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Molecular cloning, expression and characterization of a novel feruloyl esterase from a soil metagenomic library with phthalate-degrading activity

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Abstract

Objectives

To discover novel feruloyl esterases (FAEs) by the function-driven screening procedure from soil metagenome.

Results

A novel FAE gene bds4 was isolated from a soil metagenomic library and over-expressed in Escherichia coli. The recombinant enzyme BDS4 was purified to homogeneity with a predicted molecular weight of 38.8 kDa. BDS4 exhibited strong activity (57.05 U/mg) toward methyl ferulate under the optimum pH and temperature of 8.0 and 37°C. Based on its amino acid sequence and model substrates specificity, BDS4 was classified as a type-C FAE. The quantity of the releasing ferulic acid can be enhanced significantly in the presence of xylanase compared with BDS4 alone from de-starched wheat bran. In addition, BDS4 can also hydrolyze several phthalates such as diethyl phthalate, dimethyl phthalate and dibutyl phthalate.

Conclusion

The current investigation discovered a novel FAE with phthalate-degrading activity and highlighted the usefulness of metagenomic approaches as a powerful tool for discovery of novel FAEs.

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References

  • Altschul SF, Wootton JC, Gertz EM et al (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J 272(20):5101–5109

    Article  CAS  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamin S, Pradeep S, Sarath Josh M et al (2015) A monograph on the remediation of hazardous phthalates. J Hazard Mater 298:58–72

    Article  CAS  Google Scholar 

  • Benoit I, Danchin EGJ, Bleichrodt RJ, De Vries RP (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotech Lett 30:387–396. https://doi.org/10.1007/s10529-007-9564-6

    Article  CAS  Google Scholar 

  • Brady SF (2007) Construction of soil environmental DNA cosmid libraries and screening for clones that produce biologically active small molecules. Nat Protoc 2:1297–1305

    Article  CAS  Google Scholar 

  • Chen X, Zhang X, Yang Y et al (2015) Biodegradation of an endocrine-disrupting chemical di-n-butyl phthalate by newly isolated Camelimonas sp. and enzymatic properties of its hydrolase. Biodegradation 26:171–182

    Article  CAS  Google Scholar 

  • Cheng F, Sheng J, Cai T et al (2012a) A protease-insensitive feruloyl esterase from China Holstein cow rumen metagenomic library: expression, characterization, and utilization in ferulic acid release from wheat straw. J Agric Food Chem 60:2546–2553. https://doi.org/10.1021/jf204556u

    Article  CAS  PubMed  Google Scholar 

  • Cheng F, Sheng J, Dong R et al (2012b) Novel xylanase from a holstein cattle rumen metagenomic library and its application in xylooligosaccharide and ferulic Acid production from wheat straw. J Agric Food Chem 60:12516–12524

    Article  CAS  Google Scholar 

  • Crepin VF, Faulds CB, Connerton IF (2004) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652. https://doi.org/10.1007/s00253-003-1476-3

    Article  CAS  PubMed  Google Scholar 

  • Dilokpimol A, Mäkelä MR, Aguilar-Pontes MV et al (2016) Diversity of fungal feruloyl esterases: updated phylogenetic classification, properties, and industrial applications. Biotechnol Biofuels 9:1–18. https://doi.org/10.1186/s13068-016-0651-6

    Article  CAS  Google Scholar 

  • Dilokpimol A, Mäkelä MR, Varriale S et al (2018) Fungal feruloyl esterases: functional validation of genome mining based enzyme discovery including uncharacterized subfamilies. New Biotechnol 41:9–14. https://doi.org/10.1016/j.nbt.2017.11.004

    Article  CAS  Google Scholar 

  • Gopalan N, Rodríguez-Duran LV, Saucedo-Castaneda G, Nampoothiri KM (2015) Review on technological and scientific aspects of feruloyl esterases: a versatile enzyme for biorefining of biomass. Biores Technol 193:534–544. https://doi.org/10.1016/j.biortech.2015.06.117

    Article  CAS  Google Scholar 

  • Haase-Aschoff P, Linke D, Nimtz M et al (2013) An enzyme from Auricularia auricula-judae combining both benzoyl and cinnamoyl esterase activity. Process Biochem 48:1872–1878

    Article  CAS  Google Scholar 

  • Hancock JM, Bishop MJ (2004) Dictionary of bioinformatics and computational biology. ORF Finder (Open Reading Frame Finder). Wiley, New Jersey

    Book  Google Scholar 

  • Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685

    Article  CAS  Google Scholar 

  • Koseki T, Hori A, Seki S et al (2009) Characterization of two distinct feruloyl esterases, AoFaeB and AoFaeC, from Aspergillus oryzae. Appl Microbiol Biotechnol 83:689–696. https://doi.org/10.1007/s00253-009-1913-z

    Article  CAS  PubMed  Google Scholar 

  • Li W, Cowley A, Uludag M et al (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Res 43:W580–W584. https://doi.org/10.1093/nar/gkv279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Guo J, Hu Y et al (2018) Identification of a novel feruloyl esterase by functional screening of a soil metagenomic library. Appl Biochem Biotechnol 187(1):1–14

    Google Scholar 

  • Lu Y, Tang F, Wang Y et al (2009) Biodegradation of dimethyl phthalate, diethyl phthalate and di-n-butyl phthalate by Rhodococcus sp. L4 isolated from activated sludge. J Hazard Mater 168:938–943

    Article  CAS  Google Scholar 

  • MacOn MB, Fenton SE (2013) Endocrine disruptors and the breast: early life effects and later life disease. J Mammary Gland Biol Neoplasia 18(1):43–61

    Article  Google Scholar 

  • Moukouli M, Topakas E, Christakopoulos P (2008) Cloning, characterization and functional expression of an alkalitolerant type C feruloyl esterase from Fusarium oxysporum. Appl Microbiol Biotechnol 79:245–254. https://doi.org/10.1007/s00253-008-1432-3

    Article  CAS  PubMed  Google Scholar 

  • Ohlhoff CW, Kirby BM, Van Zyl L et al (2015) An unusual feruloyl esterase belonging to family VIII esterases and displaying a broad substrate range. J Mol Catal B Enzym 118:79–88

    Article  CAS  Google Scholar 

  • Oliveira DM, Mota TR, Oliva B et al (2019) Feruloyl esterases: biocatalysts to overcome biomass recalcitrance and for the production of bioactive compounds. Biores Technol 278:408–423. https://doi.org/10.1016/j.biortech.2019.01.064

    Article  CAS  Google Scholar 

  • Pereira MR, Maester TC, Mercaldi GF et al (2017) From a metagenomic source to a high-resolution structure of a novel alkaline esterase. Appl Microbiol Biotechnol 101:4935–4949. https://doi.org/10.1007/s00253-017-8226-4

    Article  CAS  Google Scholar 

  • Prates JA, Tarbouriech N, Charnock SJ et al (2001) The structure of the feruloyl esterase module of xylanase 10B from Clostridium thermocellum provides insights into substrate recognition. Structure 9(12):1183–1190

    Article  CAS  Google Scholar 

  • Record E, Asther M, Sigoillot C et al (2003) Overproduction of the Aspergillus niger feruloyl esterase for pulp bleaching application. Appl Microbiol Biotechnol 62(4):349–355

    Article  CAS  Google Scholar 

  • Reyes-Duarte D, Ferrer M, García-Arellano H (2012) Functional-based screening methods for lipases, esterases, and phospholipases in metagenomic libraries. Methods Mol Biol 861:101

    Article  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol 6:1–4

    Article  Google Scholar 

  • Shahidi F, Chandrasekara A (2010) Hydroxycinnamates and their in vitro and in vivo antioxidant activities. Phytochem Rev 9:147–170. https://doi.org/10.1007/s11101-009-9142-8

    Article  CAS  Google Scholar 

  • Shu LS, Gang L, Xiao PH, Yu HL (2011) Molecular cloning, overexpression and characterization of a novel feruloyl esterase from a soil metagenomic library. J Mol Microbiol Biotechnol 20:196–203

    Article  Google Scholar 

  • Suzuki K, Hori A, Kawamoto K et al (2014) Crystal structure of a feruloyl esterase belonging to the tannase family: a disulfide bond near a catalytic triad. Proteins: structure. Funct Bioinform 82:2857–2867. https://doi.org/10.1002/prot.24649

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  Google Scholar 

  • Torsvik V, Goksøyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Torsvik V, Daae FL, Sandaa RA, Ovreås L (1998) Novel techniques for analysing microbial diversity in natural and perturbed environments. J Biotechnol 64:53–62

    Article  CAS  Google Scholar 

  • Wang L, Li Z, Zhu M et al (2016) An acidic feruloyl esterase from the mushroom Lactarius hatsudake: a potential animal feed supplement. Int J Biol Macromol 93:290–295

    Article  CAS  Google Scholar 

  • Williamson G, Kroon PA, Faulds CB (1998) Hairy plant polysaccharides: a close shave with microbial esterases. Microbiology 144:2011–2023

    Article  CAS  Google Scholar 

  • Wong DWS, Chan VJ, Liao H, Zidwick MJ (2013) Cloning of a novel feruloyl esterase gene from rumen microbial metagenome and enzyme characterization in synergism with endoxylanases. J Ind Microbiol Biotechnol 40:287–295. https://doi.org/10.1007/s10295-013-1234-1

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Abokitse K, Grosse S et al (2012) New feruloyl esterases to access phenolic acids from grass biomass. Appl Biochem Biotechnol 168(1):129–143

    Article  CAS  Google Scholar 

  • Yang J, Roy A, Zhang Y (2013a) BioLiP: a semi-manually curated database for biologically relevant ligand–protein interactions. Nucleic Acids Res 41:1096–1103

    Article  Google Scholar 

  • Yang J, Roy A, Zhang Y (2013b) Protein–ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment. Bioinformatics 29:2588–2595

    Article  CAS  Google Scholar 

  • Yao J, Chen QL, Shen AX et al (2013) A novel feruloyl esterase from a soil metagenomic library with tannase activity. J Mol Catal B Enzym 95:55–61. https://doi.org/10.1016/j.molcatb.2013.05.026

    Article  CAS  Google Scholar 

  • Yu P, McKinnon JJ, Christensen DA (2011) Hydroxycinnamic acids and ferulic acid esterase in relation to biodegradation of complex plant cell walls. Can J Anim Sci. 85(3):255–267

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the Fundamental Research Funds for the Central Universities (KYYJ201708) and Qing Lan Project of Jiangsu Province.

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Authors and Affiliations

  1. Key Laboratory of Food Processing and Quality Control, College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Shenglu Wu, Fang Nan, Junwei Jiang, Jiarong Qiu, Yueqi Zhang, Beibei Qiao, Shan Li & Zhihong Xin

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  1. Shenglu Wu
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  2. Fang Nan
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  3. Junwei Jiang
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  4. Jiarong Qiu
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  7. Shan Li
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  8. Zhihong Xin
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Correspondence to Zhihong Xin.

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Accession Number

The bds4 gene was deposited in the GenBank database with the accession no. MH445495.

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Wu, S., Nan, F., Jiang, J. et al. Molecular cloning, expression and characterization of a novel feruloyl esterase from a soil metagenomic library with phthalate-degrading activity. Biotechnol Lett 41, 995–1006 (2019). https://doi.org/10.1007/s10529-019-02693-3

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  • DOI: https://doi.org/10.1007/s10529-019-02693-3

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