Functional and structural studies of a novel cold-adapted esterase from an Arctic intertidal metagenomic library

Applied Microbiology and Biotechnology

Volumn 97, Issue 9, 2013, Pages 3965-3978

  Fu, Juan ^a   Leiros, Hanna Kirsti S ^a   De Pascale, Donatella ^b   Johnson, Kenneth A ^a   Blencke, Hans Matti ^a   Landfald, Bjarne ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

Cold adapted; Crystal structure; Esterase; Metagenomic; Thermolabile

Indexed keywords

AMINO ACIDS; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; ESCHERICHIA COLI; ESTERS; GENES;

COLD ADAPTED; ESTERASE; ESTERASE ACTIVITIES; HIGH-RESOLUTION STRUCTURES; METAGENOMIC; METAGENOMIC LIBRARIES; SINGLE-WAVELENGTH ANOMALOUS DISPERSIONS; THERMOLABILE;

ENZYMES;

4 NITROPHENYL ESTER; 4 NITROPHENYL HEXANOATE; ALPHA BETA HYDROLASE; ESTER DERIVATIVE; ESTERASE; HEXANOIC ACID DERIVATIVE; HYDROLASE; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

COLD TOLERANCE; COLIFORM BACTERIUM; CRYSTAL STRUCTURE; ENZYME ACTIVITY; GENOMICS; INTERTIDAL ENVIRONMENT;

ARCTIC; ARTICLE; COLD ACCLIMATIZATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; DISPERSION; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE LIBRARY; GENE PRODUCT; INTERTIDAL ZONE; MELTING POINT; METAGENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; TEMPERATURE; THERMOSTABILITY; VIBRIO; VIBRIO CARIBBENTHICUS; CHEMISTRY; CIRCULAR DICHROISM; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; METHODOLOGY; PHYLOGENY; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI; VIBRIO;

ARCTIC REGIONS; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; ESTERASES; GENE LIBRARY; LIPASE; METAGENOMICS; PHYLOGENY; SUBSTRATE SPECIFICITY; TEMPERATURE; VIBRIO;

EID: 84883135502     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4276-9     Document Type: Article

References (60)

1. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143-169
2. Arpigny JL, Jaeger KE (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343:177-183
3. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276-280
4. Bornscheuer UT (2002) Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev 26:73-81
5. Byun JS, Rhee JK, Kim ND, Yoon J, Kim DU, Koh E, Oh JW, Cho HS (2007) Crystal structure of hyperthermophilic esterase EstE1 and the relationship between its dimerization and thermostability properties. BMC Struct Biol 7:47-57
6. Choo D-W, Kurihara T, Suzuki T, Soda K, Esaki N (1998) A coldadapted lipase of an Alaskan psychrotroph, Pseudomonas sp. Strain B11-1: gene cloning and enzyme purification and characterization. Appl Environ Microbiol 64:486-491
7. Chu X, He H, Guo C, Sun B (2008) Identification of two novel esterases from a marine metagenomic library derived from South China Sea. Appl Environ Microbiol 80:615-625
8. Cieśliński H, Białkowska A, Długołe¸cka A, Daroch M, Tkaczuk KL, Kalinowska H, Kur J, Turkiewicz M (2007) A cold-adapted esterase from psychrotrophic Pseudoalteromas sp. strain 643A. Arch Microbiol 188:27-36
9. Cohen SX, Ben Jelloul M, Long F, Vagin A, Knipscheer P, Lebbink J, Sixma TK, Lamzin VS, Murshudov GN, Perrakis A (2008) ARP/ wARP and molecular replacement: the next generation. Acta Crystallogr D: Biol Crystallogr 64:49-60
10. Collaborative Computational Project-4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D: Biol Crystallogr 50:760-763
11. Cowtan K (2008) Fitting molecular fragments into electron density. Acta Crystallogr D: Biol Crystallogr 64:83-89
12. de Pascale D, Cusano AM, Autore F, Parrilli E, di Prisco G, Marino G, Tutino ML (2008) The cold-active Lip1 lipase from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125 is a member of a new bacterial lipolytic enzyme family. Extremophiles 12:311-323
13. De Santi C, Tutino ML, Mandrich L, Giuliani M, Parrilli E, Del Vecchio P, de Pascale D (2010) The hormone-sensitive lipase from Psychrobacter sp. TA144: new insight in the structural/ functional characterization. Biochimie 92:949-957
14. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang J-M, Taly J-F, Notredame C (2011) T-coffee: a webserver for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucl Acids Res 39(suppl 2):W13-W17
15. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D: Biol Crystallogr 60:2126-2132
16. Ericsson DJ, Kasrayan A, Johansson P, Bergfors T, Sandström AG, Bäckvall JE, Mowbray SL (2008) X-ray structure of Candida antarctica lipase A shows a novel lid structure and a likely mode of interfacial activation. J Mol Biol 376:109-119
17. Fedøy AE, Yang N, Martinez A, Leiros H-KS, Steen IH (2007) Structural and functional properties of isocitrate dehydrogenase from the psychrophilic bacterium Desulfotalea psychrophila reveal a cold-active enzyme with an unusual high thermal stability. J Mol Biol 372:130-149
18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
19. Fu C, Hu Y, Xie F, Guo H, Ashforth EJ, Polyak SW, Zhu B, Zhang L (2011) Molecular cloning and characterization of a new coldactive esterase from a deep-sea metagenomic library. Appl Microbiol Biotechnol 90:961-970
20. Georlette D, Blaise V, Collins T, D'Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25-42
21. Goldstone DC, Villas-Boas SG, Till M, Kelly WJ, Attwood GT, Arcus VL (2010) Structural and functional characterization of a promiscuous feruloyl esterase (Est1E) from the rumen bacterium Butyrivibrio proteoclasticus. Proteins 78:1457-1469
22. Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. App Microbiol Biotechnol 64:763-781
23. Hårdeman F, Sjöling S (2007) Metagenomic approach for the isolation of a novel low-temperature-active lipase from uncultured bacteria of marine sediment. FEMS Microbiol Ecol 59:524-534
24. Hasan F, Shah AA, Hameed A (2006) Industrial applications of microbial lipases. Enzyme Microb Technol 39:235-251
25. Hausmann S, Jaeger KE (2010) Lipolytic enzymes from bacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 1099-1126
26. Heath C, Xiao PH, Cary SC, Cowan D (2009) Identification of a novel alkaliphilic esterase active at low temperatures by screening a metagenomic library from Antarctic desert soil. Appl Environ Microbiol 75:4657-4659
27. Holm L, Rosenström P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545-W549
28. Houde A, Kademi A, Leblanc D (2004) Lipases and their industrial applications: an overview. Appl Biochem Biotechnol 118:155-170
29. Hu Y, Fu C, Huang Y, Yin Y, Cheng G, Lei F, Lu N, Li J, Ashforth EJ, Zhang L, Zhu B (2010) Novel lipolytic genes from the microbial metagenomic library of the South China Sea marine sediment. FEMS Microbiol Ecol 72:228-237
30. Hu XP, Heath C, Taylor MP, Tuffin M, Cowan D (2012) A novel, extremely alkaliphilic and cold-active esterase from Antarctic desert soil. Extremophiles 16:79-86
31. Jeon JH, Kim JT, Kang SG, Lee JH, Kim SJ (2009a) Characterization and its potential application of two esterases derived from the arctic sediment metagenome. Mar Biotechnol (NY) 11:307-316
32. Jeon JH, Kim JT, Kim YJ, Kim HK, Lee HS, Kang SG, Kim SJ, Lee JH (2009b) Cloning and characterization of a new cold-active lipase from a deep-sea sediment metagenome. Appl Microbiol Biotechnol 81:865-874
33. Jeon JH, Lee HS, Kim JT, Kim SJ, Choi SH, Kang SG, Lee JH (2011) Identification of a new subfamily of salt-tolerant esterases from a metagenomic library of tidal flat sediment. Appl Microbiol Biotechnol 93:623-631
34. Joseph B, Ramteke PW, Thomas G (2008) Cold active microbial lipases: some hot issues and recent developments. Biotechnol Adv 26:457-470
35. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26:795-800
36. Kim BS, Oh HM, Kang H, Park SS, Chun J (2004) Remarkable bacterial diversity in the tidal flat sediment as revealed by 16S rDNA analysis. J Microbiol Biotechnol 14:205-211
37. Kim BS, Oh HM, Kang H, Chun J (2005) Archaeal diversity in tidal flat sediment as revealed by 16S rDNA analyis. J Microbiol 43:144-151
38. Kim EY, Oh KH, Lee MH, Kang CH, Oh TK, Yoon JH (2009) Novel cold-adapted alkaline lipase from an intertidal flat metagenome and proposal for a new family of bacterial lipases. Appl Environ Microbiol 75:257-260
39. Lee MH, Lee CH, Oh TK, Song JK, Yoon JH (2006) Isolation and characterization of a novel lipase from a metagenomic library of tidal flat sediments: evidence for a new family of bacterial lipases. Appl Environ Microbiol 72:7406-7409
40. Leiros H-KS, Brandsdal BO, McSweeney SM (2010) Biophysical characterization and mutational analysis of the antibiotic resistance protein NimA from Deinococcus radiodurans. Biochim Biophys Acta 1804:967-76
41. Liaw RB, Cheng MP, Wu MC, Lee CY (2010) Use of metagenomic approaches to isolate lipolytic genes from activated sludge. J Bioresour Technol 101:8323-8329
42. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238:777-793
43. Nacke H, Will C, Herzog S, Nowka B, Engelhaupt M, Daniel R (2011) Identification of novel lipolytic genes and gene families by screening of metagenomic libraries derived from soil samples of the German Biodiversity Exploratories. FEMS Microbiol Ecol 78:188-201
44. Nam KH, Kim M-Y, Kim S-J, Priyadarshi A, Lee WH, Hwang KY (2009) Structural and functional analysis of a novel EstE5 belonging to the subfamily of hormone-sensitive lipase. Biochem Biophys Res Commun 379:553-556
45. Rashid N, Shimada Y, Ezaki S, Atomi H, Imanaka T (2001) Lowtemperature lipase from psychrotrophic Pseudomonas sp. strain KB700A. Appl Environ Microbiol 67:4064-4069
46. Roh C, Villatte F (2008) Isolation of a low-temperature adapted lipolytic enzyme from uncultivated micro-organism. J Appl Microbiol 105:116-123
47. Ronquist F, Huelsenbeck JP (2003)MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574
48. Ryu HS, Kim HK, Choi WC, Kim MH, Park SY, Han NS, Oh TK, Lee JK (2006) New cold-adapted lipase from Photobacterium lipolyticum sp. nov. that is closely related to filamentous fungal lipases. Appl Microbiol Biotechnol 70:321-326
49. Santarossa G, Lafranconi PG, Alquati C, DeGioia L, Alberghina L, Fantucci P, Lotti M (2005) Mutations in the "lid" region affect chain length specificity and thermostability of a Pseudomonas fragi lipase. FEBS Lett 579:2383-2386
50. Schneider TR, Pape T (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J Appl Crystallogr 37:843-844
51. Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr Sect A 64:112-122
52. Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403-433
53. Smalås AO, Leiros HK, Os V, Willassen NP (2000) Cold adapted enzymes. Biotechnol Annu Rev 6:1-57
54. Suzuki T, Nakayama T, Kurihara T, Nishino T, Esaki N (2002) Primary structure and catalytic properties of a cold-active esterase from a psychrotroph, Acinetobacter sp. strain no. 6. isolated from Siberian soil. Biosci Biotechnol Biochem 66:1682-1690
55. Suzuki T, Nakayama T, Choo DW, Hirano Y, Kurihara T, Nishino T, Esaki N (2003) Cloning, heterologous expression, renaturation, and characterization of a cold-adapted esterase with unique primary structure from a psychrotroph Pseudomonas sp. strain B11- 1. Protein Expr Purif 30:171-178
56. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599
57. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882
58. Uppenberg J, Hansen MT, Patkar S, Jones TA (1994) The sequence, crystal structure determination and refinement of two crystal forms of lipase B from Candida antarctica. Structure 2:293-308 Vriend G (1990) What if: a molecular modeling and drug design program. J Mol Graph 8:52-56
59. Whitmore L, Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392-400
60. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316-322