Three Neocallimastix patriciarum esterases associated with the degradation of complex polysaccharides are members of a new family of hydrolases

Microbiology

Volumn 143, Issue 8, 1997, Pages 2605-2614

  Dalrymple, Brian P ^a   Cybinski, Daisy H ^a   Layton, Ingrid ^a   McSweeney, Christopher S ^a   Xue, Gang Ping ^a   Swadling, Yolande J ^a   Lowry, J Brian ^a  

^a CSIRO   (Australia)

Author keywords

Acetylxylan esterase; Hydrolases; Neocallimastix patriciarum; Polysaccharide degradation

Indexed keywords

2 NAPHTHYLACETIC ACID; ACETYLESTERASE; CELLULASE; COMPLEMENTARY DNA; ESTER; ESTERASE; HYDROLASE; POLYSACCHARIDE; XYLAN;

AMINO ACID SEQUENCE; ARTICLE; BOVIDS; CARBOXY TERMINAL SEQUENCE; CLOSTRIDIUM THERMOCELLUM; DNA LIBRARY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; FUNGUS; GENE EXPRESSION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; RUMINOCOCCUS; SEQUENCE HOMOLOGY;

ASPERGILLUS ACULEATUS; BOVIDAE; CLOSTRIDIUM THERMOCELLUM; FUNGI; NEOCALLIMASTIX PATRICIARUM; PIROMYCES SP.; RUMINOCOCCUS; RUMINOCOCCUS FLAVEFACIENS;

EID: 0030864850     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-143-8-2605     Document Type: Article

References (61)

1. Akin, D. E., Gordon, G. L. & Hogan, J. P. (1983). Rumen bacterial and fungal degradation of Digitaria pentzii grown with or without sulfur. Appl Environ Microbiol 46, 738-748.
2. Ali, B. R. S., Zhou, L., Graves, F. M., Freedman, R. B., Black, G. W., Gilbert, H. J. & Hazlewood, G. P. (1995). Cellulases and hemicellulases of the anaerobic fungus Piromyces constitute a multi-protein cellulose-binding complex and are encoded by multigene families. FEMS Microbiol Lett 125, 15-22.
3. Altschul, S. F. & Lipman, D. J. (1990). Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87, 5509-5513.
4. Atlan, D., Gilbert, C., Blanc, B. & Portalier, R. (1994). Cloning, sequencing and characterization of the pepIP gene encoding a proline iminopeptidase from Lactobacillus delbrueckii subsp. bulgaricus CNRZ 397. Microbiology 140, 527-535.
5. Bacon, J. S. D., Gordon, A. H. & Morris, E. J. (1975). Acetyl groups in cell-wall preparations from higher plants. Biochem J 149, 485-487.
6. Biely, P., Puls, J. & Schneider, H. (1985). Acetylxylan esterases in fungal cellulolytic systems. FEBS Lett 186, 80-84.
7. Black, G. W., Hazlewood, G. P., Xue, G.-P., Orpin, C. G. & Gilbert, H. J. (1994). Xylanase B from Neocallimastix patriciarum contains a non-catalytic 455-residue linker sequence comprised of 57 repeats of an octapeptide. Biochem J 299, 381-387.
8. Borneman, W. S., Hartley, R. D., Morrison, W. H., Akin, D. E. & Ljungdahl, L. G. L. (1990). Feruloyl and p-coumaroyl esterases from anaerobic fungi in relation to plant cell wall degradation. Appl Microbiol Biotechnol 33, 345-351.
9. Borneman, W. S., Ljungdahl, L. G., Hartley, R. D. & Akin, D. E. (1991). Isolation and characterization of p-coumaroyl esterase from the anaerobic fungus Neocallimastix strain MC-2. Appl Environ Microbiol 57, 2337-2344.
10. Borneman, W. S., Ljungdahl, L. G., Hartley, R. D. & Akin, D. E. (1992). Purification and partial characterization of two feruloyl esterases from the anaerobic fungus Neocallimastix strain MC-2. Appl Environ Microbiol 58, 3762-3766.
11. Brick, D. J., Brumlik, M. J., Buckley, J. T., Cao, J. X., Davies, P. C., Misra, S., Tranbarger, T. J. & Upton, C. (1995). A new family of lipolytic plant enzymes with members in rice, arabidopsis and maize. FEBS Lett 377, 475-480.
12. Castanares, A., McCrae, S. I. & Wood, T. M. (1992). Purification and properties of a feruloyl/p-coumaroyl esterase from the fungus Penicillium pinophilum. Enzyme Microb Technol 14, 875-884.
13. Chesson, A. & Forsberg, C. W. (1988). Polysaccharide degradation by rumen microorganisms. In The Rumen Microbial Ecosystem, pp. 251-284. Edited by P. N. Hobson. New York: Elsevier Applied Science.
14. Christov, L. P. & Prior, B. A. (1993). Esterases of xylan-degrading microorganisms: production, properties, and significance. Enzyme Microb Technol 15, 460-475.
15. Cruz, H., Perez, C., Wellington, E., Castro, C. & Sevrin-Gonzalez, L. (1994). Sequence of the Streptomyces albus G lipase-encoding gene reveals the presence of a prokaryote lipase family. Gene 141-142.
16. Cygler, M., Schrag, J. D., Sussman, J. L., Harel, M., Silman, I., Gentry, M. K. & Doctor, B. P. (1993). Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases and related proteins. Protein Sci 2, 366-382.
17. Dalrymple, B. P., Swadling, Y., Cybinski, D. H. & Xue, G.-P. (1996). Cloning of a gene encoding cinnamoyl ester hydrolase from the ruminal bacterium Butyrivibrio fibrisolvens E14 by a novel method. FEMS Microbiol Lett 143, 115-120.
18. Durrant, A. J., Hall, J., Hazlewood, G. P. & Gilbert, H. J. (1991). The non-catalytic C-terminal region of endoglucanase E from Clostridium thermocellum contains a cellulose-binding domain. Biochem J 273, 289-293.
19. Egaña, L., Gutiérrez, R., Caputo, V., Peirano, A., Steiner, J. & Eyzaguirre, J. (1996). Purification and characterization of two acetyl xylan esterases from Penicillium purpurogenum. Biotechnol Appl Biochem 24, 33-39.
20. Essar, D. W., Eberly, L. & Crawford, I. P. (1990). Evolutionary differences in chromosomal locations of four early genes of the tryptophan pathway in fluorescent pseudomonads: DNA sequences and characterization of Pseudomonas putida trpE and trpGDC. J Bacteriol 172, 867-883.
21. Ettinger, W. F., Thukral, S. K. & Kolattukudy, P. E. (1987). Structure of cutinase gene, cDNA, and the derived amino acid sequence from phytopathogenic fungi. Biochemistry 26, 7883-7892.
22. Fanutti, C., Ponyi, T., Black, G. W., Hazlewood, G. P. & Gilbert, H. J. (1995). The conserved noncatalytic 40-residue sequence in cellulases and hemicellulases from anaerobic fungi functions as a protein docking domain. J Biol Chem 270, 29314-29322.
23. Ferreira, L. M. A., Wood, T. M., Williamson, G., Faulds, C., Hazlewood, G. P., Black, G. W. & Gilbert, H. J. (1993). A modular esterase from Pseudomonas fluorescens subsp. cellulosa contains a non-catalytic cellulose-binding domain. Biochem J 294, 349-355.
24. Fukuda, K., Kuwahata, O., Kiyokawa, Y., Yanagiuchi, T., Wakai, Y., Kitamoto, K., Inoue, Y. & Kimura, A. (1996). Molecular cloning and nucleotide sequence of the isoamyl acetate-hydrolyzing esterase gene (EST2) from Saccharomyces cerevisiae. J Ferment Bioeng 82, 8-15.
25. Gilbert, H. J., Hazlewood, G. P., Laurie, J. I., Orpin, C. G. & Xue, G.-P. (1992). Homologous catalytic domains in a rumen fungal xylanase: evidence for gene duplication and prokaryotic origin. Mol Microbiol 6, 2065-2072.
26. Gomez de Segura, B. & Fèvre, M. (1993). Purification and characterization of two 1,4-β xylan endohydrolases from the rumen fungus Neocallimastix frontalis. Appl Environ Microbiol 59, 3654-3660.
27. Grohmann, K., Mitchell, P. J., Himmel, M. E., Sale, B. E. & Schroeder, H. A. (1989). The role of ester groups in resistance of plant cell wall polysaccharides to enzymatic hydrolysis. Appl Biochem Biotechnol 20/21, 45-61.
28. Halgasova, N., Kutejova, E. & Timko, J. (1994). Purification and some characteristics of the acetylxylan esterase from Schizophyllum commune. Biochem J 298, 751-755.
29. Hall, J., Hazlewood, G. P., Barker, P. J. & Gilbert, H. J. (1988). Conserved reiterated domains in Clostridium thermocellum endoglucanases are not essential for catalytic activity. Gene 69, 29-38.
30. Hattori, M., Adachi, H., Aoki, J., Tsujimoto, M., Arai, H. & Inoue, K. (1995). Cloning and expression of a cDNA encoding the β-subunit (30-kDa subunit) of bovine brain platelet-activating factor acetylhydrolase. J Biol Chem 270, 31345-31352.
31. Henrissat, B. & Bairoch, A. (1993). New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293, 781-788.
32. Ho, Y. S., Swenson, L., Derewenda, U., Serre, L., Wei, Y., Dauter, Z., Hattori, M., Adachi, T., Aoki, J., Arai, H., Inoue, K. & Derewenda, Z. S. (1997). Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer. Nature 385, 89-93.
33. Hoitink, C. W. G., Woudt, L. P., Turenhout, J. C. M., van de Kamp, M. & Canters, G. W. (1990). Isolation and sequencing of the Alcaligenes denitrificans azurin-encoding gene: comparison with the genes encoding blue copper proteins from Pseudomonas aeruginosa and Alcaligenes faecalis. Gene 90, 15-20.
34. Ichihara, S., Matsubara, Y., Kato, C., Akasaka, K. & Mizushima, S. (1993). Molecular cloning, sequencing, and mapping of the gene encoding protease I and characterization of proteinase and proteinase-defective Escherichia coli mutants. J Bacteriol 175, 1032-1037.
35. Jendrossek, D., Frisse, A., Behrends, A., Andermann, M., Kratzin, H. D., Stanislawski, T. & Schlegel, H. G. (1995). Biochemical and molecular characterization of the Pseudomonas lemoignei polyhydroxyalkanoate depolymerase system. J Bacteriol 177, 596-607.
36. Johnson, K. G., Fontana, J. D. & MacKenzie, C. R. (1988). Measurement of acetylxylan esterase in Streptomyces. Methods Enzymol 160, 551-560.
37. Kaupinnen, S., Christgau, S., Kofod, L. V., Halkier, T., Dorreich, K. & Dalboge, H. (1995). Molecular cloning and characterization of a rhamnogalacturonan acetylesterase from Aspergillus aculeatus. J Biol Chem 270, 27172-27178.
38. Li, X. L. & Calza, R. E. (1991). Fractionation of cellulases from the ruminal fungus Neocallimastix frontalis EB188. Appl Environ Microbiol 57, 3331-3336.
39. McCrae, S. I., Leith, K. M., Gordon, A. H. & Wood, T. M. (1994). Xylan-degrading enzyme system produced by the fungus Aspergillus awamori: isolation and characterization of a feruloyl esterase and a p-coumaroyl esterase. Enzyme Microbiol Technol 16, 826-834.
40. McDermid, K. P., Forsberg, C. W. & McKenzie, C. R. (1990). Purification and properties of an acetylxylan esterase from Fibrobacter succinogenes S85. Appl Environ Microbiol 56, 3805-3810.
41. Margolles-Clark, E., Tenkanen, M., Soderlund, H. & Penttila, M. (1996). Acetylxylan esterase from Trichoderma reesei contains an active-site serine residue and a cellulose-binding domain. Eur J Biochem 237, 553-560.
42. Millward-Sadler, S. J., Hall, J., Black, G. W., Hazlewood, G. P. & Gilbert, H. J. (1996). Evidence that the Piromyces gene family encoding endo-1,4-mannanases arose through gene duplication. FEMS Microbiol Lett 141, 183-188.
43. Pangborn, W., Erman, M., Li, N., Burkhart, B. M., Pletnev, V. Z., Duax, W. L., Gutierrez, R., Peirano, A., Eyzaguirre, J., Thiel, D. J. & Ghosh, D. (1996). Characterization of crystals of Penicillium purpurogenum acetyl xylan esterase from high-resolution X-ray diffraction. Proteins Struct Funct Genet 24, 523-524.
44. Poutanen, K., Sundberg, M., Korte, H. & Puls, J. (1990). Deacetylation of xylans by acetyl esterases of Trichoderma reesei. Appl Microbiol Biotechnol 33, 506-510.
45. Raymer, G., Willard, J. M. A. & Schottel, J. L. (1990). Cloning, sequencing, and regulation of expression of an extracellular esterase gene from the plant pathogen Streptomyces scabies. J Bacteriol 172, 7020-7026.
46. Rosenberg, M., Roegner, V. & Becker, F. F. (1975). The quantitation of rat serum esterases by densitometry of acrylamide gels stained for enzyme activity. Anal Biochem 66, 206-212.
47. Shareck, F., Biely, P., Morosoli, R. & Kluepfel, D. (1995). Analysis of DNA flanking the xlnB locus of Streptomyces lividans reveals genes encoding acetylxylan esterase and the RNA component of ribonuclease P. Gene 153, 105-109.
48. Shaw, J.-F., Chang, R.-C., Chuang, K.-H., Yen, Y.-T., Wang, Y. T. & Wang, F.-G. (1994). Nucleotide sequence of a novel arylesterase gene from Vibrio mimicus and characterization of the enzyme expressed in Escherichia coli. Biochem J 298, 675-680.
49. Sundberg, M. & Poutanen, K. (1991). Purification and properties of two acetylxylan esterases of Trichoderma reesei. Biotechnol Appl Biochem 13, 1-11.
50. Tamblyn Lee, J. M., Hu, Y., Zhu, H., Cheng, K. J., Krell P. J. & Forsberg, C. W. (1993). Cloning of a xylanase gene from the ruminal fungus Neocallimastix patriciarum 27 and its expression in Escherichia coli. Can J Microbiol 39, 134-139.
51. Taniguchi, H., Hirano, H., Kubomura, S., Higashi, K. & Mizuguchi, Y. (1986). Comparison of the nucleotide sequences of the genes for the thermostable direct hemolysin and the thermolabile hemolysin from Vibrio parahaemolyticus. Microb Pathog 1, 425-432.
52. Tenkanen, M., Schuseil, J., Puls, J. & Poutanen, K. (1991). Production, purification and characterization of an esterase liberating phenolic acids from lignocellulosics. J Biotechnol 18, 69-84.
53. Tesch, C., Nikoleit, K., Gnau, V., Gotz, F. & Bormann, C. (1996). Biochemical and molecular characterization of the extracellular esterase from Streptomyces diastatochromogenes. J Bacteriol 178, 1858-1865.
54. Thornton, J., Howard, S. P. & Buckley, J. T. (1988). Molecular cloning of a phospholipid-cholesterol acyltransferase from Aeromonas hydrophila. Sequence homologies with lecithin-cholesterol acyltransferase and other lipases. Biochim Biophys Acta 959, 153-159.
55. Upton, C. & Buckley, J. T. (1995). A new family of lipolytic enzymes? Trends Biochem Sci 20, 178-179.
56. Wang, H. & Dowds, B. C. A. (1993). Phase variation in Xenorhabdus luminescens: cloning and sequencing of the lipase gene and analysis of its expression in primary and secondary phases of the bacterium. J Bacteriol 175, 1665-1673.
57. Wei, Y., Schottel, J. L., Derewenda, U., Swenson, L., Patkar, S. & Derewenda, Z. S. (1995). A novel variant of the catalytic triad in the Streptomyces scabies esterase. Nat Struct Biol 2, 218-223.
58. Xue, G.-P., Orpin, C. G., Gobius, K. S., Aylward, J. H. & Simpson, G. D. (1992a). Cloning and expression of multiple cellulase cDNAs from the anaerobic rumen fungus Neocallimastix patriciarum in Escherichia coli. J Gen Microbiol 138, 1413-1420.
59. Xue, G.-P., Gobius, K. S. & Orpin, C. G. (1992b). A novel polysaccharide hydrolase cDNA (celD) from Neocallimastix patriciarum encoding three multi-functional catalytic domains with high endoglucanase, cellobiohydrolase and xylanase activities. J Gen Microbiol 138, 2397-2403.
60. Zhang, J.-X., Martin, J. & Flint, H. J. (1994). Identification of non-catalytic conserved regions in xylanases encoded by the xynB and xynD genes of the cellulolytic rumen anaerobe Ruminococcus flauefaciens. Mol Gen Genet 245, 260-264.
61. Zhou, L., Xue, G.-P., Orpin, C. G., Black, G. W., Gilbert, H. J. & Hazlewood, G. P. (1994). Intronless celB from the anaerobic fungus Neocallimastix patriciarum encodes a modular family A endoglucanase. Biochem J 297, 359-364.