Identification of novel enzymes with different hydrolytic activities by metagenome expression cloning

Journal of Biotechnology

Volumn 127, Issue 4, 2007, Pages 575-592

  Lämmle, Katrin ^a   Zipper, Hubert ^a   Breuer, Michael ^b   Hauer, Bernhard ^b   Buta, Christiane ^a   Brunner, Herwig ^a   Rupp, Steffen ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b BASF SE   (Germany)

Author keywords

Activity screening; Gene expression library; Hydrolases; Metagenome; Microbial diversity

Indexed keywords

BIOCATALYSTS; CLONING; DNA; ESCHERICHIA COLI; GENETIC ENGINEERING; HYDROLYSIS; SIZE EXCLUSION CHROMATOGRAPHY;

ACTIVITY SCREENING; GENE EXPRESSION LIBRARY; HYDROLASES; METAGENOME; MICROBIAL DIVERSITY;

ENZYMES;

AMYLASE; DIOXYGENASE; PHOSPHATASE;

ARTICLE; BIOCATALYST; COMPOST; DNA ISOLATION; DNA PURIFICATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; EXPRESSION VECTOR; GEL PERMEATION CHROMATOGRAPHY; GENE EXPRESSION; MICROBIAL DIVERSITY; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BASE SEQUENCE; BIOTECHNOLOGY; CLONING, MOLECULAR; ENZYMES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENOME, BACTERIAL; HYDROLYSIS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SOIL MICROBIOLOGY;

ESCHERICHIA COLI;

EID: 33845743463     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2006.07.036     Document Type: Article

References (89)

1. Akoh C.C., Lee G.C., Liaw Y.C., Huang T.H., and Shaw J.F. GDSL family of serine esterases/lipases. Prog. Lipid Res. 43 (2004) 534-552
2. Altenbuchner J., Viell P., and Pelletier I. Positive selection vectors based on palindromic DNA sequences. Methods Enzymol. 216 (1992) 457-466
3. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
4. Amann R.I., Ludwig W., and Schleifer K.H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59 (1995) 143-169
5. Arpigny J.L., and Jaeger K.E. Bacterial lipolytic enzymes: classification and properties. Biochem. J. 343 (1999) 177-183
6. Bachoon D.S., Otero E., and Hodson R.E. Effects of humic substances on fluorometric DNA quantification and DNA hybridization. J. Microbiol. Methods 47 (2001) 73-82
7. Bairoch A., Boeckmann B., Ferro S., and Gasteiger E. Swiss-Prot: juggling between evolution and stability. Brief. Bioinform. 5 (2004) 39-55
8. Bateman A., Coin L., Durbin R., Finn R.D., Hollich V., Griffiths-Jones S., Khanna A., Marshall M., Moxon S., Sonnhammer E.L., Studholme D.J., Yeats C., and Eddy S.R. The Pfam protein families database. Nucleic Acids Res. 32 (2004) D138-D141
9. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., and Wheeler D.L. GenBank. Nucleic Acids Res. 33 (2005) D34-D38
10. Boel E., Huge-Jensen B., Christensen M., Thim L., and Fiil N.P. Rhizomucor miehei triglyceride lipase is synthesized as a precursor. Lipids 23 (1988) 701-706
11. Bornscheuer U.T., and Kazlauskas R.J. Hydrolases in Organic Synthesis: Regio- and Stereoselective Biotransformations (1999), Wiley-VCH Verlag, Weinheim
12. Bornscheuer U.T., and Pohl M. Improved biocatalysts by directed evolution and rational protein design. Curr. Opin. Chem. Biol. 5 (2001) 137-143
13. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
14. Brenner S. The molecular evolution of genes and proteins: a tale of two serines. Nature 334 (1988) 528-530
15. Bull A.T., Goodfellow M., and Slater J.H. Biodiversity as a source of innovation in biotechnology. Annu. Rev. Microbiol. 46 (1992) 219-252
16. Calamia J., and Manoil C. lac permease of Escherichia coli: topology and sequence elements promoting membrane insertion. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 4937-4941
17. Chica R.A., Doucet N., and Pelletier J.N. Semi-rational approaches to engineering enzyme activity: combining the benefits of directed evolution and rational design. Curr. Opin. Biotechnol. 16 (2005) 378-384
18. Cottrell M.T., Moore J.A., and Kirchman D.L. Chitinases from uncultured marine microorganisms. Appl. Environ. Microbiol. 65 (1999) 2553-2557
19. Dalrymple B.P., Cybinski D.H., Layton I., McSweeney C.S., Xue G.P., Swadling Y.J., and Lowry J.B. Three Neocallimastix patriciarum esterases associated with the degradation of complex polysaccharides are members of a new family of hydrolases. Microbiology 143 (1997) 2605-2614
20. Demirjian D.C., Shah P.C., and Morís-Varas F. Screening for novel enzymes. Top. Curr. Chem. 200 (1999) 1-29
21. Denoya C.D., Skinner D.D., and Morgenstern M.R. A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J. Bacteriol. 176 (1994) 5312-5319
22. Essar D.W., Eberly L., and Crawford I.P. 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 (1990) 867-883
23. Fischer M., and Pleiss J. The Lipase Engineering Database: a navigation and analysis tool for protein families. Nucleic Acids Res. 31 (2003) 319-321
24. Frishman D., Albermann K., Hani J., Heumann K., Metanomski A., Zollner A., and Mewes H.W. Functional and structural genomics using PEDANT. Bioinformatics 17 (2001) 44-57
25. Gabor E.M., de Vries E.J., and Janssen D.B. Efficient recovery of environmental DNA for expression cloning by indirect extraction methods. FEMS Microbiol. Ecol. 44 (2003) 153-163
26. Gabor E.M., Alkema W.B., and Janssen D.B. Quantifying the accessibility of the metagenome by random expression cloning techniques. Environ. Microbiol. 6 (2004) 879-886
27. Gabor E.M., de Vries E.J., and Janssen D.B. Construction, characterization, and use of small-insert gene banks of DNA isolated from soil and enrichment cultures for the recovery of novel amidases. Environ. Microbiol. 6 (2004) 948-958
28. Gillespie D.E., Brady S.F., Bettermann A.D., Cianciotto N.P., Liles M.R., Rondon M.R., Clardy J., Goodman R.M., and Handelsman J. Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl. Environ. Microbiol. 68 (2002) 4301-4306
29. Gupta R., Beg Q.K., and Lorenz P. Bacterial alkaline proteases: molecular approaches and industrial applications. Appl. Microbiol. Biotechnol. 59 (2002) 15-32
30. Handelsman J., Rondon M.R., Brady S.F., Clardy J., and Goodman R.M. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol. 5 (1998) R245-R249
31. Henikoff J.G., Greene E.A., Pietrokovski S., and Henikoff S. Increased coverage of protein families with the blocks database servers. Nucleic Acids Res. 28 (2000) 228-230
32. Henne A., Daniel R., Schmitz R.A., and Gottschalk G. Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxybutyrate. Appl. Environ. Microbiol. 65 (1999) 3901-3907
33. Henne A., Schmitz R.A., Bömeke M., Gottschalk G., and Daniel R. Screening of environmental DNA libraries for the presence of genes conferring lipolytic activity on Escherichia coli. Appl. Environ. Microbiol. 66 (2000) 3113-3116
34. Ho Y.S., Swenson L., Derewenda U., Serre L., Wei Y., Dauter Z., Hattori M., Adachi T., Aoki J., Arai H., Inoue K., and Derewenda Z.S. Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer. Nature 385 (1997) 89-93
35. Holt S.J., and Withers R.F. Studies in enzyme cytochemistry. V. An appraisal of indigogenic reactions for esterase localization. Proc. R. Soc. Lond. B Biol. Sci. 148 (1958) 520-532
36. Hugenholtz P., Goebel B.M., and Pace N.R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180 (1998) 4765-4774
37. Hulo N., Sigrist C.J., Le Saux V., Langendijk-Genevaux P.S., Bordoli L., Gattiker A., De Castro E., Bucher P., and Bairoch A. Recent improvements to the PROSITE database. Nucleic Acids Res. 32 (2004) D134-D137
38. Jacks T.J., and Kircher H.W. Fluorometric assay for the hydrolytic activity of lipase using fatty acyl esters of 4-methylumbelliferone. Anal. Biochem. 21 (1967) 279-285
39. Kanz C., Aldebert P., Althorpe N., Baker W., Baldwin A., Bates K., Browne P., van den Broek A., Castro M., Cochrane G., Duggan K., Eberhardt R., Faruque N., Gamble J., Diez F.G., Harte N., Kulikova T., Lin Q., Lombard V., Lopez R., Mancuso R., McHale M., Nardone F., Silventoinen V., Sobhany S., Stoehr P., Tuli M.A., Tzouvara K., Vaughan R., Wu D., Zhu W., and Apweiler R. The EMBL nucleotide sequence database. Nucleic Acids Res. 33 (2005) D29-D33
40. Kauffmann I.M., Schmitt J., and Schmid R.D. DNA isolation from soil samples for cloning in different hosts. Appl. Microbiol. Biotechnol. 64 (2004) 665-670
41. Koonin E.V., and Tatusov R.L. Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. J. Mol. Biol. 244 (1994) 125-132
42. Krsek M., and Wellington E.M. Comparison of different methods for the isolation and purification of total community DNA from soil. J. Microbiol. Methods 39 (1999) 1-16
43. Lassen S.F., Breinholt J., Ostergaard P.R., Brugger R., Bischoff A., Wyss M., and Fuglsang C.C. Expression, gene cloning, and characterization of five novel phytases from four basidiomycete fungi: Peniophora lycii, Agrocybe pediades, a Ceriporia sp., and Trametes pubescens. Appl. Environ. Microbiol. 67 (2001) 4701-4707
44. Lee S.W., Won K., Lim H.K., Kim J.C., Choi G.J., and Cho K.Y. Screening for novel lipolytic enzymes from uncultured soil microorganisms. Appl. Microbiol. Biotechnol. 65 (2004) 720-726
45. Lo Y.C., Lin S.C., Shaw J.F., and Liaw Y.C. Crystal structure of Escherichia coli thioesterase I/protease I/lysophospholipase L1: consensus sequence blocks constitute the catalytic center of SGNH-hydrolases through a conserved hydrogen bond network. J. Mol. Biol. 330 (2003) 539-551
46. Lorenz P., Liebeton K., Niehaus F., and Eck J. Screening for novel enzymes for biocatalytic processes: accessing the metagenome as a resource of novel functional sequence space. Curr. Opin. Biotechnol. 13 (2002) 572-577
47. Lutz S., and Patrick W.M. Novel methods for directed evolution of enzymes: quality, not quantity. Curr. Opin. Biotechnol. 15 (2004) 291-297
48. MacNeil I.A., Tiong C.L., Minor C., August P.R., Grossman T.H., Loiacono K.A., Lynch B.A., Phillips T., Narula S., Sundaramoorthi R., Tyler A., Aldredge T., Long H., Gilman M., Holt D., and Osburne M.S. Expression and isolation of antimicrobial small molecules from soil DNA libraries. J. Mol. Microbiol. Biotechnol. 3 (2001) 301-308
49. Milcamps A., and de Bruijn F.J. Identification of a novel nutrient-deprivation-induced Sinorhizobium meliloti gene (hmgA) involved in the degradation of tyrosine. Microbiology 145 (1999) 935-947
50. Miller D.N., Bryant J.E., Madsen E.L., and Ghiorse W.C. Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl. Environ. Microbiol. 65 (1999) 4715-4724
51. Molgaard A., Kauppinen S., and Larsen S. Rhamnogalacturonan acetylesterase elucidates the structure and function of a new family of hydrolases. Structure Fold. Des. 8 (2000) 373-383
52. Moran M.A., Torsvik V.L., Torsvik T., and Hodson R.E. Direct extraction and purification of rRNA for ecological studies. Appl. Environ. Microbiol. 59 (1993) 915-918
53. Moré M.I., Herrick J.B., Silva M.C., Ghiorse W.C., and Madsen E.L. Quantitative cell lysis of indigenous microorganisms and rapid extraction of microbial DNA from sediment. Appl. Environ. Microbiol. 60 (1994) 1572-1580
54. Müller H.-J., and Bruchhaus I. Problematik der Isolierung genomischer DNA. Biospektrum 1/97 (1997) 68-73
55. Ogram A. Soil molecular microbial ecology at age 20: methodological challenges for the future. Soil Biol. Biochem. 32 (2000) 1499-1504
56. Ollis D.L., Cheah E., Cygler M., Dijkstra B., Frolow F., Franken S.M., Harel M., Remington S.J., Silman I., Schrag J., Sussman J.L., Verschueren K.H.G., and Goldman A. The alpha/beta hydrolase fold. Protein Eng. 5 (1992) 197-211
57. Pace N.R. A molecular view of microbial diversity and the biosphere. Science 276 (1997) 734-740
58. Pleiss J., Fischer M., Peiker M., Thiele C., and Schmid R.D. Lipase engineering database-understanding and exploiting sequence-structure-function relationships. J. Mol. Catal. B: Enzym. 10 (2000) 491-508
59. Purdy R.E., and Kolattukudy P.E. Depolymerization of a hydroxy fatty acid biopolymer, cutin, by an extracellular enzyme from Fusarium solani f. pisi: isolation and some properties of the enzyme. Arch. Biochem. Biophys. 159 (1973) 61-69
60. Rhee J.K., Ahn D.G., Kim Y.G., and Oh J.W. New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl. Environ. Microbiol. 71 (2005) 817-825
61. Richardson T.H., Tan X., Frey G., Callen W., Cabell M., Lam D., Macomber J., Short J.M., Robertson D.E., and Miller C. A novel, high performance enzyme for starch liquefaction. Discovery and optimization of a low pH, thermostable alpha-amylase. J. Biol. Chem. 277 (2002) 26501-26507
62. Robertson D.E., Chaplin J.A., DeSantis G., Podar M., Madden M., Chi E., Richardson T., Milan A., Miller M., Weiner D.P., Wong K., McQuaid J., Farwell B., Preston L.A., Tan X., Snead M.A., Keller M., Mathur E., Kretz P.L., Burk M.J., and Short J.M. Exploring nitrilase sequence space for enantioselective catalysis. Appl. Environ. Microbiol. 70 (2004) 2429-2436
63. Rondon M.R., August P.R., Bettermann A.D., Brady S.F., Grossman T.H., Liles M.R., Loiacono K.A., Lynch B.A., MacNeil I.A., Minor C., Tiong C.L., Gilman M., Osburne M.S., Clardy J., Handelsman J., and Goodman R.M. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol. 66 (2000) 2541-2547
64. Sanger F., Nicklen S., and Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 5463-5467
65. Schmid A., Dordick J.S., Hauer B., Kiener A., Wubbolts M., and Witholt B. Industrial biocatalysis today and tomorrow. Nature 409 (2001) 258-268
66. Shaw J.F., Chang R.C., Chuang K.H., Yen Y.T., Wang Y.J., and Wang F.G. Nucleotide sequence of a novel arylesterase gene from Vibro mimicus and characterization of the enzyme expressed in Escherichia coli. Biochem. J. 298 (1994) 675-680
67. Shinoda S., Matsuoka H., Tsuchie T., Miyoshi S., Yamamoto S., Taniguchi H., and Mizuguchi Y. Purification and characterization of a lecithin-dependent haemolysin from Escherichia coli transformed by a Vibrio parahaemolyticus gene. J. Gen. Microbiol. 137 (1991) 2705-2711
68. Skerman V.B. Abstracts of Microbiological Methods (1969), Wiley-Interscience, New York
69. Smalla K., Cresswell N., Mendonca-Hagler L.C., Wolters A., and Van Elsas J.D. Rapid DNA extraction protocol from soil for polymerase chain reaction-mediated amplification. J. Appl. Bacteriol. 74 (1993) 78-85
70. Solbak A.I., Richardson T.H., McCann R.T., Kline K.A., Bartnek F., Tomlinson G., Tan X., Parra-Gessert L., Frey G.J., Podar M., Luginbuhl P., Gray K.A., Mathur E.J., Robertson D.E., Burk M.J., Hazlewood G.P., Short J.M., and Kerovuo J. Discovery of pectin-degrading enzymes and directed evolution of a novel pectate lyase for processing cotton fabric. J. Biol. Chem. 280 (2005) 9431-9438
71. Song J.S., Jeon J.H., Lee J.H., Jeong S.H., Jeong B.C., Kim S.J., and Lee S.H. Molecular characterization of TEM-type beta-lactamases identified in cold-seep sediments of Edison Seamount (south of Lihir Island, Papua New Guinea). J. Microbiol. 43 (2005) 172-178
72. Stader J. Gene expression in recombinant Escherichia coli. In: Smith A. (Ed). Gene Expression in Recombinant Microorganisms (1995), Marcel Dekker, Inc., New York 1-51
73. Steffan R.J., Goksøyr J., Bej A.K., and Atlas R.M. Recovery of DNA from soils and sediments. Appl. Environ. Microbiol. 54 (1988) 2908-2915
74. Tatusov R.L., Natale D.A., Garkavtsev I.V., Tatusova T.A., Shankavaram U.T., Rao B.S., Kiryutin B., Galperin M.Y., Fedorova N.D., and Koonin E.V. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29 (2001) 22-28
75. Tebbe C.C., and Vahjen W. Interference of humic acids and DNA extracted directly from soil in detection and transformation of recombinant DNA from bacteria and a yeast. Appl. Environ. Microbiol. 59 (1993) 2657-2665
76. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
77. Thornton J., Howard S.P., and Buckley J.T. Molecular cloning of a phospholipid-cholesterol acyltransferase from Aeromonas hydrophila. Sequence homologies with lecithin-cholesterol acyltransferase and other lipases. Biochim. Biophys. Acta 959 (1988) 153-159
78. Tsai Y.L., and Rochelle P.A. Extraction of nucleic acids from environmental samples. In: Rochelle P.A. (Ed). Environmental Molecular Microbiology: Protocols and Applications. (2001), Horizon Scientific Press, Wymondham, UK pp. 15-30
79. Upton C., and Buckley J.T. A new family of lipolytic enzymes?. Trends Biochem. Sci. 20 (1995) 178-179
80. Vitzthum F., Geiger G., Bisswanger H., Brunner H., and Bernhagen J. A quantitative fluorescence-based microplate assay for the determination of double-stranded DNA using SYBR Green I and a standard ultraviolet transilluminator gel imaging system. Anal. Biochem. 276 (1999) 59-64
81. Vitzthum F., Geiger G., Brunner H., Bisswanger H., and Bernhagen J. DNA quantification by SYBR Green I fluorescence. Bio World 1 (2001) 18-20
82. Voget S., Leggewie C., Uesbeck A., Raasch C., Jaeger K.E., and Streit W.R. Prospecting for novel biocatalysts in a soil metagenome. Appl. Environ. Microbiol. 69 (2003) 6235-6242
83. Vohra A., and Satyanarayana T. Phytases: microbial sources, production, purification, and potential biotechnological applications. Crit. Rev. Biotechnol. 23 (2003) 29-60
84. Wang H., and Dowds B.C. 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 (1993) 1665-1673
85. Wei Y., Schottel J.L., Derewenda U., Swenson L., Patkar S., and Derewenda Z.S. A novel variant of the catalytic triad in the Streptomyces scabies esterase. Nat. Struct. Biol. 2 (1995) 218-223
86. Whitman W.B., Coleman D.C., and Wiebe W.J. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 6578-6583
87. Wu C.H., Yeh L.S., Huang H., Arminski L., Castro-Alvear J., Chen Y., Hu Z., Kourtesis P., Ledley R.S., Suzek B.E., Vinayaka C.R., Zhang J., and Barker W.C. The protein information resource. Nucleic Acids Res. 31 (2003) 345-347
88. Yun J., Kang S., Park S., Yoon H., Kim M.J., Heu S., and Ryu S. Characterization of a novel amylolytic enzyme encoded by a gene from a soil-derived metagenomic library. Appl. Environ. Microbiol. 70 (2004) 7229-7235
89. Zhou J., Bruns M.A., and Tiedje J.M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62 (1996) 316-322