Applied Microbiology and Biotechnology

, Volume 103, Issue 8, pp 3421–3437 | Cite as

Biochemical profiles of two thermostable and organic solvent–tolerant esterases derived from a compost metagenome

  • Mingji Lu
  • Amélie Dukunde
  • Rolf DanielEmail author
Biotechnologically relevant enzymes and proteins


Owing to the functional versatility and potential applications in industry, interest in lipolytic enzymes tolerant to organic solvents is increasing. In this study, functional screening of a compost soil metagenome resulted in identification of two lipolytic genes, est1 and est2, encoding 270 and 389 amino acids, respectively. The two genes were heterologously expressed and characterized. Est1 and Est2 are thermostable enzymes with optimal enzyme activities at 80 and 70 °C, respectively. A second-order rotatable design, which allows establishing the relationship between multiple variables with the obtained responses, was used to explore the combined effects of temperature and pH on esterase stability. The response curve indicated that Est1, and particularly Est2, retained high stability within a broad range of temperature and pH values. Furthermore, the effects of organic solvents on Est1 and Est2 activities and stabilities were assessed. Notably, Est2 activity was significantly enhanced (two- to tenfold) in the presence of ethanol, methanol, isopropanol, and 1-propanol over a concentration range between 6 and 30% (v/v). For the short-term stability (2 h of incubation), Est2 exhibited high tolerance against 60% (v/v) of ethanol, methanol, isopropanol, DMSO, and acetone, while Est1 activity resisted these solvents only at lower concentrations (below 30%, v/v). Est2 also displayed high stability towards some water-immiscible organic solvents, such as ethyl acetate, diethyl ether, and toluene. With respect to long-term stability, Est2 retained most of its activity after 26 days of incubation in the presence of 30% (v/v) ethanol, methanol, isopropanol, DMSO, or acetone. All of these features indicate that Est1 and Est2 possess application potential.


Carboxylesterases Metagenomic library Second-order rotatable design Thermophilic Organic solvent tolerance 



We thank Dr Silja Brady and Sarah Zachmann for providing assistance. We acknowledge the support of Mingji Lu by “Erasmus Mundus Action 2 – Lotus I Project.”

Author contributions

The manuscript was written through the contributions of all authors. All authors have given approval to the final version of the manuscript.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

253_2019_9695_MOESM1_ESM.pdf (1.8 mb)
ESM 1 (PDF 1797 kb)


  1. Adlercreutz P (2013) Immobilisation and application of lipases in organic media. Chem Soc Rev 42:6406–6436. Google Scholar
  2. Ahmed EH, Raghavendra T, Madamwar D (2010) An alkaline lipase from organic solvent–tolerant Acinetobacter sp. EH28: application for ethyl caprylate synthesis. Bioresour Technol 101:3628–3634. Google Scholar
  3. Alcaide M, Tornés J, Stogios PJ, Xu X, Gertler C, Di Leo R, Bargiela R, Lafraya Á, Guazzaroni M-E, López-Cortés 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 α/β hydrolase family. Biochem J 454:157–166. Google Scholar
  4. Alcaide M, Stogios PJ, Lafraya Á, Tchigvintsev A, Flick R, Bargiela R, Chernikova TN, Reva ON, Hai T, Leggewie CC, Katzke N, La Cono V, Matesanz R, Jebbar M, Jaeger K-E, Yakimov MM, Yakunin AF, Golyshin PN, Golyshina OV, Savchenko A, Ferrer M, MAMBA Consortium (2015) Pressure adaptation is linked to thermal adaptation in salt-saturated marine habitats. Environ Microbiol 17:332–345. Google Scholar
  5. Angkawidjaja C, Koga Y, Takano K, Kanaya S (2012) Structure and stability of a thermostable carboxylesterase from the thermoacidophilic archaeon Sulfolobus tokodaii. FEBS J 279:3071–3084. Google Scholar
  6. Antranikian G, Egorova K (2007) Extremophiles, a unique resource of biocatalysts for industrial biotechnology. In: Physiology and biochemistry of extremophiles. American Society of Microbiology, Washington DC, pp 361–406Google Scholar
  7. Arpigny JL, Jaeger K-E (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343:177. Google Scholar
  8. Auernik KS, Cooper CR, Kelly RM (2008) Life in hot acid: pathway analyses in extremely thermoacidophilic archaea. Curr Opin Biotechnol 19:445–453. Google Scholar
  9. Benaiges MD, Alarcón M, Fuciños P, Ferrer P, Rua M, Valero F (2010) Recombinant Candida rugosa lipase 2 from Pichia pastoris: immobilization and use as biocatalyst in a stereoselective reaction. Biotechnol Prog 26:1252–1258. Google Scholar
  10. Bendtsen JD, Nielsen H, Von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795. Google Scholar
  11. Berlemont R, Spee O, Delsaute M, Lara Y, Schuldes J, Simon C, Power P, Daniel R, Galleni M (2013) Novel organic solvent–tolerant esterase isolated by metagenomics: insights into the lipase/esterase classification. Rev Argent Microbiol 45:3–12Google Scholar
  12. Biver S, Vandenbol M (2013) Characterization of three new carboxylic ester hydrolases isolated by functional screening of a forest soil metagenomic library. J Ind Microbiol Biotechnol 40:191–200. Google Scholar
  13. Bora L (2014) Purification and characterization of highly alkaline lipase from Bacillus licheniformis MTCC 2465: and study of its detergent compatibility and applicability. J Surfactant Deterg 17:889–898. Google Scholar
  14. Bornscheuer UT (2002) Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev 26:73–81. Google Scholar
  15. Box GEP, Hunter JS, Hunter WG (2005) Statistics for experimenters: design, innovation and discovery, 2nd edn. Wiley-Interscience, HobokenGoogle Scholar
  16. Boyineni J, Kim J, Kang BS, Lee C, Jang SH (2014) Enhanced catalytic site thermal stability of cold-adapted esterase EstK by a W208Y mutation. Biochim Biophys Acta, Proteins Proteomics 1844:1076–1082. Google Scholar
  17. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  18. Brault G, Shareck F, Hurtubise Y, Lépine F, Doucet N (2012) Isolation and characterization of EstC, a new cold-active esterase from Streptomyces coelicolor A3(2). PLoS One 7:e32041. Google Scholar
  19. Bunterngsook B, Kanokratana P, Thongaram T, Tanapongpipat S, Uengwetwanit T, Rachdawong S, Vichitsoonthonkul T, Eurwilaichitr L (2010) Identification and characterization of lipolytic enzymes from a peat-swamp forest soil metagenome. Biosci Biotechnol Biochem 74:1848–1854. Google Scholar
  20. 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 Microbiol Biotechnol 80:615–625. Google Scholar
  21. Cook GM, Rainey FA, Patel BKC, Morgan HW (1996) Characterization of a new obligately anaerobic thermophile, Thermoanaerobacter wiegelii sp. nov. Int J Syst Bacteriol 46:123–127. Google Scholar
  22. D’Auria S, Herman P, Lakowicz J, Bertoli E, Tanfani F, Rossi M, Manco G (2000) The thermophilic esterase from Archaeoglobus fulgidus: structure and conformational dynamics at high temperature. Proteins Struct Funct Genet 38:351–360Google Scholar
  23. Dandavate V, Jinjala J, Keharia H, Madamwar D (2009) Production, partial purification and characterization of organic solvent–tolerant lipase from Burkholderia multivorans V2 and its application for ester synthesis. Bioresour Technol 100:3374–3381. Google Scholar
  24. Daniel R (2005) The metagenomics of soil. Nat Rev Microbiol 3:470–478. Google Scholar
  25. Delgado-García M, Valdivia-Urdiales B, Aguilar-González CN, Contreras-Esquivel JC, Rodríguez-Herrera R (2012) Halophilic hydrolases as a new tool for the biotechnological industries. J Sci Food Agric 92:2575–2580. Google Scholar
  26. Dougherty MJ, D’haeseleer P, Hazen TC, Simmons BA, Adams PD, Hadi MZ (2012) Glycoside hydrolases from a targeted compost metagenome, activity screening and functional characterization. BMC Biotechnol 12:38. Google Scholar
  27. Doukyu N, Ogino H (2010) Organic solvent-tolerant enzymes. Biochem Eng J 48:270–282. Google Scholar
  28. Dukunde A, Schneider D, Lu M, Brady S, Daniel R (2017) A novel, versatile family IV carboxylesterase exhibits high stability and activity in a broad pH spectrum. Biotechnol Lett 39:577–587. Google Scholar
  29. Ebrahimi M, Lakizadeh A, Agha-Golzadeh P, Ebrahimie E, Ebrahimi M (2011) Prediction of thermostability from amino acid attributes by combination of clustering with attribute weighting: a new vista in engineering enzymes. PLoS One 6:e23146. Google Scholar
  30. Elend C, Schmeisser C, Leggewie C, Babiak P, Steele HL, Reymond J, Jaeger K, Streit R, Carballeira JD, Streit WR (2006) Isolation and biochemical characterization of two novel metagenome-derived esterases. Appl Environ Microbiol 72:3637–3645. Google Scholar
  31. Faiz O, Colak A, Saglam N, Canakçi S, Beldüz AO (2007) Determination and characterization of thermostable esterolytic activity from a novel thermophilic bacterium Anoxybacillus gonensis A4. J Biochem Mol Biol 40:588–594. Google Scholar
  32. Faulds CB, Pérez-Boada M, Martínez ÁT (2011) Influence of organic co-solvents on the activity and substrate specificity of feruloyl esterases. Bioresour Technol 102:4962–4967. Google Scholar
  33. Ferrer M, Bargiela R, Martínez-Martínez M, Mir J, Koch R, Golyshina OV, Golyshin PN (2015) Biodiversity for biocatalysis: a review of the α/β-hydrolase fold superfamily of esterases-lipases discovered in metagenomes. Biocatal Biotransformation 33:235–249. Google Scholar
  34. Gall MG, Nobili A, Pavlidis IV, Bornscheuer UT (2014) Improved thermostability of a Bacillus subtilis esterase by domain exchange. Appl Microbiol Biotechnol 98:1719–1726. Google Scholar
  35. Gao W, Wu K, Chen L, Fan H, Zhao Z, Gao B, Wang H, Wei D (2016) A novel esterase from a marine mud metagenomic library for biocatalytic synthesis of short-chain flavor esters. Microb Cell Factories 15:41. Google Scholar
  36. Georis J, Esteves FDL, Lamotte-Brasseur J, Bougnet V, Giannotta F, Frère J-M, Devreese B, Granier B (2000) An additional aromatic interaction improves the thermostability and thermophilicity of a mesophilic family 11 xylanase: structural basis and molecular study. Protein Sci 9:466–475. Google Scholar
  37. Glogauer A, Martini VP, Faoro H, Couto GH, Müller-Santos M, Monteiro RA, Mitchell DA, de Souza EM, Pedrosa FO, Krieger N (2011) Identification and characterization of a new true lipase isolated through metagenomic approach. Microb Cell Factories 10:54. Google Scholar
  38. González-González R, Fuciños P, Rúa ML (2017) An overview on extremophilic esterases. In: Extremophilic enzymatic processing of lignocellulosic feedstocks to bioenergy. Springer International Publishing, Cham, pp 181–204Google Scholar
  39. Hardeman F, Sjoling 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. Google Scholar
  40. Hasan F, Shah AA, Hameed A (2006) Industrial applications of microbial lipases. Enzym Microb Technol 39:235–251. Google Scholar
  41. Hausmann S, Jaeger K-E (2010) Lipolytic enzymes from bacteria. In: Handbook of Hydrocarbon and Lipid Microbiology. Springer Berlin Heidelberg, Berlin, pp 1099–1126Google Scholar
  42. Hita E, Robles A, Camacho B, González PA, Esteban L, Jiménez MJ, Muñío MM, Molina E (2009) Production of structured triacylglycerols by acidolysis catalyzed by lipases immobilized in a packed bed reactor. Biochem Eng J 46:257–264. Google Scholar
  43. Hotta Y, Ezaki S, Atomi H, Imanaka T (2002) Extremely stable and versatile carboxylesterase from a hyperthermophilic archaeon. Appl Environ Microbiol 68:3925–3931. Google Scholar
  44. Hu X, Thumarat U, Zhang X, Tang M, Kawai F (2010) Diversity of polyester-degrading bacteria in compost and molecular analysis of a thermoactive esterase from Thermobifida alba AHK119. Appl Microbiol Biotechnol 87:771–779. Google Scholar
  45. Hun CJ, Rahman RNZA, Salleh AB, Basri M (2003) A newly isolated organic solvent–tolerant Bacillus sphaericus 205y producing organic solvent-stable lipase. Biochem Eng J 15:147–151. Google Scholar
  46. Ishikawa J, Hotta K (1999) FramePlot: a new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G + C content. FEMS Microbiol Lett 174:251–263Google Scholar
  47. Jaeger K-E, Dijkstra BW, Reetz MT (1999) Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu Rev Microbiol 53:315–351. Google Scholar
  48. Jayanath G, Mohandas SP, Kachiprath B, Solomon S, Sajeevan TP, Bright Singh IS, Philip R (2018) A novel solvent–tolerant esterase of GDSGG motif subfamily from solar saltern through metagenomic approach: recombinant expression and characterization. Int J Biol Macromol 119:393–401. Google Scholar
  49. Jeon JH, Lee HS, Kim JT, Kim SJ, Choi SH, Kang SG, Lee JH (2012) Identification of a new subfamily of salt-tolerant esterases from a metagenomic library of tidal flat sediment. Appl Microbiol Biotechnol 93:623–631. Google Scholar
  50. Jin P, Pei X, Du P, Yin X, Xiong X, Wu H, Zhou X, Wang Q (2012) Overexpression and characterization of a new organic solvent-tolerant esterase derived from soil metagenomic DNA. Bioresour Technol 116:234–240. Google Scholar
  51. Jochens H, Aerts D, Bornscheuer UT (2010) Thermostabilization of an esterase by alignment-guided focussed directed evolution. Protein Eng Des Sel 23:903–909. Google Scholar
  52. Kamal Z, Yedavalli P, Deshmukh MV, Rao NM (2013) Lipase in aqueous-polar organic solvents: activity, structure, and stability. Protein Sci 22:904–915. Google Scholar
  53. Kamimura ES, Medieta O, Rodrigues MI, Maugeri F (2001) Studies on lipase-affinity adsorption using response surface analysis. Biotechnol Appl Biochem 33:153–159Google Scholar
  54. Kang CH, Oh KH, Lee MH, Oh TK, Kim BH, Yoon JH (2011) A novel family VII esterase with industrial potential from compost metagenomic library. Microb Cell Factories 10:41. Google Scholar
  55. Kang LJ, Meng ZT, Hu C, Zhang Y, Guo HL, Li Q, Li M (2017) Screening, purification, and characterization of a novel organic solvent-tolerant esterase, Lip2, from Monascus purpureus strain M7. Extremophiles 21:345–355. Google Scholar
  56. Kawata T, Ogino H (2009) Enhancement of the organic solvent-stability of the LST-03 lipase by directed evolution. Biotechnol Prog 25:1605–1611. Google Scholar
  57. Kim TD (2017) Bacterial hormone-sensitive lipases (bHSLs): Emerging enzymes for biotechnological applications. J Microbiol Biotechnol 27:1907–1915. Google Scholar
  58. Kim YH, Kwon EJ, Kim SK, Jeong YS, Kim J, Yun HD, Kim H (2010) Molecular cloning and characterization of a novel family VIII alkaline esterase from a compost metagenomic library. Biochem Biophys Res Commun 393:45–49. Google Scholar
  59. Klibanov AM (2001) Improving enzymes by using them in organic solvents. Nature 409:241–246. Google Scholar
  60. Kovacic F, Mandrysch A, Poojari C, Strodel B, Jaeger K-E (2016) Structural features determining thermal adaptation of esterases. Protein Eng Des Sel 29:65–76. Google Scholar
  61. Kumagai PS, Gutierrez RF, Lopes JLS, Martins JM, Jameson DM, Castro AM, Martins LF, DeMarco R, Bossolan NRS, Wallace BA, Araujo APU (2018) Characterization of esterase activity from an Acetomicrobium hydrogeniformans enzyme with high structural stability in extreme conditions. Extremophiles 22:781–793. Google Scholar
  62. Kumar A, Dhar K, Singh Kanwar S, Arora PK (2016) Lipase catalysis in organic solvents: advantages and applications. Biol Proced Online 18:2. Google Scholar
  63. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. Google Scholar
  64. Lämmle K, Zipper H, Breuer M, Hauer B, Buta C, Brunner H, Rupp S (2007) Identification of novel enzymes with different hydrolytic activities by metagenome expression cloning. J Biotechnol 127:575–592. Google Scholar
  65. Lazić ŽR (2004) Design of experiments in chemical engineering. Wiley-VCH Verlag GmbH & Co. KGaA, WeinheimGoogle Scholar
  66. Léonard-Nevers V, Marton Z, Lamare S, Hult K, Graber M (2009) Understanding water effect on Candida antarctica lipase B activity and enantioselectivity towards secondary alcohols. J Mol Catal B Enzym 59:90–95. Google Scholar
  67. Li X, Yu H (2013) Purification and characterization of an extracellular esterase with organic solvent tolerance from a halotolerant isolate, Salimicrobium sp. LY19. BMC Biotechnol 13:108Google Scholar
  68. Li P, Chen X, Ji P, Li C, Wang P, Zhang Y, Xie B, Qin Q, Su H, Zhou B, Zhang Y, Zhang X (2015) Interdomain hydrophobic interactions modulate the thermostability of microbial esterases from the hormone-sensitive lipase family. J Biol Chem 290:11188–11,198.
  69. Lima VMG, Krieger N, Mitchell DA, Baratti JC, de FI, Fontana JD (2004) Evaluation of the potential for use in biocatalysis of a lipase from a wild strain of Bacillus megaterium. J Mol Catal B Enzym 31:53–61. Google Scholar
  70. Lineweaver H, Burk D (1934) The determination of enzyme dissociation constants. J Am Chem Soc 56:658–666. Google Scholar
  71. Lopez-Lopez O, Cerdan M, Siso M (2014) New extremophilic lipases and esterases from metagenomics. Curr Protein Pept Sci 15:445–455. Google Scholar
  72. Lotti M, Alberghina L (2007) Lipases: molecular structure and function. In: Industrial Enzymes. Springer Netherlands, Dordrecht, pp 263–281Google Scholar
  73. Mandelli F, Goncalves TA, Gandin CA, Oliveira ACP, Oliveira Neto M, Squina FM (2016) Characterization and low-resolution structure of an extremely thermostable esterase of potential biotechnological interest from Pyrococcus furiosus. Mol Biotechnol 58:757–766. Google Scholar
  74. Martínez-Martínez M, Coscolín C, Santiago G, Chow J, Stogios PJ, Bargiela R, Gertler C, Navarro-Fernández J, Bollinger A, Thies S, Méndez-García C, Popovic A, Brown G, Chernikova TN, García-Moyano A, Bjerga GEK, Pérez-García P, Hai T, Del Pozo M V., Stokke R, Steen IH, Cui H, Xu X, Nocek BP, Alcaide M, Distaso M, Mesa V, Peláez AI, Sánchez J, Buchholz PCF, Pleiss J, Fernández-Guerra A, Glöckner FO, Golyshina O V., Yakimov MM, Savchenko A, Jaeger K-E, Yakunin AF, Streit WR, Golyshin PN, Guallar V, Ferrer M, The INMARE Consortium TI (2018) Determinants and prediction of esterase substrate promiscuity patterns. ACS Chem Biol 13:225–234. doi:
  75. Metin K, Burcu Bakir Ateslier Z, Basbulbul G, Halil Biyik H (2006) Characterization of esterase activity in Geobacillus sp. HBB-4. J Basic Microbiol 46:400–409. Google Scholar
  76. Mohamed YM, Ghazy MA, Sayed A, Ouf A, El-Dorry H, Siam R (2013) Isolation and characterization of a heavy metal-resistant, thermophilic esterase from a Red Sea Brine Pool. Sci Rep 3:3358. Google Scholar
  77. Monsef Shokri M, Ahmadian S, Akbari N, Khajeh K (2014) Hydrophobic substitution of surface residues affects lipase stability in organic solvents. Mol Biotechnol 56:360–368. Google Scholar
  78. 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. Google Scholar
  79. Nasaruddin RR, Alam MZ, Jami MS (2014) Evaluation of solvent system for the enzymatic synthesis of ethanol-based biodiesel from sludge palm oil (SPO). Bioresour Technol 154:155–161. Google Scholar
  80. Nerurkar M, Joshi M, Pariti S, Adivarekar R (2013) Application of lipase from marine bacteria Bacillus sonorensis as an additive in detergent formulation. J Surfactant Deterg 16:435–443. Google Scholar
  81. Ngo TD, Ryu BH, Ju H, Jang E, Park K, Kim KK, Kim TD (2013) Structural and functional analyses of a bacterial homologue of hormone-sensitive lipase from a metagenomic library. Acta Crystallogr Sect D Biol Crystallogr 69:1726–1737. Google Scholar
  82. Ngo TD, Ryu BH, Ju H, Jang EJ, Kim KK, Kim TD (2014) Crystallographic analysis and biochemical applications of a novel penicillin-binding protein/β-lactamase homologue from a metagenomic library. Acta Crystallogr Sect D Biol Crystallogr 70:2455–2466. Google Scholar
  83. Notredame C, Higgins DG, Heringa J (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217. Google Scholar
  84. Ó’Fágáin C (2003) Enzyme stabilization—recent experimental progress. Enzym Microb Technol 33:137–149. Google Scholar
  85. Ogino H, Ishikawa H (2001) Enzymes which are stable in the presence of organic solvents. J Biosci Bioeng 91:109–116Google Scholar
  86. Ogino H, Mimitsuka T, Muto T, Matsumura M, Yasuda M, Ishimi K, Ishikawa H (2004) Cloning, expression, and characterization of a lipolytic enzyme gene (lip8) from Pseudomonas aeruginosa LST-03. J Mol Microbiol Biotechnol 7:212–223. Google Scholar
  87. Ohlhoff CW, Kirby BM, Van Zyl L, Mutepfa DLR, Casanueva A, Huddy RJ, Bauer R, Cowan DA, Tuffin M (2015) An unusual feruloyl esterase belonging to family VIII esterases and displaying a broad substrate range. J Mol Catal B Enzym 118:79–88. Google Scholar
  88. Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J, Sussman JL, Verschueren KHG, Goldman A (1992) The α/β hydrolase fold. Protein Eng Des Sel 5:197–211. Google Scholar
  89. Panda T, Gowrishankar BS (2005) Production and applications of esterases. Appl Microbiol Biotechnol 67:160–169. Google Scholar
  90. Park HJ, Joo JC, Park K, Yoo YJ (2012) Stabilization of Candida antarctica lipase B in hydrophilic organic solvent by rational design of hydrogen bond. Biotechnol Bioprocess Eng 17:722–728. Google Scholar
  91. Park SH, Kim S, Park S, Kim HK (2018) Characterization of organic solvent-tolerant lipolytic enzyme from Marinobacter lipolyticus isolated from the Antarctic Ocean. Appl Biochem Biotechnol.
  92. 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 Factories 10:95. Google Scholar
  93. Pérez D, Kovačic F, Wilhelm S, Jaeger K-E, García MT, Ventosa A, Mellado EN (2012) Identification of amino acids involved in the hydrolytic activity of lipase LipBL from Marinobacter lipolyticus. Microbiology 158:2192–2203. doi:
  94. Petersen EI, Valinger G, Sölkner B, Stubenrauch G, Schwab H (2001) A novel esterase from Burkholderia gladioli which shows high deacetylation activity on cephalosporins is related to beta-lactamases and DD-peptidases. J Biotechnol 89:11–25Google Scholar
  95. Pezzullo M, Del Vecchio P, Mandrich L, Nucci R, Rossi M, Manco G (2013) Comprehensive analysis of surface charged residues involved in thermal stability in Alicyclobacillus acidocaldarius esterase 2. Protein Eng Des Sel 26:47–58. Google Scholar
  96. Popovic A, Hai T, Tchigvintsev A, Hajighasemi M, Nocek B, Khusnutdinova AN, Brown G, Glinos J, Flick R, Skarina T, Chernikova TN, Yim V, Brüls T, Le PD, Yakimov MM, Joachimiak A, Ferrer M, Golyshina OV, Savchenko A, Golyshin PN, Yakunin AF (2017) Activity screening of environmental metagenomic libraries reveals novel carboxylesterase families. Sci Rep 7:44103. Google Scholar
  97. Rahman RNZRA, Baharum SN, Basri M, Salleh AB (2005) High-yield purification of an organic solvent-tolerant lipase from Pseudomonas sp. strain S5. Anal Biochem 341:267–274. Google Scholar
  98. Raja A, Prabakarana P (2011) Actinomycetes and drug-an overview. Am J Drug Discov Dev 1:75–84. Google Scholar
  99. Rashamuse K, Magomani V, Ronneburg T, Brady D (2009) A novel family VIII carboxylesterase derived from a leachate metagenome library exhibits promiscuous β-lactamase activity on nitrocefin. Appl Microbiol Biotechnol 83:491–500. Google Scholar
  100. Riedel K, Sutherland R, Donato JJ, Liebl W, Leis B, Angelov A, Mientus M, Li H, Pham VTT, Lauinger B, Bongen P, Pietruszka J, Gonçalves LG, Santos H (2015) Identification of novel esterase-active enzymes from hot environments by use of the host bacterium Thermus thermophilus. Front Microbiol 6:27. Google Scholar
  101. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:320–324. Google Scholar
  102. Romdhane IB-B, Fendri A, Gargouri Y, Gargouri A, Belghith H (2010) A novel thermoactive and alkaline lipase from Talaromyces thermophilus fungus for use in laundry detergents. Biochem Eng J 53:112–120. Google Scholar
  103. Ryckeboer J, Mergaert J, Vaes K, Klammer S, Clercq D, Coosemans J, Insam H, Swings J (2003) A survey of bacteria and fungi occurring during composting and self-heating processes. Ann Microbiol 53:349–410Google Scholar
  104. Sadeghi M, Naderi-Manesh H, Zarrabi M, Ranjbar B (2006) Effective factors in thermostability of thermophilic proteins. Biophys Chem 119:256–270. Google Scholar
  105. Sakai Y, Ishikawa J, Fukasaka S, Yurimoto H, Mitsui R, Yanase H, Kato N (1999) A new carboxylesterase from Brevibacterium linens IFO 12171 responsible for the conversion of 1,4-butanediol diacrylate to 4-hydroxybutyl acrylate: purification, characterization, gene cloning, and gene expression in Escherichia coli. Biosci Biotechnol Biochem 63:688–697. Google Scholar
  106. Salihu A, Alam MZ (2015) Solvent tolerant lipases: a review. Process Biochem 50:86–96. Google Scholar
  107. Sana B, Ghosh D, Saha M, Mukherjee J (2007) Purification and characterization of an extremely dimethylsulfoxide tolerant esterase from a salt-tolerant Bacillus species isolated from the marine environment of the Sundarbans. Process Biochem 42:1571–1578. Google Scholar
  108. Sarmah N, Revathi D, Sheelu G, Yamuna Rani K, Sridhar S, Mehtab V, Sumana C (2018) Recent advances on sources and industrial applications of lipases. Biotechnol Prog 34:5–28. Google Scholar
  109. Sayer C, Isupov MN, Bonch-Osmolovskaya E, Littlechild JA (2015a) Structural studies of a thermophilic esterase from a new Planctomycetes species, Thermogutta terrifontis. FEBS J 282:2846–2857. Google Scholar
  110. Sayer C, Szabo Z, Isupov MN, Ingham C, Littlechild JA (2015b) The structure of a novel thermophilic esterase from the Planctomycetes species, Thermogutta terrifontis reveals an open active site due to a minimal “Cap” domain. Front Microbiol 6:1294. Google Scholar
  111. Schütte M, Fetzner S (2007) EstA from Arthrobacter nitroguajacolicus Ru61a, a thermo- and solvent-tolerant carboxylesterase related to class C b-Lactamases. Curr Microbiol 54:230–236. Google Scholar
  112. Secundo F, Carrea G (2002) Lipase activity and conformation in neat organic solvents. J Mol Catal B Enzym 19:93–102. Google Scholar
  113. Selvin J, Kennedy J, Lejon DPH, Kiran GS, Dobson ADW (2012) Isolation identification and biochemical characterization of a novel halo-tolerant lipase from the metagenome of the marine sponge Haliclona simulans. Microb Cell Factories 11:72. Google Scholar
  114. Seo S, Lee YS, Yoon SH, Kim SJ, Cho JY, Hahn BS, Koo BS, Lee CM (2014) Characterization of a novel cold-active esterase isolated from swamp sediment metagenome. World J Microbiol Biotechnol 30:879–886. Google Scholar
  115. Shao H, Xu L, Yan Y (2013) Isolation and characterization of a thermostable esterase from a metagenomic library. J Ind Microbiol Biotechnol 40:1211–1222. Google Scholar
  116. Sharma R, Soni S, Vohra R, Gupta L, Gupta J (2002) Purification and characterisation of a thermostable alkaline lipase from a new thermophilic Bacillus sp. RSJ-1. Process Biochem 37:1075–1084. Google Scholar
  117. Shieh C-J, Liao H-F, Lee C-C (2003) Optimization of lipase-catalyzed biodiesel by response surface methodology. Bioresour Technol 88:103–116Google Scholar
  118. Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microbiol 77:1153–1161. Google Scholar
  119. Song JK, Rhee JS (2001) Enhancement of stability and activity of phospholipase A1 in organic solvents by directed evolution. Biochim Biophys Acta Protein Struct Mol Enzymol 1547:370–378. Google Scholar
  120. Sood S, Sharma A, Sharma N, Kanwar SS (2016) Carboxylesterases: sources, characterization and broader applications. Insights Enzym Res 1:1. Google Scholar
  121. Srimhan P, Kongnum K, Taweerodjanakarn S, Hongpattarakere T (2011) Selection of lipase producing yeasts for methanol-tolerant biocatalyst as whole cell application for palm-oil transesterification. Enzym Microb Technol 48:293–298. Google Scholar
  122. Takeda Y, Aono R, Doukyu N (2006) Purification, characterization, and molecular cloning of organic-solvent-tolerant cholesterol esterase from cyclohexane-tolerant Burkholderia cepacia strain ST-200. Extremophiles 10:269–277. Google Scholar
  123. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. Google Scholar
  124. Tirawongsaroj P, Sriprang R, Harnpicharnchai P, Thongaram T, Champreda V, Tanapongpipat S, Pootanakit K, Eurwilaichitr L (2008) Novel thermophilic and thermostable lipolytic enzymes from a Thailand hot spring metagenomic library. J Biotechnol 133:42–49. Google Scholar
  125. Torres S, Castro GR (2004) Non-aqueous biocatalysis in homogeneous solvent systems. Crit Rev Biotechnol 42:271–277Google Scholar
  126. Torres S, Martínez MA, Pandey A, Castro GR (2009) An organic-solvent-tolerant esterase from thermophilic Bacillus licheniformis S-86. Bioresour Technol 100:896–902. Google Scholar
  127. Wang X, Qin X, Li D, Yang B, Wang Y (2017) One-step synthesis of high-yield biodiesel from waste cooking oils by a novel and highly methanol-tolerant immobilized lipase. Bioresour Technol 235:18–24. Google Scholar
  128. Woo Lee H, Kyeong Jung W, Ho Kim Y, Han Ryu B, Doohun Kim T, Kim J, Kim H (2016) Characterization of a novel alkaline family VIII esterase with s-enantiomer preference from a compost metagenomic library. J Microbiol Biotechnol 26:315–325. Google Scholar
  129. Wu G, Zhang S, Zhang H, Zhang S, Liu Z (2013) A novel esterase from a psychrotrophic bacterium Psychrobacter celer 3Pb1 showed cold-adaptation and salt tolerance. J Mol Catal B Enzym 98:119–126. Google Scholar
  130. Xing MN, Zhang XZ, Huang H (2012) Application of metagenomic techniques in mining enzymes from microbial communities for biofuel synthesis. Biotechnol Adv 30:920–929. Google Scholar
  131. Yang Y, Yu Y, Zhang Y, Liu C, Shi W, Li Q (2011) Lipase/esterase-catalyzed ring-opening polymerization: a green polyester synthesis technique. Process Biochem 46:1900–1908. Google Scholar
  132. Yang X, Wu L, Xu Y, Ke C, Hu F, Xiao X, Huang J (2018) Identification and characterization of a novel alkalistable and salt-tolerant esterase from the deep-sea hydrothermal vent of the East Pacific Rise. Microbiology 7:e00601. Google Scholar
  133. Ye J, McGinnis S, Madden TL (2006) BLAST: improvements for better sequence analysis. Nucleic Acids Res 34:W6–W9. Google Scholar
  134. Yu S, Zheng B, Zhao X, Feng Y (2010) Gene cloning and characterization of a novel thermophilic esterase from Fervidobacterium nodosum Rt17-B1. Acta Biochim Biophys Sin Shanghai 42:288–295. Google Scholar
  135. Yu EY, Kwon MA, Lee M, Oh JY, Choi JE, Lee JY, Song BK, Hahm DH, Song JK (2011) Isolation and characterization of cold-active family VIII esterases from an arctic soil metagenome. Appl Microbiol Biotechnol 90:573–581. Google Scholar
  136. Zarafeta D, Moschidi D, Ladoukakis E, Gavrilov S, Chrysina ED, Chatziioannou A, Kublanov I, Skretas G, Kolisis FN (2016) Metagenomic mining for thermostable esterolytic enzymes uncovers a new family of bacterial esterases. Sci Rep 6:38886. Google Scholar
  137. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 23:40. Google Scholar
  138. Zhang S, Wu G, Liu Z, Shao Z, Liu Z (2014) Characterization of EstB, a novel cold-active and organic solvent-tolerant esterase from marine microorganism Alcanivorax dieselolei B-5(T). Extremophiles 18:251–259. Google Scholar
  139. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Genomic and Applied Microbiology, Göttingen Genomics Laboratory, Institute of Microbiology and GeneticsGeorg-August-University of GöttingenGöttingenGermany

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