The environment shapes microbial enzymes: five cold-active and salt-resistant carboxylesterases from marine metagenomes

Applied Microbiology and Biotechnology

Volumn 99, Issue 5, 2015, Pages 2165-2178

  Tchigvintsev, Anatoli ^a   Tran, Hai ^a,b   Popovic, Ana ^a   Kovacic, Filip ^c   Brown, Greg ^a   Flick, Robert ^a   Hajighasemi, Mahbod ^a   Egorova, Olga ^a   Somody, Joseph C ^a   Tchigvintsev, Dmitri ^a   Khusnutdinova, Anna ^a   Chernikova, Tatyana N ^b   Golyshina, Olga V ^b   Yakimov, Michail M ^d   Savchenko, Alexei ^a   Golyshin, Peter N ^b   Jaeger, Karl Erich ^c   Yakunin, Alexander F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b BANGOR UNIVERSITY   (United Kingdom)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d CNR   (Italy)

Author keywords

Cold adaptation; Esterase; Marine metagenome; Metagenomic library; Polyester hydrolysis; Salt resistance

Indexed keywords

ENZYME INHIBITION; HYDROLYSIS; POLYESTERS; POTASSIUM COMPOUNDS; PURIFICATION; SOAPS (DETERGENTS); SODIUM CHLORIDE; SUBSTRATES;

COLD ADAPTATION; ESTERASE; METAGENOMES; METAGENOMIC LIBRARIES; SALT RESISTANCE;

ESTERS;

CARBOXYLESTERASE; GLYCEROL; MICROBIAL ENZYME; POLYESTER; POTASSIUM CHLORIDE; SODIUM CHLORIDE; ENZYME ACTIVATOR;

ADAPTATION; BIOCHEMICAL COMPOSITION; BIOSPHERE; COLD FRONT; ENZYME ACTIVITY; GENOME; HYDROLYSIS; MICROBIAL ACTIVITY; SALT; SUBSTRATE;

ARTICLE; COLD; CONTROLLED STUDY; DEPOLYMERIZATION; DNA EXTRACTION; ENRICHMENT CULTURE; ENVIRONMENT; ENVIRONMENTAL TEMPERATURE; ENZYME ACTIVITY; ENZYME PURIFICATION; GENE LIBRARY; MARINE METAGENOME; METAGENOME; MICROBIAL COMMUNITY; NONHUMAN; OSMOREGULATION; SCREENING; THERMOSTABILITY; AQUATIC SPECIES; DNA SEQUENCE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS;

AQUATIC ORGANISMS; CARBOXYLIC ESTER HYDROLASES; COLD TEMPERATURE; ENZYME ACTIVATORS; METAGENOME; MOLECULAR SEQUENCE DATA; POTASSIUM CHLORIDE; SEQUENCE ANALYSIS, DNA; SODIUM CHLORIDE; SUBSTRATE SPECIFICITY;

EID: 84923261245     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6038-3     Document Type: Article

References (83)

1. Akutsu-Shigeno Y, Teeraphatpornchai T, Teamtisong K, Nomura N, Uchiyama H, Nakahara T, Nakajima-Kambe T (2003) Cloning and sequencing of a poly(DL-lactic acid) depolymerase gene from Paenibacillus amylolyticus strain TB-13 and its functional expression in Escherichia coli. Appl Environ Microbiol 69:2498–2504
2. Alcaide M, Tornes J, Stogios PJ, Xu X, Gertler C, Di Leo R, Bargiela R, Lafraya A, Guazzaroni ME, Lopez-Cortes N, Chernikova TN, Golyshina OV, Nechitaylo TY, Plumeier I, Pieper DH, Yakimov MM, Savchenko A, Golyshin PN, Ferrer M (2013) Single residues dictate the co-evolution of dual esterases: MCP hydrolases from the alpha/beta hydrolase family. Biochem J 454:157–166
3. Arpigny JL, Jaeger KE (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343:177–183
4. Baumann M, Hauer B, Bornscheuer UT (2000) Rapid screening of hydrolases for enantioselective conversion of “difficult-to-resolve substrates”. Tetrahedron Asymmetry 11:4781–4790
5. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SB, Gates CM, Feldman RA, Spudich JL, DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906
6. Beloqui A, Pita M, Polaina J, Martinez-Arias A, Golyshina OV, Zumarraga M, Yakimov MM, Garcia-Arellano H, Alcalde M, Fernandez VM, Elborough K, Andreu JM, Ballesteros A, Plou FJ, Timmis KN, Ferrer M, Golyshin PN (2006) Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J Biol Chem 281:22933–22942
7. Ben-Amotz A, Avron M (1973) The role of glycerol in the osmotic regulation of the halophilic alga Dunaliella parva. Plant Physiol 51:875–878
8. Bornscheuer UT (2002) Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev 26:73–81
9. Bornscheuer UT, Kazlauskas RJ (2006) Hydrolases in organic synthesis, 2nd edn. WILEY-VCH, Weinheim
10. Bornscheuer UT, Ordonez G, Hidalgo A, Gollin A, Lyon J, Hitchman TS, Weiner DP (2005) Selectivity of lipases and esterases towards phenol esters. J Mol Catal B Enzym 36:8–13
11. Chow J, Kovacic F, Dall Antonia Y, Krauss U, Fersini F, Schmeisser C, Lauinger B, Bongen P, Pietruszka J, Schmidt M, Menyes I, Bornscheuer UT, Eckstein M, Thum O, Liese A, Mueller-Dickmann J, Jaeger K-E, Streit WR (2012) The metagenome-derived enzymes LipS and LipT increase the diversity of known lipases. PLoS One 7:e47665
12. Christian JH, Waltho JA (1961) The sodium and potassium content of non-halophilic bacteria in relation to salt tolerance. J Gen Microbiol 25:97–102
13. Christian JH, Waltho JA (1962) Solute concentrations within cells of halophilic and non-halophilic bacteria. Biochim Biophys Acta 65:506–508
14. Danson MJ, Hough DW (1997) The structural basis of protein halophilicity. Comp Biochem Physiol 117:307–312
15. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li L, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan Y, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–632
16. Elend C, Schmeisser C, Leggewie C, Babiak P, Carballeira JD, Steele HL, Reymond JL, Jaeger KE, Streit WR (2006) Isolation and biochemical characterization of two novel metagenome-derived esterases. Appl Environ Microbiol 72:3637–3645
17. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1:200–208
18. Ferrer M, Golyshina OV, Chernikova TN, Khachane AN, Martins Dos Santos VA, Yakimov MM, Timmis KN, Golyshin PN (2005a) Microbial enzymes mined from the Urania deep-sea hypersaline anoxic basin. Chem Biol 12:895–904
19. Ferrer M, Golyshina OV, Chernikova TN, Khachane AN, Reyes-Duarte D, Santos VA, Strompl C, Elborough K, Jarvis G, Neef A, Yakimov MM, Timmis KN, Golyshin PN (2005b) Novel hydrolase diversity retrieved from a metagenome library of bovine rumen microflora. Environ Microbiol 7:1996–2010
20. Ferrer M, Golyshina O, Beloqui A, Golyshin PN (2007) Mining enzymes from extreme environments. Curr Opin Microbiol 10:207–214
21. Ferrer M, Beloqui A, Timmis KN, Golyshin PN (2009) Metagenomics for mining new genetic resources of microbial communities. J Mol Microbiol Biotechnol 16:109–123
22. Fu C, Hu Y, Xie F, Guo H, Ashforth EJ, Polyak SW, Zhu B, Zhang L (2011) Molecular cloning and characterization of a new cold-active esterase from a deep-sea metagenomic library. Appl Microbiol Biotechnol 90:961–970
23. Gilbert JA, Dupont CL (2011) Microbial metagenomics: beyond the genome. Ann Rev Mar Sci 3:347–371
24. Giovannoni S, Stingl U (2007) The importance of culturing bacterioplankton in the ‘omics’ age. Nat Rev Microbiol 5:820–826
25. Gonzalez CF, Proudfoot M, Brown G, Korniyenko Y, Mori H, Savchenko AV, Yakunin AF (2006) Molecular basis of formaldehyde detoxification. Characterization of two S-formylglutathione hydrolases from Escherichia coli, FrmB and YeiG. J Biol Chem 281:14514–14522
26. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685
27. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:R245–R249
28. Hausmann S, Jaeger K-E (2010) Lipolytic enzymes from bacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology v. 2 (part 4). Springer, Berlin, pp 1099–1126
29. Heath C, Hu XP, 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
30. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467
31. Hummel A, Brusehaber E, Bottcher D, Trauthwein H, Doderer K, Bornscheuer UT (2007) Isoenzymes of pig-liver esterase reveal striking differences in enantioselectivities. Angew Chem Int Ed Engl 46:8492–8494
32. Izawa S, Sato M, Yokoigawa K, Inoue Y (2004) Intracellular glycerol influences resistance to freeze stress in Saccharomyces cerevisiae: analysis of a quadruple mutant in glycerol dehydrogenase genes and glycerol-enriched cells. Appl Microbiol Biotechnol 66:108–114
33. Jabbour D, Sorger A, Sahm K, Antranikian G (2013) A highly thermoactive and salt-tolerant alpha-amylase isolated from a pilot-plant biogas reactor. Appl Microbiol Biotechnol 97:2971–2978
34. Jaeger KE, Steinbuchel A, Jendrossek D (1995) Substrate specificities of bacterial polyhydroxyalkanoate depolymerases and lipases: bacterial lipases hydrolyze poly(omega-hydroxyalkanoates). Appl Environ Microbiol 61:3113–3118
35. Janes LE, Lowendahl AC, Kazlauskas RJ (1998) Quantitative screening of hydrolase libraries using pH indicators: identifying active and enantioselective hydrolases. Chem Eur J 4:2324–2331
36. Jarerat A, Tokiwa Y, Tanaka H (2006) Production of poly(L-lactide)-degrading enzyme by Amycolatopsis orientalis for biological recycling of poly(L-lactide). Appl Microbiol Biotechnol 72:726–731
37. Jiang X, Xu X, Huo Y, Wu Y, Zhu X, Zhang X, Wu M (2012) Identification and characterization of novel esterases from a deep-sea sediment metagenome. Arch Microbiol 194:207–214
38. Kang CH, Oh KH, Lee MH, Oh TK, Kim BH, Yoon J (2011) A novel family VII esterase with industrial potential from compost metagenomic library. Microb Cell Fact 10:41
39. Kim SB, Lee W, Ryu YW (2008) Cloning and characterization of thermostable esterase from Archaeoglobus fulgidus. J Microbiol 46:100–107
40. Kouker G, Jaeger KE (1987) Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol 53:211–213
41. Kourist R, Hari Krishna S, Patel JS, Bartnek F, Hitchman TS, Weiner DP, Bornscheuer UT (2007) Identification of a metagenome-derived esterase with high enantioselectivity in the kinetic resolution of arylaliphatic tertiary alcohols. Org Biomol Chem 5:3310–3313
42. Kube M, Chernikova TN, Al-Ramahi Y, Beloqui A, Lopez-Cortez N, Guazzaroni ME, Heipieper HJ, Klages S, Kotsyurbenko OR, Langer I, Nechitaylo TY, Lunsdorf H, Fernandez M, Juarez S, Ciordia S, Singer A, Kagan O, Egorova O, Petit PA, Stogios P, Kim Y, Tchigvintsev A, Flick R, Denaro R, Genovese M, Albar JP, Reva ON, Martinez-Gomariz M, Tran H, Ferrer M, Savchenko A, Yakunin AF, Yakimov MM, Golyshina OV, Reinhardt R, Golyshin PN (2013) Genome sequence and functional genomic analysis of the oil-degrading bacterium Oleispira antarctica. Nat Commun 4:2156
43. Lange S, Musidlowska A, Schmidt-Dannert C, Schmitt J, Bornscheuer UT (2001) Cloning, functional expression, and characterization of recombinant pig liver esterase. Chembiochem 2:576–582
44. Lemak S, Tchigvintsev A, Petit P, Flick R, Singer AU, Brown G, Evdokimova E, Egorova O, Gonzalez CF, Chernikova TN, Yakimov MM, Kube M, Reinhardt R, Golyshin PN, Savchenko A, Yakunin AF (2012) Structure and activity of the cold-active and anion-activated carboxyl esterase OLEI01171 from the oil-degrading marine bacterium Oleispira antarctica. Biochem J 445:193–203
45. Lewis JG, Learmonth RP, Watson K (1995) Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology 141:687–694
46. Lorenz P, Eck J (2005) Metagenomics and industrial applications. Nat Rev Microbiol 3:510–516
47. Lorenz P, Liebeton K, Niehaus F, Eck J (2002) Screening for novel enzymes for biocatalytic processes: accessing the metagenome as a resource of novel functional sequence space. Curr Opin Biotechnol 13:572–577
48. Managbanag JR, Torzilli AP (2002) An analysis of trehalose, glycerol, and mannitol accumulation during heat and salt stress in a salt marsh isolate of Aureobasidium pullulans. Mycologia 94:384–391
49. Martinez-Martinez M, Alcaide M, Tchigvintsev A, Reva O, Polaina J, Bargiela R, Guazzaroni ME, Chicote A, Canet A, Valero F, Eguizabal ER, Guerrero MC, Yakunin AF, Ferrer M (2013) Biochemical diversity of carboxyl esterases and lipases from Lake Arreo (Spain): a metagenomic approach. Appl Environ Microbiol 79:3553–3562
50. Matsuda E, Abe N, Tamakawa H, Kaneko J, Kamio Y (2005) Gene cloning and molecular characterization of an extracellular poly(L-lactic acid) depolymerase from Amycolatopsis sp. strain K104-1. J Bacteriol 187:7333–7340
51. Mayumi D, Akutsu-Shigeno Y, Uchiyama H, Nomura N, Nakajima-Kambe T (2008) Identification and characterization of novel poly(DL-lactic acid) depolymerases from metagenome. Appl Microbiol Biotechnol 79:743–750
52. Morar M, Pengelly K, Koteva K, Wright GD (2012) Mechanism and diversity of the erythromycin esterase family of enzymes. Biochemistry 51:1740–1751
53. Nass R, Rao R (1999) The yeast endosomal Na+/H+ exchanger, Nhx1, confers osmotolerance following acute hypertonic shock. Microbiology 145:3221–3228
54. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348
55. Oren A (2002) Halophilic microorganisms and their environments. Kluwer Academic Publisher, Dordrecht
56. Peng Q, Zhang X, Shang M, Wang X, Wang G, Li B, Guan G, Li Y, Wang Y (2011) A novel esterase gene cloned from a metagenomic library from neritic sediments of the South China Sea. Microb Cell Fact 10:95
57. Ram RJ, Verberkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC 2nd, Shah M, Hettich RL, Banfield JF (2005) Community proteomics of a natural microbial biofilm. Science 308:1915–1920
58. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394
59. Robertson DE, Chaplin JA, DeSantis G, Podar M, Madden M, Chi E, Richardson T, Milan A, Miller M, Weiner DP, Wong K, McQuaid J, Farwell B, Preston LA, Tan X, Snead MA, Keller M, Mathur E, Kretz PL, Burk MJ, Short JM (2004) Exploring nitrilase sequence space for enantioselective catalysis. Appl Environ Microbiol 70:2429–2436
60. Satoh T, Hosokawa M (2006) Structure, function and regulation of carboxylesterases. Chem Biol Interact 162:195–211
61. Schmeisser C, Steele H, Streit WR (2007) Metagenomics, biotechnology with non-culturable microbes. Appl Microbiol Biotechnol 75:955–962
62. Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Puhler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorholter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004
63. Schultz SG, Solomon AK (1961) Cation transport in Escherichia coli. I. Intracellular Na and K concentrations and net cation movement. J Gen Physiol 45:355–369
64. Schutte M, Fetzner S (2007) EstA from Arthrobacter nitroguajacolicus Ru61a, a thermo- and solvent-tolerant carboxylesterase related to class C beta-lactamases. Curr Microbiol 54:230–236
65. Sehgal AC, Tompson R, Cavanagh J, Kelly RM (2002) Structural and catalytic response to temperature and cosolvents of carboxylesterase EST1 from the extremely thermoacidophilic archaeon Sulfolobus solfataricus P1. Biotechnol Bioeng 80:784–793
66. Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433
67. Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161
68. Srimathi S, Jayaraman G, Feller G, Danielsson B, Narayanan PR (2007) Intrinsic halotolerance of the psychrophilic alpha-amylase from Pseudoalteromonas haloplanktis. Extremophiles 11:505–515
69. Steele HL, Jaeger KE, Daniel R, Streit WR (2009) Advances in recovery of novel biocatalysts from metagenomes. J Mol Microbiol Biotechnol 16:25–37
70. Strynadka NC, Adachi H, Jensen SE, Johns K, Sielecki A, Betzel C, Sutoh K, James MN (1992) Molecular structure of the acyl-enzyme intermediate in beta-lactam hydrolysis at 1.7 A resolution. Nature 359:700–705
71. Tan TC, Mijts BN, Swaminathan K, Patel BK, Divne C (2008) Crystal structure of the polyextremophilic alpha-amylase AmyB from Halothermothrix orenii: details of a productive enzyme-substrate complex and an N domain with a role in binding raw starch. J Mol Biol 378:852–870
72. Teeraphatpornchai T, Nakajima-Kambe T, Shigeno-Akutsu Y, Nakayama M, Nomura N, Nakahara T, Uchiyama H (2003) Isolation and characterization of a bacterium that degrades various polyester-based biodegradable plastics. Biotechnol Lett 25:23–28
73. Toone EJ, Werth MJ, Jones JB (1990) Active site model for interpreting and predicting the specificity of pig liver esterase. J Am Chem Soc 112:4946–4952
74. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43
75. Uchiyama T, Miyazaki K (2009) Functional metagenomics for enzyme discovery: challenges to efficient screening. Curr Opin Biotechnol 20:616–622
76. Vedadi M, Niesen FH, Allali-Hassani A, Fedorov OY, Finerty PJ Jr, Wasney GA, Yeung R, Arrowsmith C, Ball LJ, Berglund H, Hui R, Marsden BD, Nordlund P, Sundstrom M, Weigelt J, Edwards AM (2006) Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination. Proc Natl Acad Sci U S A 103:15835–15840
77. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74
78. Vieites JM, Guazzaroni ME, Beloqui A, Golyshin PN, Ferrer M (2009) Metagenomics approaches in systems microbiology. FEMS Microbiol Rev 33:236–255
79. Wagner UG, Petersen EI, Schwab H, Kratky C (2002) EstB from Burkholderia gladioli: a novel esterase with a beta-lactamase fold reveals steric factors to discriminate between esterolytic and beta-lactam cleaving activity. Protein Sci 11:467–478
80. Wilkins D, Yau S, Williams TJ, Allen MA, Brown MV, DeMaere MZ, Lauro FM, Cavicchioli R (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37:303–335
81. Yakimov MM, Golyshin PN, Lang S, Moore ER, Abraham WR, Lunsdorf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48:339–348
82. Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W, Jaroszewski L, Cieplak P, Miller CS, Li H, Mashiyama ST, Joachimiak MP, van Belle C, Chandonia JM, Soergel DA, Zhai Y, Natarajan K, Lee S, Raphael BJ, Bafna V, Friedman R, Brenner SE, Godzik A, Eisenberg D, Dixon JE, Taylor SS, Strausberg RL, Frazier M, Venter JC (2007) The Sorcerer II Global Ocean Sampling expedition: expanding the universe of protein families. PLoS Biol 5:e16
83. Zhu L-M, Tedford MC (1990) Application of pig liver esterases (PLE) in asymetric synthesis. Tetrahedron 46:6587–6611