Skip to main content
SpringerLink
Log in

Characterization of a Novel One-Domain Halotolerant Laccase from Parageobacillus thermoglucosidasius and Its Application in Dye Decolorization

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Laccases are widespread multi-copper oxidases and generally classified into three-domain laccases and two-domain laccases. In this study, a novel laccase PthLac from Parageobacillus thermoglucosidasius harbored only one domain of Cu-oxidase_4 and showed no sequence relatedness or structure similarity to three-domain and two-domain laccases. PthLac was heterologously expressed in Escherichia coli, purified, and characterized. The optimum temperature and pH of PthLac on guaiacol were at 60 ℃ and pH 6, respectively. The effects of various metal ions on PthLac were analyzed. All the tested metal ions did not suppress the activity of PthLac, except for 10 mM Cu2+, which increased the activity of PthLac to 316%, indicating that PthLac was activated by Cu2+. Meanwhile, PthLac kept 121% and 69% activity when incubated at concentrations of 2.5 and 3 M NaCl for 9 h, suggesting the long-term halotolerancy of this enzyme. In addition, PthLac showed resistance to the organic solvents and surfactants, and displayed dye decolorization capacity. This study enriched our knowledge about one-domain laccase and its potential industrial applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  1. Arregui, L., Ayala, M., Gomez-Gil, X., Gutierrez-Soto, G., Hernandez-Luna, C. E., de Los, H., Santos, M., Levin, L., Rojo-Dominguez, A., Romero-Martinez, D., Saparrat, M. C. N., Trujillo-Roldan, M. A., & Valdez-Cruz, N. A. (2019). Laccases: Structure, function, and potential application in water bioremediation. Microbial Cell Factories, 18(1), 200.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Janusz, G., Pawlik, A., Swiderska-Burek, U., Polak, J., Sulej, J., Jarosz-Wilkolazka, A., Paszczynski, A. (2020). Laccase properties, physiological functions, and evolution. International Journal of Molecular Science, 21(3).

  3. Graff, M., Buchholz, P. C. F., Le Roes-Hill, M., & Pleiss, J. (2020). Multicopper oxidases: Modular structure, sequence space, and evolutionary relationships. Proteins, 88(10), 1329–1339.

    Article  PubMed  Google Scholar 

  4. Melo, E. P., Fernandes, A. T., Durao, P., & Martins, L. O. (2007). Insight into stability of CotA laccase from the spore coat of Bacillus subtilis. Biochemical Society Transactions, 35(Pt 6), 1579–1582.

    Article  PubMed  CAS  Google Scholar 

  5. Enguita, F. J., Martins, L. O., Henriques, A. O., & Carrondo, M. A. (2003). Crystal structure of a bacterial endospore coat component. A laccase with enhanced thermostability properties. Journal of Biological Chemistry, 278(21), 19416–25.

    Article  PubMed  CAS  Google Scholar 

  6. Skalova, T., Dohnalek, J., Ostergaard, L. H., Ostergaard, P. R., Kolenko, P., Duskova, J., Stepankova, A., & Hasek, J. (2009). The structure of the small laccase from Streptomyces coelicolor reveals a link between laccases and nitrite reductases. Journal of Molecular Biology, 385(4), 1165–1178.

    Article  PubMed  CAS  Google Scholar 

  7. Beloqui, A., Pita, M., Polaina, J., Martinez-Arias, A., Golyshina, O. V., Zumarraga, M., Yakimov, M. M., Garcia-Arellano, H., Alcalde, M., Fernandez, V. M., Elborough, K., Andreu, J. M., Ballesteros, A., Plou, F. J., Timmis, K. N., Ferrer, M., & Golyshin, P. N. (2006). Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: Biochemical properties, structural analysis, and phylogenetic relationships. Journal of Biological Chemistry, 281(32), 22933–22942.

    Article  PubMed  CAS  Google Scholar 

  8. Al-Kahem Al-Balawi, T. H., Wood, A. L., Solis, A., Cooper, T., & Barabote, R. D. (2017). Anoxybacillus sp. strain UARK-01, a new thermophilic soil bacterium with hyperthermostable alkaline laccase activity. Current Microbiology, 74(6), 762–771.

    Article  PubMed  CAS  Google Scholar 

  9. De Paula, N. M., da Silva, K., Brugnari, T., Haminiuk, C. W. I., & Maciel, G. M. (2022). Biotechnological potential of fungi from a mangrove ecosystem: Enzymes, salt tolerance and decolorization of a real textile effluent. Microbiological Research, 254, 126899.

    Article  PubMed  Google Scholar 

  10. Chandra, R., & Chowdhary, P. (2015). Properties of bacterial laccases and their application in bioremediation of industrial wastes. Environmental Science Processes & Impacts, 17(2), 326–342.

    Article  CAS  Google Scholar 

  11. Mate, D. M., & Alcalde, M. (2017). Laccase: A multi-purpose biocatalyst at the forefront of biotechnology. Microbial Biotechnology, 10(6), 1457–1467.

    Article  PubMed  CAS  Google Scholar 

  12. Khatami, S. H., Vakili, O., Movahedpour, A., Ghesmati, Z., Ghasemi, H., & Taheri-Anganeh, M. (2022). Laccase: Various types and applications. Biotechnology and Applied Biochemistry, 69(6), 2658–2672.

    Article  PubMed  CAS  Google Scholar 

  13. Vieira, Y. A., Gurgel, D., Henriques, R. O., Machado, R. A. F., de Oliveira, D., Oechsler, B. F., & Furigo Junior, A. (2022). A perspective review on the application of polyacrylonitrile-based supports for laccase immobilization. Chemical Record, 22(2), e202100215.

    Article  PubMed  CAS  Google Scholar 

  14. Su, J., Fu, J., Wang, Q., Silva, C., & Cavaco-Paulo, A. (2018). Laccase: A green catalyst for the biosynthesis of poly-phenols. Critical Reviews in Biotechnology, 38(2), 294–307.

    Article  PubMed  CAS  Google Scholar 

  15. Fang, Z., Li, T., Wang, Q., Zhang, X., Peng, H., Fang, W., Hong, Y., Ge, H., & Xiao, Y. (2011). A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Applied Microbiology and Biotechnology, 89(4), 1103–1110.

    Article  PubMed  CAS  Google Scholar 

  16. Siroosi, M., Amoozegar, M. A., & Khajeh, K. (2016). Purification and characterization of an alkaline chloride-tolerant laccase from a halotolerant bacterium, Bacillus sp. strain WT. Journal of Molecular Catalysis B: Enzymatic, 134, 89–97.

    Article  CAS  Google Scholar 

  17. Motamedi, E., Kavousi, K., Sadeghian Motahar, S. F., Reza Ghaffari, M., Sheykh Abdollahzadeh Mamaghani, A., Hosseini Salekdeh, G., & Ariaeenejad, S. (2021). Efficient removal of various textile dyes from wastewater by novel thermo-halotolerant laccase. Bioresource Technology, 337, 125468.

    Article  PubMed  CAS  Google Scholar 

  18. Zhou, J., Lian, J., & Rao, C. V. (2020). Metabolic engineering of Parageobacillus thermoglucosidasius for the efficient production of (2R, 3R)-butanediol. Applied Microbiology and Biotechnology, 104(10), 4303–4311.

    Article  PubMed  CAS  Google Scholar 

  19. Hussein, A. H., Lisowska, B. K., & Leak, D. J. (2015). The genus Geobacillus and their biotechnological potential. Advances in Applied Microbiology, 92, 1–48.

    Article  PubMed  CAS  Google Scholar 

  20. Aliyu, H., de Maayer, P., & Neumann, A. (2021). Not all that glitters is gold: The paradox of CO-dependent hydrogenogenesis in Parageobacillus thermoglucosidasius. Frontiers in Microbiology, 12, 784652.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Zhang, C., Wang, X., Zhang, W., Zhao, Y., & Lu, X. (2017). Expression and characterization of a glucose-tolerant beta-1,4-glucosidase with wide substrate specificity from Cytophaga hutchinsonii. Applied Microbiology and Biotechnology, 101(5), 1919–1926.

    Article  PubMed  CAS  Google Scholar 

  22. Wang, X., Zhao, D., Gao, L., Zhang, W., & Lu, X. (2020). Cage-like polyhedrons of DegQ from Cytophaga hutchinsonii show stable proteolytic activity and strong chaperone activity. Bio Eng J, 159, 107585.

    Article  CAS  Google Scholar 

  23. Si, J., Ma, H., Cao, Y., Cui, B., & Dai, Y. (2021). Introducing a thermo-alkali-stable, metallic ion-tolerant laccase purified from white rot fungus Trametes hirsuta. Frontiers in Microbiology, 12, 670163.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Navas, L. E., Martinez, F. D., Taverna, M. E., Fetherolf, M. M., Eltis, L. D., Nicolau, V., Estenoz, D., Campos, E., Benintende, G. B., & Berretta, M. F. (2019). A thermostable laccase from Thermus sp. 2.9 and its potential for delignification of Eucalyptus biomass. AMB Express, 9(1), 24.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Othman, A. M., Elsayed, M. A., Elshafei, A. M., & Hassan, M. M. (2018). Purification and biochemical characterization of two isolated laccase isoforms from Agaricus bisporus CU13 and their potency in dye decolorization. International Journal of Biological Macromolecules, 113, 1142–1148.

    Article  PubMed  CAS  Google Scholar 

  26. Kumar, M., Mishra, A., Singh, S. S., Srivastava, S., & Thakur, I. S. (2018). Expression and characterization of novel laccase gene from Pandoraea sp. ISTKB and its application. International Journal of Biological Macromolecules, 115, 308–316.

    Article  PubMed  CAS  Google Scholar 

  27. Wang, X., Wang, Z., Bai, X., Zhao, Y., Zhang, W., & Lu, X. (2018). Deletion of a gene encoding a putative peptidoglycan-associated lipoprotein prevents degradation of the crystalline region of cellulose in Cytophaga hutchinsonii. Frontiers in Microbiology, 9, 632.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Mehandia, S., Sharma, S. C., & Arya, S. K. (2020). Isolation and characterization of an alkali and thermostable laccase from a novel Alcaligenes faecalis and its application in decolorization of synthetic dyes. Biotechnology Reports (Amsterdam, Netherlands), 25, e00413.

    PubMed  Google Scholar 

  29. Mtibaa, R., de Eugenio, L., Ghariani, B., Louati, I., Belbahri, L., Nasri, M., & Mechichi, T. (2017). A halotolerant laccase from Chaetomium strain isolated from desert soil and its ability for dye decolourization. 3 Biotechnology, 7, 1–13.

    Google Scholar 

  30. Raseda, N., Hong, S., Kwon, O. Y., & Ryu, K. (2014). Kinetic evidence for the interactive inhibition of laccase from Trametes versicolor by pH and chloride. Journal of Microbiology and Biotechnology, 24(12), 1673–1678.

    Article  PubMed  CAS  Google Scholar 

  31. Damas, J. M., Baptista, A. M., & Soares, C. M. (2014). The pathway for O2 diffusion inside cota laccase and possible implications on the multicopper oxidases family. Journal of Chemical Theory and Computation, 10(8), 3525–3531.

    Article  PubMed  CAS  Google Scholar 

  32. Li, Z., Jiang, S., Xie, Y., Fang, Z., Xiao, Y., Fang, W., & Zhang, X. (2020). Mechanism of the salt activation of laccase Lac15. Biochemical and Biophysical Research Communications, 521(4), 997–1002.

    Article  PubMed  CAS  Google Scholar 

  33. Javadzadeh, S. G., & Asoodeh, A. (2020). A novel textile dye degrading extracellular laccase from symbiotic bacterium of Bacillus sp. CF96 isolated from gut termite (Anacanthotermes). International Journal of Biological Macromolecules, 145, 355–363.

    Article  PubMed  CAS  Google Scholar 

  34. Wang, S. N., Chen, Q. J., Zhu, M. J., Xue, F. Y., Li, W. C., Zhao, T. J., Li, G. D., & Zhang, G. Q. (2018). An extracellular yellow laccase from white rot fungus Trametes sp. F1635 and its mediator systems for dye decolorization. Biochimie, 148, 46–54.

    Article  PubMed  CAS  Google Scholar 

  35. Berini, F., Verce, M., Ausec, L., Rosini, E., Tonin, F., Pollegioni, L., & Mandic-Mulec, I. (2018). Isolation and characterization of a heterologously expressed bacterial laccase from the anaerobe Geobacter metallireducens. Applied Microbiology and Biotechnology, 102(5), 2425–2439.

    Article  PubMed  CAS  Google Scholar 

  36. Singh, G., & Arya, S. K. (2019). Utility of laccase in pulp and paper industry: A progressive step towards the green technology. International Journal of Biological Macromolecules, 134, 1070–1084.

    Article  PubMed  CAS  Google Scholar 

Download references

Funding

This study was funded by the Key Scientific Projects for colleges of Henan Province (Grant number 21A180004), the Henan Provincial Science and Technology Research Project (Grant number 222102320250), and the Doctoral Scientific Research Start-up Foundation from Henan University of Technology (Grant number 2018BS080).

Author information

Authors and Affiliations

  1. College of Biological Engineering, Henan University of Technology, Zhengzhou, 450001, China

    Xifeng Wang, Haifeng Li, Jianhang Qu & Zhi Liu

  2. School of Food and Strategic Reserves, Henan University of Technology, Zhengzhou, 450001, China

    Pengxiao Chen

Authors
  1. Xifeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pengxiao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haifeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianhang Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XW, PC, HL, and JQ conceived and designed research. XW, PC, and ZL conducted experiments. XW analyzed data. XW and PC wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Xifeng Wang.

Ethics declarations

Ethics Approval and Consent to Participate

This study does not contain any studies with human participants or animals performed by any of the authors. Informed consent was obtained from all individual participants included in the study.

Consent for Publication

The participant has consented to the submission of the case report to the journal.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 947 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Chen, P., Li, H. et al. Characterization of a Novel One-Domain Halotolerant Laccase from Parageobacillus thermoglucosidasius and Its Application in Dye Decolorization. Appl Biochem Biotechnol 195, 6465–6477 (2023). https://doi.org/10.1007/s12010-023-04389-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-023-04389-x

Keywords

Search

Navigation