Bacterial pectate lyases, structural and functional diversity

Environmental Microbiology Reports

Volumn 6, Issue 5, 2014, Pages 427-440

  Hugouvieux Cotte Pattat, Nicole ^a,b   Condemine, Guy ^a,b   Shevchik, Vladimir E ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; PECTATE LYASE; POLYSACCHARIDE LYASE;

BACTERIAL INFECTION; BACTERIUM; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PLANT DISEASE;

BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; HUMANS; PLANT DISEASES; POLYSACCHARIDE-LYASES;

EID: 84907829170     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12166     Document Type: Review

References (88)

1. Abad, P., Gouzy, J., Aury, J.M., Castagnone-Sereno, P., Danchin, E.G., Deleury, E., etal. (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26: 909-915.
2. Abbott, D.W., and Boraston, A.B. (2007) A family 2 pectate lyase displays a rare fold and transition metal-assisted beta-elimination. J Biol Chem 282: 35328-35336.
3. Abbott, D.W., and Boraston, A.B. (2008) Structural biology of pectin degradation by Enterobacteriaceae. Microbiol Mol Biol Rev 72: 301-316.
4. Abbott, D.W., Gilbert, H.J., and Boraston, A.B. (2010) The active site of oligogalacturonate lyase provides unique insights into cytoplasmic oligogalacturonate beta-elimination. J Biol Chem 285: 39029-39038.
5. Akita, M., Suzuki, A., Kobayashi, T., Ito, S., and Yamane, T. (2001) The first structure of pectate lyase belonging to polysaccharide lyase family 3. Acta Crystallogr D Biol Crystallogr 57: 1786-1792.
6. Bekri, M.A., Desair, J., Keijers, V., Proost, P., Searle-van Leeuwen, M., Vanderleyden, J., and Vande Broek, A. (1999) Azospirillum irakense produces a novel type of pectate lyase. J Bacteriol 181: 2440-2447.
7. Blot, N., Berrier, C., Hugouvieux-Cotte-Pattat, N., Ghazi, A., and Condemine, G. (2002) The oligogalacturonate-specific porin KdgM of Erwinia chrysanthemi belongs to a new porin family. J Biol Chem 277: 7936-7944.
8. Braccini, I., Grasso, R.P., and Perez, S. (1999) Conformational and configurational features of acidic polysaccharides and their interactions with calcium ions: a molecular modeling investigation. Carbohydr Res 317: 119-130.
9. Brown, I.E., Mallen, M.H., Charnock, S.J., Davies, G.J., and Black, G.W. (2001) Pectate lyase 10A from Pseudomonas cellulosa is a modular enzyme containing a family 2a carbohydrate-binding module. Biochem J 355: 155-165.
10. Caffall, K.H., and Mohnen, D. (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344: 1879-1900.
11. 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.
12. Charkowski, A., Blanco, C., Condemine, G., Expert, D., Franza, T., Hayes, C., etal. (2012) The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu Rev Phytopathol 50: 425-449.
13. Charkowski, A.O., Alfano, J.R., Preston, G., Yuan, J., He, S.Y., and Collmer, A. (1998) The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J Bacteriol 180: 5211-5217.
14. Charnock, S.J., Brown, I.E., Turkenburg, J.P., Black, G.W., and Davies, G.J. (2002) Convergent evolution sheds light on the anti-beta-elimination mechanism common to family 1 and 10 polysaccharide lyases. Proc Natl Acad Sci USA 99: 12067-12072.
15. Choi, M.-S., Kim, W., Lee, C., and Oh, C.-S. (2013) Harpins, multifunctional proteins secreted by Gram-negative plant-pathogenic bacteria. Mol Plant Microbe Interact 26: 1115-1122.
16. Condemine, G., and Ghazi, A. (2007) Differential regulation of two oligogalacturonate outer membrane channels, KdgN and KdgM, of Dickeya dadantii (Erwinia chrysanthemi). J Bacteriol 189: 5955-5962.
17. Condemine, G., and Robert-Baudouy, J. (1987) 2-keto-3-deoxygluconate transport system in Erwinia chrysanthemi. J Bacteriol 169: 1972-1978.
18. Condemine, G., Dorel, C., Hugouvieux-Cotte-Pattat, N., and Robert-Baudouy, J. (1992) Some of the out genes involved in the secretion of pectate lyases in Erwinia chrysanthemi are regulated by kdgR. Mol Microbiol 6: 3199-3211.
19. Cosgrove, D.J. (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13: 171-201.
20. Creze, C., Castang, S., Derivery, E., Haser, R., Hugouvieux-Cotte-Pattat, N., Shevchik, V.E., and Gouet, P. (2008) The crystal structure of pectate lyase PelI from soft rot pathogen Erwinia chrysanthemi in complex with its substrate. J Biol Chem 283: 18260-18268.
21. Czajkowski, R., Perombelon, M.C.M., van Veen, J.A., and van der Wolf, J.M. (2011) Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review. Plant Pathol 60: 999-1013.
22. Danchin, E.G., Rosso, M.N., Vieira, P., de Almeida-Engler, J., Coutinho, P.M., Henrissat, B., and Abad, P. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107: 17651-17656.
23. De Lorenzo, G., Brutus, A., Savatin, D.V., Sicilia, F., and Cervone, F. (2011) Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 585: 1521-1528.
24. El Kaoutari, A., Armougom, F., Gordon, J.I., Raoult, D., and Henrissat, B. (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11: 497-504.
25. Fauvart, M., Verstraeten, N., Dombrecht, B., Venmans, R., Beullens, S., Heusdens, C., and Michiels, J. (2009) Rhizobium etli HrpW is a pectin-degrading enzyme and differs from phytopathogenic homologues in enzymatically crucial tryptophan and glycine residues. Microbiology 155: 3045-3054.
26. Ferrandez, Y., and Condemine, G. (2008) Novel mechanism of outer membrane targeting of proteins in Gram-negative bacteria. Mol Microbiol 69: 1349-1357.
27. Ferrari, S., Savatin, D.V., Sicilia, F., Gramegna, G., Cervone, F., and De Lorenzo, G. (2013) Oligogalacturonides: plant damage-associated patterns and regulators of growth and development. Front Plant Sci 4: 49.
28. Fries, M., Ihrig, J., Brocklehurst, K., Shevchik, V.E., and Pickersgill, R.W. (2007) Molecular basis of the activity of the phytopathogen pectin methylesterase. EMBO J 26: 3879-3887.
29. Gangola, P., and Rosen, B.P. (1987) Maintenance of intracellular calcium in Escherichia coli. J Biol Chem 262: 12570-12574.
30. Garron, M.L., and Cygler, M. (2010) Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20: 1547-1573.
31. Goudeau, D.M., Parker, C.T., Zhou, Y., Sela, S., Kroupitski, Y., and Brandl, M.T. (2013) The Salmonella transcriptome in lettuce and cilantro soft rot reveals a niche overlap with the animal host intestine. Appl Environ Microbiol 79: 250-262.
32. Gummadi, S.N., Kumar, S., and Aneesh, C.N. (2007) Effect of salts on growth and pectinase production by halotolerant yeast, Debaryomyces nepalensis NCYC 3413. Curr Microbiol 54: 472-476.
33. Hassan, S., and Hugouvieux-Cotte-Pattat, N. (2010) Identification of two feruloyl esterases in Dickeya daedantii 3937 and induction of the major feruloyl esterase and of pectate lyases by ferulic acid. J Bacteriol 193: 963-970.
34. Hassan, S., Shevchik, V.E., Robert, X., and Hugouvieux-Cotte-Pattat, N. (2013) PelN is a new pectate lyase of Dickeya dadantii with unusual characteristics. J Bacteriol 195: 2197-2206.
35. Hatada, Y., Saito, K., Koike, K., Yoshimatsu, T., Ozawa, T., Kobayashi, T., and Ito, S. (2000) Deduced amino-acid sequence and possible catalytic residues of a novel pectate lyase from an alkaliphilic strain of Bacillus. Eur J Biochem 267: 2268-2275.
36. Herron, S.R., Benen, J.A., Scavetta, R.D., Visser, J., and Jurnak, F. (2000) Structure and function of pectic enzymes: virulence factors of plant pathogens. Proc Natl Acad Sci USA 97: 8762-8769.
37. Hla, S.S., Kurokawa, J., Suryani, Kimura, T., Ohmiya, K., and Sakka, K. (2005) A novel thermophilic pectate lyase containing two modules of Clostridium stercorarium. Biosci Biotechnol Biochem 69: 2138-2145.
38. Hugouvieux-Cotte-Pattat, N., and Reverchon, S. (2001) Two transporters, TogT and TogMNAB, are responsible for oligogalacturonide uptake in Erwinia chrysanthemi 3937. Mol Microbiol 41: 1125-1132.
39. Hugouvieux-Cotte-Pattat, N., and Robert-Baudouy, J. (1985) Isolation of kdgK-lac and kdgA-lac gene fusions in the phytophatogenic bacteria Erwinia chrysanthemi. J Gen Microbiol 131: 1205-1211.
40. Hugouvieux-Cotte-Pattat, N., Condemine, G., Nasser, W., and Reverchon, S. (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 50: 213-257.
41. Hugouvieux-Cotte-Pattat, N., Blot, N., and Reverchon, S. (2001) Identification of TogMNAB, an ABC transporter which mediates the uptake of pectic oligomers in Erwinia chrysanthemi 3937. Mol Microbiol 41: 1113-1123.
42. Jenkins, J., Mayans, O., and Pickersgill, R. (1998) Structure and evolution of parallel beta-helix proteins. J Struct Biol 122: 236-246.
43. Jenkins, J., Shevchik, V.E., Hugouvieux-Cotte-Pattat, N., and Pickersgill, R.W. (2004) The crystal structure of pectate lyase Pel9A from Erwinia chrysanthemi. J Biol Chem 279: 9139-9145.
44. Jensen, M.H., Otten, H., Christensen, U., Borchert, T.V., Christensen, L.L., Larsen, S., and Leggio, L.L. (2010) Structural and biochemical studies elucidate the mechanism of rhamnogalacturonan lyase from Aspergillus aculeatus. J Mol Biol 404: 100-111.
45. Kazemi-Pour, N., Condemine, G., and Hugouvieux-Cotte-Pattat, N. (2004) The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4: 3177-3186.
46. Kester, H.C., Magaud, D., Roy, C., Anker, D., Doutheau, A., Shevchik, V., etal. (1999) Performance of selected microbial pectinases on synthetic monomethyl-esterified di- and trigalacturonates. J Biol Chem 274: 37053-37059.
47. Kikuchi, T., Shibuya, H., Aikawa, T., and Jones, J.T. (2006) Cloning and characterization of pectate lyases expressed in the esophageal gland of the pine wood nematode Bursaphelenchus xylophilus. Mol Plant Microbe Interact 19: 280-287.
48. Kim, J.F., and Beer, S.V. (1998) HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J Bacteriol 180: 5203-5210.
49. Laatu, M., and Condemine, G. (2003) Rhamnogalacturonate lyase RhiE is secreted by the out system in Erwinia chrysanthemi. J Bacteriol 185: 1642-1649.
50. Liao, C.H., Revear, L., Hotchkiss, A., and Savary, B. (1999) Genetic and biochemical characterization of an exopolygalacturonase and a pectate lyase from Yersinia enterocolitica. Can J Microbiol 45: 396-403.
51. Lietzke, S.E., Yoder, M.D., Keen, N.T., and Jurnak, F. (1994) The three-dimensional structure of pectate lyase E, a plant virulence factor from Erwinia chrysanthemi. Plant Physiol 106: 849-862.
52. Lojkowska, E., Masclaux, C., Boccara, M., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1995) Characterization of the pelL gene encoding a novel pectate lyase of Erwinia chrysanthemi 3937. Mol Microbiol 16: 1183-1195.
53. Lombard, V., Bernard, T., Rancurel, C., Brumer, H., Coutinho, P.M., and Henrissat, B. (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432: 437-444.
54. McDonough, M.A., Kadirvelraj, R., Harris, P., Poulsen, J.C., and Larsen, S. (2004) Rhamnogalacturonan lyase reveals a unique three-domain modular structure for polysaccharide lyase family 4. FEBS Lett 565: 188-194.
55. Marin-Rodriguez, M.C., Orchard, J., and Seymour, G.B. (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53: 2115-2119.
56. Martens, E.C., Lowe, E.C., Chiang, H., Pudlo, N.A., Wu, M., McNulty, N.P., etal. (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9: e1001221.
57. Mayans, O., Scott, M., Connerton, I., Gravesen, T., Benen, J., Visser, J., etal. (1997) Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. Structure 5: 677-689.
58. Moscatiello, R., Baldan, B., Squartini, A., Mariani, P., and Navazio, L. (2012) Oligogalacturonides: novel signaling molecules in Rhizobium-legume communications. Mol Plant Microbe Interact 25: 1387-1395.
59. Nakajima, N., Ishihara, K., Tanabe, M., Matsubara, K., and Matsuura, Y. (1999) Degradation of pectic substances by two pectate lyases from a human intestinal bacterium, Clostridium butyricum-beijerinckii group. J Biosci Bioeng 88: 331-333.
60. Novoa De Armas, H., Verboven, C., De Ranter, C., Desair, J., Vande Broek, A., Vanderleyden, J., and Rabijns, A. (2004) Azospirillum irakense pectate lyase displays a toroidal fold. Acta Crystallogr D Biol Crystallogr 60: 999-1007.
61. Ochiai, A., Itoh, T., Maruyama, Y., Kawamata, A., Mikami, B., Hashimoto, W., and Murata, K. (2007) A novel structural fold in polysaccharide lyases: Bacillus subtilis family 11 rhamnogalacturonan lyase YesW with an eight-bladed beta-propeller. J Biol Chem 282: 37134-37145.
62. Ochiai, A., Itoh, T., Mikami, B., Hashimoto, W., and Murata, K. (2009) Structural determinants responsible for substrate recognition and mode of action in family 11 polysaccharide lyases. J Biol Chem 284: 10181-10189.
63. O'Neill, M.A., Ishii, T., Albersheim, P., and Darvill, A.G. (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55: 109-139.
64. Pages, S., Valette, O., Abdou, L., Belaich, A., and Belaich, J.P. (2003) A rhamnogalacturonan lyase in the Clostridium cellulolyticum cellulosome. J Bacteriol 185: 4727-4733.
65. Payasi, A., Mishra, N.N., Chaves, A.L., and Singh, R. (2009) Biochemistry of fruit softening: an overview. Physiol Mol Biol Plants 15: 103-113.
66. Pissavin, C., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1998) Biochemical characterization of the pectate lyase PelZ of Erwinia chrysanthemi 3937. Biochim Biophys Acta 1383: 188-196.
67. Popeijus, H., Overmars, H., Jones, J., Blok, V., Goverse, A., Helder, J., etal. (2000) Degradation of plant cell walls by a nematode. Nature 406: 36-37.
68. Reverchon, S., and Nasser, W. (2013) Dickeya ecology, environment sensing and regulation of virulence programme. Environ Microbiol Rep 5: 622-636.
69. Rodionov, D.A., Gelfand, M.S., and Hugouvieux-Cotte-Pattat, N. (2004) Comparative genomics of the KdgR regulon in Erwinia chrysanthemi 3937 and other gamma-proteobacteria. Microbiology 150: 3571-3590.
70. Roy, C., Kester, H., Visser, J., Shevchik, V., Hugouvieux-Cotte-Pattat, N., Robert-Baudouy, J., and Benen, J. (1999) Modes of action of five different endopectate lyases from Erwinia chrysanthemi 3937. J Bacteriol 181: 3705-3709.
71. Scavetta, R.D., Herron, S.R., Hotchkiss, A.T., Kita, N., Keen, N.T., Benen, J.A., etal. (1999) Strucure of a plant cell wall fragment complexed to pectate lyase C. Plant Cell 11: 1081-1092.
72. Shevchik, V.E., and Hugouvieux-Cotte-Pattat, N. (1997) Identification of a bacterial pectin acetyl esterase in Erwinia chrysanthemi 3937. Mol Microbiol 24: 1285-1301.
73. Shevchik, V.E., and Hugouvieux-Cotte-Pattat, N. (2003) PaeX, a second pectin acetylesterase of Erwinia chrysanthemi 3937. J Bacteriol 185: 3091-3100.
74. Shevchik, V.E., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1997) Pectate lyase PelI of Erwinia chrysanthemi 3937 belongs to a new family. J Bacteriol 179: 7321-7330.
75. Shevchik, V.E., Boccara, M., Vedel, R., and Hugouvieux-Cotte-Pattat, N. (1998) Processing of the pectate lyase PelI by extracellular proteases of Erwinia chrysanthemi 3937. Mol Microbiol 29: 1459-1469.
76. Shevchik, V.E., Condemine, G., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1999a) The exopolygalacturonate lyase PelW and the oligogalacturonate lyase Ogl, two cytoplasmic enzymes of pectin catabolism in Erwinia chrysanthemi 3937. J Bacteriol 181: 3912-3919.
77. Shevchik, V.E., Kester, H.C., Benen, J.A., Visser, J., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1999b) Characterization of the exopolygalacturonate lyase PelX of Erwinia chrysanthemi 3937. J Bacteriol 181: 1652-1663.
78. Sirotek, K., Slovakova, L., Kopecny, J., and Marounek, M. (2004) Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rabbit caecal bacterium Bacteroides caccae. Lett Appl Microbiol 38: 327-332.
79. Soriano, M., Blanco, A., Diaz, P., and Pastor, F.I. (2000) An unusual pectate lyase from a Bacillus sp. with high activity on pectin: cloning and characterization. Microbiology 146: 89-95.
80. Tamaru, Y., and Doi, R.H. (2001) Pectate lyase A, an enzymatic subunit of the Clostridium cellulovorans cellulosome. Proc Natl Acad Sci USA 98: 4125-4129.
81. Tardy, F., Nasser, W., Robert-Baudouy, J., and Hugouvieux-Cotte-Pattat, N. (1997) Comparative analysis of the five major Erwinia chrysanthemi pectate lyases: enzyme characteristics and potential inhibitors. J Bacteriol 179: 2503-2511.
82. Thibault, J.F., Renard, C.M.G.C., Axelos, M.A.V., Roger, P., and Crepeau, M.J. (1993) Studies of the length of homogalacturonic regions in pectins by acid hydrolysis. Carbohydr Res 238: 271-280.
83. Thomas, L.M., Doan, C.N., Oliver, R.L., and Yoder, M.D. (2002) Structure of pectate lyase A: comparison to other isoforms. Acta Crystallogr D Biol Crystallogr 58: 1008-1015.
84. Wong, D. (2008) Enzymatic deconstruction of backbone structures of the ramified regions of pectins. Protein J 27: 30-42.
85. Xie, F., Murray, J.D., Kim, J., Heckmann, A.B., Edwards, A., Oldroyd, G.E., and Downie, J.A. (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109: 633-638.
86. Yoder, M.D., Lietzke, S.E., and Jurnak, F. (1993) Unusual structural features in the parallel beta-helix in pectate lyases. Structure 1: 241-251.
87. Yuan, P., Meng, K., Wang, Y., Luo, H., Huang, H., Shi, P., etal. (2012) Abundance and genetic diversity of microbial polygalacturonase and pectate lyase in the sheep rumen ecosystem. PLoS ONE 7: e40940.
88. Zerillo, M.M., Adhikari, B.N., Hamilton, J.P., Buell, C.R., Lévesque, C.A., and Tisserat, N. (2013) Carbohydrate-active enzymes in pythium and their role in plant cell wall and storage polysaccharide degradation. PLoS ONE 8: e72572.