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Volume 143, Issue 8

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

Abstract

Summary: Acetylesterase and cinnamoyl ester hydrolase activities were demonstrated in culture supernatant of the anaerobic ruminal fungus A cDNA expression library from was screened for esterases using β-naphthyl acetate and a model cinnamoyl ester compound. cDNA clones representing four different esterase genes () were isolated. None of the enzymes had cinnamoyl ester hydrolase activity, but two of the enzymes (BnaA and BnaC) had acetylxylan esterase activity. and encode proteins with several distinct domains. Carboxy-terminal repeats in BnaA and BnaC are homologous to protein-docking domains in other enzymes from species and another anaerobic fungue, a sp. The catalytic domains of BnaB and BnaC are members of a recently described family of Ser/His active site hydrolases [Upton, C. & Buckley, J. T. (1995). 20, 178-179]. BnaB exhibits 40% amino acid identity to a domain of unknown function in the CeIE cellulase from and BnaC exhibits 52% amino acid identity to a domain of unknown function in the XynB xylanase from BnaA, whilst exhibiting less than 10% overall amino acid identity to BnaB or BnaC, or to any other known protein, appears to be a member of the same family of hydrolases, having the three universally conserved amino acid sequence motifs. Several other previously described esterases are also shown to be members of this family, including a rhamnogalacturonan acetylesterase from However, none of the other previously described enzymes with acetylxylan esterase activity are members of this family of hydrolases.

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Keyword(s): acetylxylan esterase , hydrolases , Neocallimastix patriciarum and polysaccharide degradation
© Society for General Microbiology 1997
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1997-08-01
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References

  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
     [Google Scholar]
  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
     [Google Scholar]
  3. Altschul S. F., Lipman D. J. 1990; Protein database searches for multiple alignments. Proc Natl Acad Sci USA 87:5509–5513
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  6. Biely P., Puls J., Schneider H. 1985; Acetylxylan esterases in fungal cellulolytic systems. FEBS Lett 186:80–84
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  13. Chesson A., Forsberg C. W. 1988; Polysaccharide degradation by rumen microorganisms. . In The Rumen Microbial Ecosystem pp. 251–284 . Edited by Hobson P. N. New York: Elsevier Applied Science;
     [Google Scholar]
  14. Christov L. P., Prior B. A. 1993; Esterases of xylan-degrading microorganisms: production, properties, and significance. Enzyme Microb Technol 15:460–475
     [Google Scholar]
  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. Gene141–142
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  28. Halgasova N., Kutejova E., Timko J. 1994; Purification and some characteristics of the acetylxylan esterase from Schizophyllum commune. . Biochem J 298:751–755
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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 poly-hydroxyalkanoate depolymerase system. J Bacteriol 177:596–607
     [Google Scholar]
  36. Johnson K. G., Fontana J. D., MacKenzie C. R. 1988; Measurement of acetylxylan esterase in Streptomyces. . Methods Enzymol 160:551–560
     [Google Scholar]
  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
     [Google Scholar]
  38. Li X., L.& Calza R. E. 1991; Fractionation of cellulases from the ruminal fungus Neocallimastix frontalis EB188. Appl Environ Microbiol 57:3331–3336
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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-l,4-mannanases arose through gene duplication. FEMS Microbiol Lett 141:183–188
     [Google Scholar]
  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 Fund Genet 24:523–524
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  49. Sundberg M., Poutanen K. 1991; Purification and properties of two acetylxylan esterases of Trichoderma reesei. . Biotechnol Appl Biochem 13:1–11
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  55. Upton C., Buckley J.T. 1995; A new family of lipolytic enzymes ?. Trends Biochem Sci 20:178–179
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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
     [Google Scholar]
  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 flavefaciens. . Mol Gen Genet 245:260–264
     [Google Scholar]
  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
     [Google Scholar]
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Three Neocallimastix patriciarum esterases associated with the degradation of complex polysaccharides are members of a new family of hydrolases
Microbiology 143, 2605 (1997); https://doi.org/10.1099/00221287-143-8-2605
/content/journal/micro/10.1099/00221287-143-8-2605
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