Abstract
A esterase gene was characterized from a halophilic bacterium Chromohalobacter canadensis which was originally isolated from a salt well mine. Sequence analysis showed that the esterase, named as EstSHJ2, contained active site serine encompassed by a conserved pentapeptide motif (GSSMG). The EstSHJ2 was classified into a new lipase/esterase family by phylogenetic association analysis. Molecular weight of EstSHJ2 was 26 kDa and the preferred substrate was p-NP butyrate. The EstSHJ2 exhibited a maximum activity at 2.5 M NaCl concentration. Intriguingly, the optimum temperature, pH and stability of EstSHJ2 were related to NaCl concentration. At 2.5 M NaCl concentration, the optimum temperature and pH of EstSHJ2 were 65 ℃ and pH 9.0, and enzyme remained 81% active after 80 ℃ treatment for 2 h. Additionally, the EstSHJ2 showed strong tolerance to metal ions and organic solvents. Among these, 10 mM K+, Ca2+ , Mg2+ and 30% hexane, benzene, toluene has significantly improved activity of EstSHJ2. The EstSHJ2 was the first reported esterase from Chromohalobacter canadensis, and may carry considerable potential for industrial applications under extreme conditions.
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References
Aiyar A (2000) The use of CLUSTAL W and CLUSTAL X for multiple sequence alignment. Methods Mol Biol 132:221–241. https://doi.org/10.1385/1-59259-192-2:221
Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43:534–552. https://doi.org/10.1016/j.plipres.2004.09.002
Arpigny JL, Jaeger KE (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343:177–183. https://doi.org/10.1042/0264-6021:3430177
Barone R, De Santi C, Palma Esposito F, Tedesco P, Galati F, Visone M (2014) Marine metagenomics, a valuable tool for enzymes and bioactive compounds discovery. Front Mar Sci 1:1–6. https://doi.org/10.3389/fmars.2014.00038
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 classifcation. Rev Argent Microbiol 45:3–12. https://doi.org/10.2147/0TT.S44474
Bornscheuer UT (2002) Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol Rev 26:73–81. https://doi.org/10.1016/S0168-6445(01)00075-4
Camacho RM, Mateos JC, González-Reynoso O, Prado LA, Córdova J (2009) Production and characterization of esterase and lipase from Haloarcula marismortui. J Ind Microbiol Biot 36:901–909. https://doi.org/10.1007/s10295-009-0568-1
Camacho RM, Mateos-Díaz JC, Diaz-Montaño DM, González-Reynoso O, Córdova J (2010) Carboxyl ester hydrolases production and growth of a halophilic archaeon, Halobacterium sp. NRC-1. Extremophiles 14:99–106. https://doi.org/10.1007/s00792-009-0291-x
Castilla A, Panizza P, Rodríguez D, Bonino L, Díaz P, Irazoqui G, Giordano SR (2017) A novel thermophilic and halophilic esterase from Janibacter sp. R02, the first member of a new lipase family (Family XVII). Enzyme Microb Tech 98:86–95. https://doi.org/10.1016/j.enzmictec.2016.12.010
Chauhan M, Garlapati VK (2013) Production and characterization of a halo-, solvent-, thermo-tolerant alkaline lipase by Staphylococcus arlettae JPBW-1, isolated from rock salt mine. Appl Biochem Biotech 171:1429–1443. https://doi.org/10.1007/s12010-013-0433-6
Dalmaso G, Ferreira D, Vermelho A (2015) Marine extremophiles: a source of hydrolases for biotechnological applications. Mar Drugs 13:1925–1965. https://doi.org/10.3390/md13041925
De Santi C, Ambrosino L, Tedesco P, de Pascale D (2015) Identification and characterization of a novel salt-tolerant ssterase from a Tibetan glacier metagenomic library. Biotechnol Progr 31:890–899. https://doi.org/10.1002/btpr.2124
De Santi C, Leiros H-KS, Di Scala A, de Pascale D, Altermark B, Willassen N-P (2016) Biochemical characterization and structural analysis of a new cold-active and salt-tolerant esterase from the marine bacterium Thalassospira sp. Extremophiles 20:323–336. https://doi.org/10.1007/s00792-016-0824-z
Doukyu N, Ogino H (2010) Organic solvent-tolerant enzymes. Biochem Eng J 48:270–282. https://doi.org/10.1016/j.bej.2009.09.009
Fang Z, Li J, Wang Q, Fang W, Peng H, Zhang X, **ao Y (2014) A novel esterase from a marine metagenomic library exhibiting salt tolerance ability. J Microbiol Biotechn 24:771–780. https://doi.org/10.4014/jmb.1311.11071
Ferrer M, Golyshina OV, Chernikova TN, Khachane AN, Martins dos Santos VAP, Yakimov MM, Timmis KN, Golyshin PN (2005) Microbial enzymes mined from the Urania deep-sea hypersaline anoxic basin. Chem Biol 12:895–904. https://doi.org/10.1016/j.chembiol.2005.05.020
Forouhar F, Lew S, Seetharaman J, Shastry R, Kohan E, Maglaqui M, Mao L, **ao R, Acton TB, Everett JK, Montelione GT, Tong L, Hunt JF (2012) Crystal structure of the esterase YqiA (YE3661) from Yersinia enterocolitica. Northeast Struct Genom Consortium Target YeR85. https://doi.org/10.2210/pdb4FLE/pdb
Fukuchi S, Yoshimune K, Wakayama M, Moriguchi M, Nishikawa K (2003) Unique amino acid composition of proteins in halophilic bacteria. J Mol Biol 327:347–357. https://doi.org/10.1016/S0022-2836(03)00150-5
Ghati A, Paul G (2015) Purification and characterization of a thermo-halophilic, alkali-stable and extremely benzene tolerant esterase from a thermo-halo tolerant Bacillus cereus strain AGP-03, isolated from “Bakreshwar” hot spring. India Process Biochem 50:771–781. https://doi.org/10.1016/j.procbio.2015.01.026
Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. Appl Microbiol Biot 64:763–781. https://doi.org/10.1007/s00253-004-1568-8
Hasan F, Shah AA, Hameed A (2006) Industrial applications of microbial lipases. Enzyme Microb Tech 39:235–251. https://doi.org/10.1016/j.enzmictec.2005.10.016
Holmquist M (2000) Alpha/Beta-hydrolase fold enzymes: structures, functions and mechanisms. Curr Protein Pept Sci 1:209–235. https://doi.org/10.2174/1389203003381405
Huo YY, Rong Z, Jian SL, Xu CD, Li J, Xu XW (2017) A novel halotolerant thermoalkaliphilic esterase from marine bacterium Erythrobacter seohaensis SW-135. Front Microbiol 8:1–11. https://doi.org/10.1016/10.3389/fmicb.2017.02315
Jeon JH, Lee HS, Kim JT, Kim S-J, 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 Biot 93:623–631. https://doi.org/10.1007/s00253-011-3433-x
Jiang X, Huo Y, Cheng H, Zhang X, Zhu X, Wu M (2012) Cloning, expression and characterization of a halotolerant esterase from a marine bacterium Pelagibacterium halotolerans B2T. Extremophiles. 16: 427–435. https://doi.org/10.1016/j.molcatb.2013.09.002
Joseph B, Ramteke PW, Thomas G (2008) Cold active microbial lipases: some hot issues and recent developments. Biotechnol Adv 26:457–470. https://doi.org/10.1016/j.biotechadv.2008.05.003
Kapoor M, Gupta MN (2012) Lipase promiscuity and its biochemical applications. Process Biochem 47:555–569. https://doi.org/10.1016/j.procbio.2012.01.011
Kelly SA, Megaw J, Caswell J, Scott CJ, Allen CCR, Moody TS, Gilmore BF (2017) Isolation and characterisation of a halotolerant ω-transaminase from a Triassic period salt mine and its application to biocatalysis. ChemistrySelect 2:9783–9791. https://doi.org/10.1002/slct.201701642
Ke M, Ramesh B, Hang Y, Liu Z (2018) Engineering and characterization of a novel low temperature active and thermo stable esterase from marine Enterobacter cloacae. Int J Biol Macromol 118:304–310. https://doi.org/10.1016/j.ijbiomac.2018.05.193
Kumar L, Singh B, Adhikari DK, Mukherjee J, Ghosh D (2012) A thermoalkaliphilic halotolerant esterase from Rhodococcus sp. LKE-028 (MTCC 5562): enzyme purification and characterization. Process Biochem 47:983–991. https://doi.org/10.1016/j.procbio.2012.03.020
Lee D-W, Koh Y-S, Kim K-J, Kim B-C, Choi H-J, Kim D-S, Suhartono MT, Pyun Y-R (1999) Isolation and characterization of a thermophilic lipase from Bacillus thermoleovorans ID-1. FEMS Microbiol Lett 179:393–400. https://doi.org/10.1016/s0378-1097(99)00440-1
López-López O, Cerdán ME, González Siso MI (2014) New extremophilic lipases and esterases from metagenomics. Curr Protein Pept Sci 15:445–455. https://doi.org/10.2174/1389203715666140228153801
Manco G, Adinolfi E, Pisani FM, Ottolina G, Carrea G, Rossi M (1998) Overexpression and properties of a new thermophilic and thermostable esterase from Bacillus acidocaldarius with sequence similarity to hormone-sensitive lipase subfamily. Biochem J 332:203–212. https://doi.org/10.1042/bj3320203
Moreno ML, Márquez MC, García MT, Mellado E (2016) Halophilic bacteria and archaea as producers of lipolytic enzymes. Biotechnol Extremo 1:375–397. https://doi.org/10.1007/978-3-319-13521-2_13
Müller-Santos M, de Souza EM, de Pedrosa F, O., Mitchell DA, Longhi S, Carrière F, Canaan S, Krieger N, (2009) First evidence for the salt-dependent folding and activity of an esterase from the halophilic archaea Haloarcula marismortui. BBA-Mol Cell Biol L 1791:719–729. https://doi.org/10.1016/j.bbalip.2009.03.006
Ozcan B, Ozyilmaz G, Cihan A, Cokmus C, Caliskan M (2012) Phylogenetic analysis and characterization of lipolytic activity of halophilic archaeal isolates. Microbiology 81:186–194. https://doi.org/10.1134/S0026261712020105
Perez-Jimenez R, Godoy-Ruiz R, Ibarra-Molero B, Sanchez-Ruiz JM (2004) The efficiency of different salts to screen charge interactions in proteins: a Hofmeister effect? Biophy J 86:2414–2429. https://doi.org/10.1016/S0006-3495(04)74298-8
Rao L, Zhao X, Pan F, Li Y, Xue Y, Ma Y, Lu JR (2009) Solution behavior and activity of a halophilic esterase under high salt concentration. PLoS ONE 4:e6980. https://doi.org/10.1371/journal.pone.0006980
Rahman MA, Culsum U, Tang W, Zhang SW, Wu G, Liu Z (2016) Characterization of a novel cold active and salt tolerant esterase from Zunongwangia profunda. Enzyme Microb Tech 85:1–11. https://doi.org/10.1016/j.enzmictec.2015.12.013
Rashid N, Shimada Y, Ezaki S, Atomi H (2001) Low-temperature lipase from psychrotrophic Pseudomonas sp. strain kb700a. Appl Environ Microb 67:4064–4069. https://doi.org/10.1002/cbic.200900080
Rúa ML, Díaz-Mauriño T, Fernández VM, Otero C, Ballesteros A (1993) Purification and characterization of two distinct lipases from Candida cylindracea. BBA-Gen Subjects 1156:181–189. https://doi.org/10.1016/0304-4165(93)90134-T
Salihu A, Alam MZ (2015) Solvent tolerant lipases: a review. Process Biochem 50:86–96. https://doi.org/10.1016/j.procbio.2014.10.019
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. https://doi.org/10.1016/j.procbio.2007.05.026
Schreck SD, Grunden AM (2014) Biotechnological applications of halophilic lipases and thioesterases. Appl. Microbiol. Biotechnol. 98: 1011–1021. https://doi.org/10.1007/s00253-013-5417-5
Smichi N, Fendri A, Gargouri Y, Miled N (2015) A high salt-tolerant thermoactive esterase from golden grey mullet: purification, characterization and kinetic properties. J Food Biochem 39:289–299. https://doi.org/10.1111/jfbc.12129
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Wang G, Wang Q, Lin X, Bun Ng T, Yan R, Lin J, Ye X (2016a) A novel cold-adapted and highly salt-tolerant esterase from Alkalibacterium sp. SL3 from the sediment of a soda lake. Sci Rep 6:1–10. https://doi.org/10.1038/srep19494
Wang S, Wang K, Li L, Liu Y (2013) Isolation and characterization of a novel organic solvent-tolerant and halotolerant esterase from a soil metagenomic library. J Mol Catal B- Enzym 95:1–8. https://doi.org/10.1016/j.molcatb.2013.05.015
Wang Y, Xu Y, Zhang Y, Sun A, Hu Y (2018) Functional characterization of salt-tolerant microbial esterase WDEst17 and its use in the generation of optically pure ethyl (R)-3-hydroxybutyrate. Chirality. 30: 769–776. https://doi.org/10.1002/chir.22847
Wang Y, Zhang Y, Sun A, Hu Y (2016b) Characterization of a novel marine microbial esterase and its use to make D-methyl lactate. Chin J Catal 37:1396–1402. https://doi.org/10.1016/S1872-2067(16)62495-6
Wei X, Jiang X, Ye L, Yuan S, Chen Z, Wu M, Yu H (2013) Cloning, expression and characterization of a new enantioselective esterase from a marine bacterium Pelagibacterium halotolerans B2T.J. Mol Catal B-Enzym 97:270–277. https://doi.org/10.1016/j.molcatb.2013.09.002
Wu G, Wu G, Zhan T, Shao Z, Liu Z (2013a) Characterization of a cold-adapted and salt-tolerant esterase from a psychrotrophic bacterium Psychrobacter pacificensis. Extremophiles 17:809–819. https://doi.org/10.1007/s00792-013-0562-4
Wu G, Zhang S, Zhang H, Zhang S, Liu Z (2013b) A novel esterase from a psychrotrophic bacterium Psychrobacter celer 3Pb1 showed cold-adaptation and salt-tolerance. J Mol Catal B-Enzym 98:119–126. https://doi.org/10.1016/j.molcatb.2013.10.012
Wu G, Zhang X, Wei L, Wu G, Kumar A, Mao T, Liu Z (2015) A cold-adapted, solvent and salt tolerant esterase from marine bacterium Psychrobacter pacificensis. Int J Biol Macromol 81:180–187. https://doi.org/10.1016/j.ijbiomac.2015.07.045
**n L, Hui-Ying Y (2013) Purification and characterization of an extracellular esterase with organic solvent tolerance from a halotolerant isolate, Salimicrobium sp. LY19. BMC Biotechnol. 13: 108. https://doi.org/10.1186/1472-6750-13-108
Yang X, Wu L, Xu Y, Ke C, Hu F, **ao 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. MicrobiologyOpen. e00601:1–10. https://doi.org/10.1002/mbo3.601
Zaccai G (2004) The effect of water on protein dynamics. Philos T R Soc B 359:1269–1275. https://doi.org/10.1098/rstb.2004.1503
Zhang W, Xu H, Wu Y, Zeng J, Guo Z, Wang L, Shen C, Qiao D, Cao Y (2018) A new cold-adapted, alkali-stable and highly salt-tolerant esterase from Bacillus licheniformis. Int J Biol Macromol 111:1183–1193. https://doi.org/10.1016/j.ijbiomac.2018.01.152
Zhang Y, Hao J, Zhang Y-Q, Chen X-L, **e B-B, Shi M, Zhou B-C, Zhang Y-Z, Li P-Y (2017) Identification and characterization of a novel salt-tolerant esterase from the deep-sea sediment of the South China Sea. Front Microbiol 8:1–10. https://doi.org/10.3389/fmicb.2017.00441
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This research was supported by Liquor Making Biological Technology and Application of Key Laboratory of Sichuan Province (NJ2018-07).
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All authors contributed to the study conception and design. MW, LA, MPZ, and CW conceived and designed the experiments. MW, LA and MPZ performed the experiments and analyzed the data. MW, CW wrote the manuscript. CW and FQW critically revised manuscript.
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Wang, M., Ai, L., Zhang, M. et al. Characterization of a novel halotolerant esterase from Chromohalobacter canadensis isolated from salt well mine. 3 Biotech 10, 430 (2020). https://doi.org/10.1007/s13205-020-02420-0
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DOI: https://doi.org/10.1007/s13205-020-02420-0