characterization of genes in the cellulose-synthesizing operon (acs operon) of Acetobacter xylinum: implications for cellulose crystallization. J Bacteriol 1994, 176:5735-5752. 196778, 8083166.
32. Matthysse AG, Thomas DL, White AR. Mechanism of cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 1995, 177:1076-1081. 176704, 7860586.
33. Mateos PF, Baker D, Petersen M, Velázquez E, Jiménez-Zurdo JI, Martínez-Molina E, Squartini A, Orgambide G, Hubbell D, Dazzo FB. Erosion of root epidermal cell walls by Rhizobium polysaccharide-degrading enzymes as related to primary host infection in the Rhizobium-legume symbiosis. Can J Microbiol 2001, 47:475-487.
34. Robledo M, Jiménez-Zurdo JI, Soto MJ, Velázquez E, Dazzo F, Martínez-Molina E, Mateos PF. Development of functional symbiotic white clover root hairs and nodules requires tightly regulated production of rhizobial cellulase celC2. Mol Plant Microbe Interact 2011, 24:798-807. 10.1094/MPMI-10-10-0249, 21405987.
35. Robledo M, Velázquez E, Ramírez-Bahena MH, García-Fraile P, Pérez-Alonso A, Rivas R, Martínez-Molina E, Mateos PF. The celC gene, a new phylogenetic marker useful for taxonomic studies in Rhizobium. Syst Appl Microbiol 2011, 34:393-399. 10.1016/j.syapm.2011.01.010, 21621937.
36. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 2001, 39:1452-1463. 10.1046/j.1365-2958.2001.02337.x, 11260463.
37. Saldaña Z, Xicohtencatl-Cortes J, Avelino F, Phillips AD, Kaper JB, Puente JL, Giron JA. Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of Fis as a negative regulator of curli. Environ Microbiol 2009, 11:992-1006. 10.1111/j.1462-2920.2008.01824.x, 2672964, 19187284.
38. Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 2002, 43:793-808. 10.1046/j.1365-2958.2002.02802.x, 11929533.
39. Theisen M, Rioux CR, Potter AA. Molecular cloning, nucleotide sequence, and characterization of lppB, encoding an antigenic 40-kilodalton lipoprotein of Haemophilus somnus. Infect Immun 1993, 61:1793-1798. 280767, 8478068.
40. Zevenhuizen LP, Bertocchi C, van Neerven AR. Congo red absorption and cellulose synthesis by Rhizobiaceae. Antonie Van Leeuwenhoek 1986, 52:381-386. 10.1007/BF00393465, 3789702.
41. Peng L, Kawagoe Y, Hogan P, Delmer D. Sitosterol-beta-glucoside as primer for cellulose synthesis in plants. Science 2002, 295:147-150. 10.1126/science.1064281, 11778054.
42. Moulin L, Munive A, Dreyfus B, Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 2001, 411:948-950. 10.1038/35082070, 11418858.
43. Dazzo FB, Hollingsworth R, Philipp-Hollingsworth S, Robeles M, Olen T, Salzwedel J, Djordjevic M, Rolfe B. Recognition processes in the Rhizobium trifolii-white clover symbiosis. In Nitrogen fixation: Hundred years after 1988, 431-436. Justav Fischer Publisher, Stuttgard, Bothe FdB H, Newton W.
44. Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM. Rhizobium common nod genes are required for biofilm formation. Mol Microbiol 2008, 67:504-515. 10.1111/j.1365-2958.2007.06064.x, 18086203.
45. Jordan DC. Family III. Rhizobiaceae 1984, Willians and Wilkins, Baltimore.
46. Beringer JE. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 1974, 84:188-198. 10.1099/00221287-84-1-188, 4612098.
47. Somasegaran P, Hoben HJ. Handbook for rhizobia: methods in legume-Rhizobium technology 1994, Springer, New York.
48. O'Gara F, Shanmugam KT. Regulation of nitrogen fixation by Rhizobia. Export of fixed N2 as NH + 4. Biochim Biophys Acta 1976, 437:313-321. 10.1016/0304-4165(76)90001-5, 8100.
49. Mateos PF, Jiménez-Zurdo JI, Chen J, Squartini AS, Haack SK, Martínez-Molina E, Hubbell DH, Dazzo FB. Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 1992, 58:1816-1822. 195689, 1622257.
50. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y, 2.
51. Cheng HP, Walker GC. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 1998, 180:5183-5191. 107556, 9748453.
52. Da Re S, Le Quere B, Ghigo JM, Beloin C. Tight modulation of Escherichia coli bacterial biofilm formation through controlled expression of adhesion factors. Appl Environ Microbiol 2007, 73:3391-3403. 10.1128/AEM.02625-06, 1907114, 17384304.
53. Rivas R, Velazquez E, Valverde A, Mateos PF, Martínez-Molina E. A two primers random amplified polymorphic DNA procedure to obtain polymerase chain reaction fingerprints of bacterial species. Electrophoresis 2001, 22:1086-1089. 10.1002/1522-2683()22:6<1086::AID-ELPS1086>3.0.CO;2-6, 11358129.
54. Liu J, Dazzo FB, Glagoleva O, Yu B, Jain AK. CMEIAS: a computer-aided system for the image analysis of bacterial morphotypes in microbial communities. Microb Ecol 2001, 41:173-194.
55. Dazzo F. Applications of quantitative microscopy in studies of plant surface microbiology. In Plant surface microbiology 2004, 503-550. Springer- Verlag, Germany, Varma A, Abbott D, Werner D, Hampp R.
56. Gross CA, Reddy CK, Dazzo FB. CMEIAS color segmentation: an improved computing technology to process color images for quantitative microbial ecology studies at single-cell resolution. Microb Ecol 2010, 59:400-414. 10.1007/s00248-009-9616-7, 20020121.
57. Rolfe BG, Gresshoff PM, Shine J. Rapid screening method for symbiotic mutants of Rhizobium leguminosarum biovar trifolii on white clover plants. Plant Sci Lett 1980, 19:277-284.