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References

  1. Arpigny JL, Jaeger KE. 1999. Bacterial lipolytic enzymes:classification and properties. Biochem. J. 343: 177-183.
    CrossRef
  2. Bornscheuer UT. 2002. Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol. Rev. 26: 73-81.
    CrossRef
  3. Chen IC, Lin WD, Hsu SK, Thiruvengadam V, Hsu WH. 2009. Isolation and characterization of a novel lysine racemase from a soil metagenomic library. Appl. Environ. Microbiol. 75:5161-5166.
    CrossRef
  4. 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: 615625.
    CrossRef
  5. Chung EJ, Lim HK, Kim JC, Choi GJ, Park EJ, Lee MH, et al. 2008. Forest soil metagenome gene cluster involved in antifungal activity expression in Escherichia coli. Appl. Environ. Microbiol. 74: 723-730.
    CrossRef
  6. Fang Z, Fang W, Liu J, Hong Y, Peng H, Zhang X, et al. 2010. Cloning and characterization of a beta-glucosidase from marine microbial metagenome with excellent glucose tolerance. J. Microbiol. Biotechnol. 20: 1351-1358.
    CrossRef
  7. Fang Z, Li T, Wang Q, Zhang X, Peng H, Fang W, et al. 2011. A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Appl. Microbiol. Biotechnol. 89: 1103-1110.
    CrossRef
  8. Fu C, Hu Y, Xie F, Guo H, Ashforth EJ, Polyak SW, et al. 2011. Molecular cloning and characterization of a new cold active esterase from a deep-sea metagenomic library. Appl. Microbiol. Biotechnol. 90: 961-970.
    CrossRef
  9. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
    CrossRef
  10. 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.
    CrossRef
  11. 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.
  12. Hess M, Katzer M, Antranikian G. 2008. Extremely thermostable esterases from the thermoacidophilic euryarchaeon Picrophilus torridus. Extremophiles 12: 351-364.
    CrossRef
  13. Hu Y, Fu C, Huang Y, Yin Y, Cheng G, Lei F, et al. 2010. Novel lipolytic genes from the microbial metagenomic library of t he S outh C hina S ea m arine sediment. FEMS Microbiol. Ecol. 72: 228-237.
    CrossRef
  14. Hu Y, Zhang G, Li A, Chen J, Ma L. 2008. Cloning and enzymatic characterization of a xylanase gene from a soilderived metagenomic library with an efficient approach. Appl. Microbiol. Biotechnol. 80: 823-830.
    CrossRef
  15. Jaeger KE, Dijkstra BW, Reetz MT. 1999. Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu. Rev. Microbiol. 53: 315-351.
    CrossRef
  16. Jaeger KE, Reetz MT. 1998. Microbial lipases form versatile tools for biotechnology. Trends Biotechnol. 16: 396-403.
    CrossRef
  17. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403-405.
    CrossRef
  18. 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.
    CrossRef
  19. Jeon JH, Kim JT, Lee HS, Kim SJ, Kang SG, Choi SH, Lee JH. 2011. Novel lipolytic enzymes identified from metagenomic library of deep-sea sediment. Evid. Based Complement. Alternat. Med. 2011: 271419.
    CrossRef
  20. Jiang X , Huo Y, C heng H , Zhang X, Z hu X , Wu M . 2012. Cloning, expression and characterization of a halotolerant esterase from a marine bacterium Pelagibacterium halotolerans B2T. Extremophiles 16: 427-435.
    CrossRef
  21. Kennedy J, Marchesi JR, Dobson AD. 2008. Marine metagenomics: strategies for the discovery of novel enzymes with biotechnological applications from marine environments. Microb. Cell Fact. 7: 27.
    CrossRef
  22. 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.
    CrossRef
  23. LeCleir GR, Buchan A, Maurer J, Moran MA, Hollibaugh JT. 2007. Comparison of chitinolytic enzymes from an alkaline, hypersaline lake and an estuary. Environ. Microbiol. 9: 197205.
    CrossRef
  24. Lee MH, Hong KS, Malhotra S, Park JH, Hwang EC, Choi HK, et al. 2010. A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Appl. Microbiol. Biotechnol. 88:1125-1134.
    CrossRef
  25. 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.
    CrossRef
  26. Lorenz P, Eck J. 2005. Metagenomics and industrial applications. Nat. Rev. Microbiol. 3: 510-516.
    CrossRef
  27. Panda T, Gowrishankar BS. 2005. Production and applications of esterases. Appl. Microbiol. Biotechnol. 67: 160-169.
    CrossRef
  28. Park HJ, Jeon JH, Kang SG, Lee JH, Lee SA, Kim HK. 2007. Functional expression and refolding of new alkaline esterase, EM2L8 from deep-sea sediment metagenome. Protein Expr. Purif. 52: 340-347.
    CrossRef
  29. Peng Q, Zhang X, Shang M, Wang X, Wang G, Li B, et al. 2011. A novel esterase gene cloned from a metagenomic library from neritic sediments of the South China Sea. Microb. Cell Fact. 10: 95.
    CrossRef
  30. 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.
    CrossRef
  31. Rhee JK, Ahn DG, Kim YG, Oh JW. 2005. New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl. Environ. Microbiol. 71: 817-825.
    CrossRef
  32. Saerens K, Descamps D, Dewettinck K. 2008. Release of short chain fatty acids from cream lipids by commercial lipases and esterases. Biotechnol. Lett. 30: 311-315.
    CrossRef
  33. Schloss PD, Handelsman J. 2003. Biotechnological prospects from metagenomics. Curr. Opin. Biotechnol. 14: 303-310.
    CrossRef
  34. Schmidt-Dannert C, Sztajer H, Stocklein W, Menge U, Schmid RD. 1994. Screening, purification and properties of a thermophilic lipase from Bacillus thermocatenulatus. Biochim. Biophys. Acta 1214: 43-53.
  35. Sharma S, Khan FG, Qazi GN. 2010. Molecular cloning and characterization of amylase from soil metagenomic library derived from Northwestern Himalayas. Appl. Microbiol. Biotechnol. 86: 1821-1828.
    CrossRef
  36. Sheridan PP, Panasik N, Coombs JM, Brenchley JE. 2000. Approaches for deciphering the structural basis of low temperature enzyme activity. Biochim. Biophys. Acta 1543:417-433.
    CrossRef
  37. Singh A, Singh Chauhan N, Thulasiram HV, Taneja V, Sharma R. 2010. Identification of two flavin monooxygenases from an effluent treatment plant sludge metagenomic library. Bioresour. Technol. 101: 8481-8484.
    CrossRef
  38. Sleator RD, Shortall C, Hill C. 2008. Metagenomics. Lett. Appl. Microbiol. 47: 361-366.
    CrossRef
  39. 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.
    CrossRef
  40. Voget S, Leggewie C, Uesbeck A, Raasch C, Jaeger KE, Streit WR. 2003. Prospecting for novel biocatalysts in a soil metagenome. Appl. Environ. Microbiol. 69: 6235-6242.
    CrossRef
  41. Waschkowitz T, Rockstroh S, Daniel R. 2009. Isolation and characterization of metalloproteases with a novel domain structure by construction and screening of metagenomic libraries. Appl. Environ. Microbiol. 75: 2506-2516.
    CrossRef
  42. Wu GJ, Zhang S, Zhang HJ, Zhan SS, Liu ZD. 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.
    CrossRef
  43. Zhang YJ, Zhang XY, Mi ZH, Chen CX, Gao ZM, Chen XL, et al. 2011. Glaciecola arctica sp. nov., isolated from Arctic marine sediment. Int. J. Syst. Evol. Microbiol. 61: 2338-2341.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(6): 771-780

Published online June 28, 2014 https://doi.org/10.4014/jmb.1311.11071

Copyright © The Korean Society for Microbiology and Biotechnology.

A Novel Esterase from a Marine Metagenomic Library Exhibiting Salt Tolerance Ability

Zemin Fang 1, 2, Jingjing Li 1, 2, Quan Wang 1, 2, Wei Fang 1, 2, Hui Peng 1, 2, Xuecheng Zhang 1, 2 and Yazhong Xiao 1, 2*

1School of Life Sciences, Anhui University, Hefei, Anhui 230601, China, 2Anhui Provincial Engineering Technology Research Center of Microorganisms and Biocatalysis, Hefei, Anhui 230601, China

Received: November 22, 2013; Accepted: March 11, 2014

Abstract

A putative lipolytic enzyme gene, named as est9x, was obtained from a marine microbial
metagenome of the South China Sea. Sequence analysis showed that Est9X shares lower than
27% sequence identities with the characterized lipolytic enzymes, but possesses a catalytic
triad highly conserved in lipolytic enzymes of the α/β hydrolase superfamily. By phylogenetic
tree construction, Est9X was grouped into a new lipase/esterase family. To understand Est9X
protein in depth, it was recombinantly expressed, purified, and biochemically characterized.
Within potential hydrolytic activities, only lipase/esterase activity was detected for Est9X,
confirming its identity as a lipolytic enzyme. When using p-nitrophenol esters with varying
lengths of fatty acid as substrates, Est9X exhibited the highest activity to the C2 substrate,
indicating it is an esterase. The optimal activity of Est9X occurred at a temperature of 65°C,
and Est9X was pretty stable below the optimum temperature. Distinguished from other salttolerant
esterases, Est9X’s activity was tolerant to and even promoted by as high as 4 M NaCl.
Our results imply that Est9X is a unique esterase and could be a potential candidate for
industrial application under extreme conditions.

Keywords: Esterase, Marine metagenome, Salt tolerance

References

  1. Arpigny JL, Jaeger KE. 1999. Bacterial lipolytic enzymes:classification and properties. Biochem. J. 343: 177-183.
    CrossRef
  2. Bornscheuer UT. 2002. Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol. Rev. 26: 73-81.
    CrossRef
  3. Chen IC, Lin WD, Hsu SK, Thiruvengadam V, Hsu WH. 2009. Isolation and characterization of a novel lysine racemase from a soil metagenomic library. Appl. Environ. Microbiol. 75:5161-5166.
    CrossRef
  4. 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: 615625.
    CrossRef
  5. Chung EJ, Lim HK, Kim JC, Choi GJ, Park EJ, Lee MH, et al. 2008. Forest soil metagenome gene cluster involved in antifungal activity expression in Escherichia coli. Appl. Environ. Microbiol. 74: 723-730.
    CrossRef
  6. Fang Z, Fang W, Liu J, Hong Y, Peng H, Zhang X, et al. 2010. Cloning and characterization of a beta-glucosidase from marine microbial metagenome with excellent glucose tolerance. J. Microbiol. Biotechnol. 20: 1351-1358.
    CrossRef
  7. Fang Z, Li T, Wang Q, Zhang X, Peng H, Fang W, et al. 2011. A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Appl. Microbiol. Biotechnol. 89: 1103-1110.
    CrossRef
  8. Fu C, Hu Y, Xie F, Guo H, Ashforth EJ, Polyak SW, et al. 2011. Molecular cloning and characterization of a new cold active esterase from a deep-sea metagenomic library. Appl. Microbiol. Biotechnol. 90: 961-970.
    CrossRef
  9. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
    CrossRef
  10. 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.
    CrossRef
  11. 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.
  12. Hess M, Katzer M, Antranikian G. 2008. Extremely thermostable esterases from the thermoacidophilic euryarchaeon Picrophilus torridus. Extremophiles 12: 351-364.
    CrossRef
  13. Hu Y, Fu C, Huang Y, Yin Y, Cheng G, Lei F, et al. 2010. Novel lipolytic genes from the microbial metagenomic library of t he S outh C hina S ea m arine sediment. FEMS Microbiol. Ecol. 72: 228-237.
    CrossRef
  14. Hu Y, Zhang G, Li A, Chen J, Ma L. 2008. Cloning and enzymatic characterization of a xylanase gene from a soilderived metagenomic library with an efficient approach. Appl. Microbiol. Biotechnol. 80: 823-830.
    CrossRef
  15. Jaeger KE, Dijkstra BW, Reetz MT. 1999. Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annu. Rev. Microbiol. 53: 315-351.
    CrossRef
  16. Jaeger KE, Reetz MT. 1998. Microbial lipases form versatile tools for biotechnology. Trends Biotechnol. 16: 396-403.
    CrossRef
  17. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403-405.
    CrossRef
  18. 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.
    CrossRef
  19. Jeon JH, Kim JT, Lee HS, Kim SJ, Kang SG, Choi SH, Lee JH. 2011. Novel lipolytic enzymes identified from metagenomic library of deep-sea sediment. Evid. Based Complement. Alternat. Med. 2011: 271419.
    CrossRef
  20. Jiang X , Huo Y, C heng H , Zhang X, Z hu X , Wu M . 2012. Cloning, expression and characterization of a halotolerant esterase from a marine bacterium Pelagibacterium halotolerans B2T. Extremophiles 16: 427-435.
    CrossRef
  21. Kennedy J, Marchesi JR, Dobson AD. 2008. Marine metagenomics: strategies for the discovery of novel enzymes with biotechnological applications from marine environments. Microb. Cell Fact. 7: 27.
    CrossRef
  22. 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.
    CrossRef
  23. LeCleir GR, Buchan A, Maurer J, Moran MA, Hollibaugh JT. 2007. Comparison of chitinolytic enzymes from an alkaline, hypersaline lake and an estuary. Environ. Microbiol. 9: 197205.
    CrossRef
  24. Lee MH, Hong KS, Malhotra S, Park JH, Hwang EC, Choi HK, et al. 2010. A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Appl. Microbiol. Biotechnol. 88:1125-1134.
    CrossRef
  25. 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.
    CrossRef
  26. Lorenz P, Eck J. 2005. Metagenomics and industrial applications. Nat. Rev. Microbiol. 3: 510-516.
    CrossRef
  27. Panda T, Gowrishankar BS. 2005. Production and applications of esterases. Appl. Microbiol. Biotechnol. 67: 160-169.
    CrossRef
  28. Park HJ, Jeon JH, Kang SG, Lee JH, Lee SA, Kim HK. 2007. Functional expression and refolding of new alkaline esterase, EM2L8 from deep-sea sediment metagenome. Protein Expr. Purif. 52: 340-347.
    CrossRef
  29. Peng Q, Zhang X, Shang M, Wang X, Wang G, Li B, et al. 2011. A novel esterase gene cloned from a metagenomic library from neritic sediments of the South China Sea. Microb. Cell Fact. 10: 95.
    CrossRef
  30. 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.
    CrossRef
  31. Rhee JK, Ahn DG, Kim YG, Oh JW. 2005. New thermophilic and thermostable esterase with sequence similarity to the hormone-sensitive lipase family, cloned from a metagenomic library. Appl. Environ. Microbiol. 71: 817-825.
    CrossRef
  32. Saerens K, Descamps D, Dewettinck K. 2008. Release of short chain fatty acids from cream lipids by commercial lipases and esterases. Biotechnol. Lett. 30: 311-315.
    CrossRef
  33. Schloss PD, Handelsman J. 2003. Biotechnological prospects from metagenomics. Curr. Opin. Biotechnol. 14: 303-310.
    CrossRef
  34. Schmidt-Dannert C, Sztajer H, Stocklein W, Menge U, Schmid RD. 1994. Screening, purification and properties of a thermophilic lipase from Bacillus thermocatenulatus. Biochim. Biophys. Acta 1214: 43-53.
  35. Sharma S, Khan FG, Qazi GN. 2010. Molecular cloning and characterization of amylase from soil metagenomic library derived from Northwestern Himalayas. Appl. Microbiol. Biotechnol. 86: 1821-1828.
    CrossRef
  36. Sheridan PP, Panasik N, Coombs JM, Brenchley JE. 2000. Approaches for deciphering the structural basis of low temperature enzyme activity. Biochim. Biophys. Acta 1543:417-433.
    CrossRef
  37. Singh A, Singh Chauhan N, Thulasiram HV, Taneja V, Sharma R. 2010. Identification of two flavin monooxygenases from an effluent treatment plant sludge metagenomic library. Bioresour. Technol. 101: 8481-8484.
    CrossRef
  38. Sleator RD, Shortall C, Hill C. 2008. Metagenomics. Lett. Appl. Microbiol. 47: 361-366.
    CrossRef
  39. 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.
    CrossRef
  40. Voget S, Leggewie C, Uesbeck A, Raasch C, Jaeger KE, Streit WR. 2003. Prospecting for novel biocatalysts in a soil metagenome. Appl. Environ. Microbiol. 69: 6235-6242.
    CrossRef
  41. Waschkowitz T, Rockstroh S, Daniel R. 2009. Isolation and characterization of metalloproteases with a novel domain structure by construction and screening of metagenomic libraries. Appl. Environ. Microbiol. 75: 2506-2516.
    CrossRef
  42. Wu GJ, Zhang S, Zhang HJ, Zhan SS, Liu ZD. 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.
    CrossRef
  43. Zhang YJ, Zhang XY, Mi ZH, Chen CX, Gao ZM, Chen XL, et al. 2011. Glaciecola arctica sp. nov., isolated from Arctic marine sediment. Int. J. Syst. Evol. Microbiol. 61: 2338-2341.
    CrossRef