Skip to main content

Advertisement

Log in

Chitinase from Streptomyces mutabilis as an Effective Eco-friendly Biocontrol Agent

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

Abstract

Blood sucking parasites not only cause economic loss but also transmit numerous diseases. Dermanyssus gallinae, an obligatory blood feeding ectoparasite causes huge production loss to the poultry industry. Mosquitoes act as vector for transmitting several viral and parasitic diseases in humans. Acaricide resistance limits the control of these parasites. The present study was aimed to control the parasites using chitinase that have selective degradation of chitin, an important component in exoskeleton development. Chitinase was induced in Streptomyces mutabilis IMA8 with chitin extracted from Charybdis smithii. The enzyme showed more than 50% activity at 30–50 °C and the optimum activity at 45 °C. The enzyme activity of chitinase was highest at pH 7.0. The kinetic parameters Km and Vmax values of chitinase were determined by non-linear regression using Michaelis–Menten equation and its derivative Hanes-Wolf plot. The larvicidal effect of different concentrations of chitinase was evaluated against all instar larvae (I–IV) and pupae of An. stephensi and Ae. aegypti after 24 h of exposure. The percentage of mortality was directly proportional to the chitinase concentration. Bioassay for miticidal activity showed that chitinase had excellent miticidal activity (LC50 = 24.2 ppm) against D. gallinae. The present study suggested the usage of Streptomyces mutabilis for preparation of chitinase in mosquito and mite control.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data Availability

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

References

  1. Harrington, D. W. J., George, D. R., Guy, J. H., & Sparagano, O. A. E. (2011). Opportunities for integrated pest management to control the poultry red mite, Dermanyssus gallinae. World’s Poultry Science Journal, 67, 83–94.

    Article  Google Scholar 

  2. Pritchard, J., Kuster, T., Sparagano, O., & Tomley, F. (2015). Understanding the biology and control of the poultry red mite Dermanyssus gallinae: A review. Avian Pathology, 44, 143–153.

    Article  PubMed  Google Scholar 

  3. Thomas, E., Zoller, H., Liebisch, G., et al. (2018). In vitro activity of fluralaner and commonly used acaricides against Dermanyssus gallinae isolates from Europe and Brazil. Parasites & Vectors, 11, 361.

    Article  Google Scholar 

  4. George, D. R., Finn, R. D., Graham, K. M., et al. (2015). Should the poultry red mite Dermanyssus gallinae be of wider concern for veterinary and medical science? Parasites & Vectors, 8, 178.

    Article  Google Scholar 

  5. Sigognault Flochlay, A., Thomas, E., & Sparagano, O. (2017). Poultry red mite (Dermanyssus gallinae) infestation: A broad impact parasitological disease that still remains a significant challenge for the egg-laying industry in Europe. Parasites & Vectors, 10, 357.

    Article  Google Scholar 

  6. Diniz, M. M., Henriques, A. D., Leandro Rda, S., Aguiar, D. L., & Beserra, E. B. (2014). Resistance of Aedes aegypti to temephos and adaptive disadvantages. Revista de Saude Publica, 48, 775–782.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Ranson, H., & Lissenden, N. (2016). Insecticide resistance in African Anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends in Parasitology, 32, 187–196.

    Article  CAS  PubMed  Google Scholar 

  8. Weill, M., Lutfalla, G., Mogensen, K., et al. (2003). Insecticide resistance in mosquito vectors. Nature, 423, 136–137.

    Article  CAS  PubMed  Google Scholar 

  9. Liu, N. (2015). Insecticide resistance in mosquitoes: Impact, mechanisms, and research directions. Annual Review of Entomology, 60, 537–559.

    Article  CAS  PubMed  Google Scholar 

  10. Naqqash, M. N., Gokce, A., Bakhsh, A., & Salim, M. (2016). Insecticide resistance and its molecular basis in urban insect pests. Parasitology Research, 115, 1363–1373.

    Article  PubMed  Google Scholar 

  11. Agency, E. M. (2018). Reflection paper on resistance in ectoparasites. Available from: https://www.ema.europa.eu/en/reflection-paper-resistance-ectoparasites-scientific-guideline. Accessed 15 Nov 2022

  12. Zdybel, J., Karamon, J., & Cencek, T. (2011). In vitro effectiveness of selected acaricides against red poultry mites (Dermanyssus gallinae, De Geer, 1778) isolated from laying hen battery cage farms localised in different regions of Poland. Bulletin of the Veterinary Institute in Pulawy, 55, 411–416.

    Google Scholar 

  13. Widiastuti, D., Ikawati, B., & Hadi, U. (2018). Larvicidal effect of mixture of Beauveria bassiana crude metabolite and chitinase enzyme against Aedes Aegypti larvae. Kesmas: National Public Health Journal, 12, 187–193.

    Google Scholar 

  14. Kumar, M., Brar, A., Vivekanand, V., & Pareek, N. (2018). Process optimization, purification and characterization of a novel acidic, thermostable chitinase from Humicola grisea. International Journal of Biological Macromolecules, 116, 931–938.

    Article  CAS  PubMed  Google Scholar 

  15. Shahidi, F., & Synowiecki, J. (1991). Isolation and characterization of nutrients and value-added products from snow crab (Chionoecetes opilio) and shrimp (Pandalus borealis) processing discards. Journal of Agriculture and Food Chemistry, 39, 1527–1532.

    Article  CAS  Google Scholar 

  16. Hsu, S. C., & Lockwood, J. L. (1975). Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Applied Microbiology, 29, 422–426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Krishnamoorthy, M., Dharmaraj, D., Rajendran, K., Karuppiah, K., Balasubramanian, M. & Ethiraj, K. (2020). Pharmacological activities of coral reef associated actinomycetes, Saccharopolyspora sp. IMA1. Biocatalysis and Agricultural Biotechnology, 28, 101748.

  18. Mukherjee, G., & Sen, S. K. (2006). Purification, characterization, and antifungal activity of chitinase from Streptomyces venezuelae P10. Current Microbiology, 53, 265–269.

    Article  CAS  PubMed  Google Scholar 

  19. Sambrook, J. & Russell, D. (2006). SDS-Polyacrylamide gel electrophoresis of proteins. CSH protocols, 2006(4).

  20. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  21. Sanjivkumar, M., Vijayalakshmi, K., Silambarasan, T., Sholkamy, E. N., & Immanuel, G. (2020). Biosynthesis, statistical optimization and molecular modeling of chitinase from crab shell wastes by a mangrove associated actinobacterium Streptomyces olivaceus (MSU3) using Box-Behnken design and its antifungal effects. Bioresource Technology Reports, 11, 100493.

    Article  Google Scholar 

  22. Xiayun, J., Chen, D., Shenle, H., Wang, W., Chen, S., & Zou, S. (2012). Identification, characterization and functional analysis of a GH-18 chitinase from Streptomyces roseolus. Carbohydrate Polymers, 87, 2409–2415.

    Article  Google Scholar 

  23. Murugan, K., Panneerselvam, C., Subramaniam, J., et al. (2016). Eco-friendly drugs from the marine environment: Spongeweed-synthesized silver nanoparticles are highly effective on Plasmodium falciparum and its vector Anopheles stephensi, with little non-target effects on predatory copepods. Environmental Science and Pollution Research International, 23, 16671–16685.

    Article  CAS  PubMed  Google Scholar 

  24. Wu, L., Huo, X., Zhou, X., et al. (2017). Acaricidal activity and synergistic effect of thyme oil constituents against carmine spider mite (Tetranychus cinnabarinus (Boisduval)). Molecules, 22(11), 1873.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Riseh, R. S., Hassanisaadi, M., Vatankhah, M., Babaki, S. A., & Barka, E. A. (2022). Chitosan as a potential natural compound to manage plant diseases. International Journal of Biological Macromolecules, 220, 998–1009.

    Article  CAS  PubMed  Google Scholar 

  26. Saberi Riseh, R., Tamanadar, E., Hajabdollahi, N., Vatankhah, M., Thakur, V. K., & Skorik, Y. A. (2022). Chitosan microencapsulation of rhizobacteria for biological control of plant pests and diseases: Recent advances and applications. Rhizosphere, 23, 100565.

    Article  Google Scholar 

  27. Saberi Riseh, R., Ebrahimi-Zarandi, M., Gholizadeh Vazvani, M., & Skorik, Y. A. (2021). Reducing drought stress in plants by encapsulating plant growth-promoting bacteria with polysaccharides. International Journal of Molecular Sciences, 22(23), 12979.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Saberi-Riseh, R., & Moradi-Pour, M. (2021). A novel encapsulation of Streptomyces fulvissimus Uts22 by spray drying and its biocontrol efficiency against Gaeumannomyces graminis, the causal agent of take-all disease in wheat. Pest Management Science, 77, 4357–4364.

    Article  CAS  PubMed  Google Scholar 

  29. Saberi Riseh, R., Moradi Pour, M., & Ait Barka, E. (2022). A Novel route for double-layered encapsulation of Streptomyces fulvissimus Uts22 by alginate-arabic gum for controlling of Pythium aphanidermatum in cucumber. Agronomy, 12(3), 655.

    Article  CAS  Google Scholar 

  30. Saberi Riseh, R., Skorik, Y. A., Thakur, V. K., Moradi Pour, M., Tamanadar, E., & Noghabi, S. S. (2021). Encapsulation of plant biocontrol bacteria with alginate as a main polymer material. International Journal of Molecular Sciences, 22, 11165.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lacombe-Harvey, M. E., Brzezinski, R., & Beaulieu, C. (2018). Chitinolytic functions in actinobacteria: Ecology, enzymes, and evolution. Applied Microbiology and Biotechnology, 102, 7219–7230.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Reynolds, D. M. (1954). Exocellular chitinase from a Streptomyces sp. Journal of General Microbiology, 11, 150–159.

    Article  CAS  PubMed  Google Scholar 

  33. Han, Y., Yang, B., Zhang, F., Miao, X., & Li, Z. (2009). Characterization of antifungal chitinase from marine Streptomyces sp. DA11 associated with South China Sea sponge Craniella australiensis. Marine Biotechnology (New York, N.Y.), 11, 132–140.

    Article  CAS  PubMed  Google Scholar 

  34. Rabeeth, M., Anitha, A., & Srikanth, G. (2011). Purification of an antifungal endochitinase from a potential biocontrol agent Streptomyces griseus. Pakistan Journal of Biological Sciences, 14, 788–797.

    Article  CAS  PubMed  Google Scholar 

  35. Pradeep, G. C., Yoo, H. Y., Cho, S. S., Choi, Y. H., & Yoo, J. C. (2015). An extracellular chitinase from Streptomyces sp. CS147 releases N-acetyl-D-glucosamine (GlcNAc) as principal product. Applied Biochemistry and Biotechnology, 175, 372–386.

    Article  Google Scholar 

  36. Cheba, B. A., Zaghloul, T. I., El-Massry, M. H., & El-Mahdy, A. R. (2017). Kinetics properties of marine chitinase from novel Red Sea strain of Bacillus. Procedia Eng, 181, 146–152.

    Article  CAS  Google Scholar 

  37. Emruzi, Z., Aminzadeh, S., Karkhane, A. A., Alikhajeh, J., Haghbeen, K., & Gholami, D. (2018). Improving the thermostability of Serratia marcescens B4A chitinase via G191V site-directed mutagenesis. International Journal of Biological Macromolecules, 116, 64–70.

    Article  CAS  PubMed  Google Scholar 

  38. Bucker, A., Bucker, N. C., Souza, A. Q., et al. (2013). Larvicidal effects of endophytic and basidiomycete fungus extracts on Aedes and Anopheles larvae (Diptera, Culicidae). Revista da Sociedade Brasileira de Medicina Tropical, 46, 411–419.

    Article  PubMed  Google Scholar 

  39. Louis, M. R. L. M., Rani, V. P., Krishnan, P., et al. (2022). Mosquito larvicidal activity of compounds from unripe fruit peel of avocado (Persea americana Mill.). Applied Biochemistry and Biotechnology, 195(4), 2636–2647.

  40. Mendonsa, E. S., Vartak, P. H., Rao, J. U., & Deshpande, M. V. (1996). An enzyme from Myrothecium verrucaria that degrades insect cuticles for biocontrol of Aedes aegypti mosquito. Biotechnology Letters, 18, 373–376.

    Article  CAS  Google Scholar 

  41. Sharma, A., Arya, S. K., Singh, J., et al. (2023). Prospects of chitinase in sustainable farming and modern biotechnology: An update on recent progress and challenges. Biotechnology and Genetic Engineering Reviews. https://doi.org/10.1080/02648725.2023.2183593

  42. Tabari, M. A., Jafari, A., Jafari, M., & Youssefi, M. R. (2023). Laboratory and field efficacy of terpene combinations (carvacrol, thymol and menthol) against the poultry red mite (Dermanyssus gallinae). Veterinary Parasitology, 313, 109842.

    Article  CAS  PubMed  Google Scholar 

  43. Dehghani-Samani, A., Madreseh-Ghahfarokhi, S., Dehghani-Samani, A., & Pirali-Kheirabadi, K. (2015). Acaricidal and repellent activities of essential oil of Eucalyptus globulus against Dermanyssus gallinae (Acari: Mesostigmata). Journal of Herbmedicine Pharmacology, 4, 81–84.

    CAS  Google Scholar 

  44. George, D. R., Sparagano, O. A., Port, G., Okello, E., Shiel, R. S., & Guy, J. H. (2010). Environmental interactions with the toxicity of plant essential oils to the poultry red mite Dermanyssus gallinae. Medical and Veterinary Entomology, 24, 1–8.

    Article  CAS  PubMed  Google Scholar 

  45. George, D. R., Smith, T. J., Shiel, R. S., Sparagano, O. A., & Guy, J. H. (2009). Mode of action and variability in efficacy of plant essential oils showing toxicity against the poultry red mite, Dermanyssus gallinae. Veterinary Parasitology, 161, 276–282.

    Article  CAS  PubMed  Google Scholar 

  46. Locher, N., Al-Rasheid, K. A., Abdel-Ghaffar, F., & Mehlhorn, H. (2010). In vitro and field studies on the contact and fumigant toxicity of a neem-product (Mite-Stop) against the developmental stages of the poultry red mite Dermanyssus gallinae. Parasitology Research, 107, 417–423.

    Article  PubMed  Google Scholar 

  47. Bartley, K., Wright, H. W., Huntley, J. F., et al. (2015). Identification and evaluation of vaccine candidate antigens from the poultry red mite (Dermanyssus gallinae). International Journal for Parasitology, 45, 819–830.

    Article  CAS  PubMed  Google Scholar 

  48. Harrington, D., Canales, M., de la Fuente, J., et al. (2009). Immunisation with recombinant proteins subolesin and Bm86 for the control of Dermanyssus gallinae in poultry. Vaccine, 27, 4056–4063.

    Article  CAS  PubMed  Google Scholar 

  49. Lima-Barbero, J. F., Contreras, M., Mateos-Hernández, L., et al. (2019). A Vaccinology approach to the identification and characterization of Dermanyssus gallinae candidate protective antigens for the control of poultry red mite infestations. Vaccines, 7, 190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Mul, M., Van Niekerk, T., Chirico, J., et al. (2009). Control methods for Dermanyssus gallinae in systems for laying hens: Results of an international seminar. World’s Poultry Science Journal, 65, 589–600.

    Article  Google Scholar 

  51. Park, S. E., Lee, M. R., Lee, S. J., et al. (2022). Strategic positioning of Beauveria bassiana sensu lato JEF-410 in management of poultry red mite, Dermanyssus gallinae (Mesostigmata: Dermanyssidae). BioControl, 67, 39–48.

    Article  CAS  Google Scholar 

  52. Park, S. E., Kim, J.-C., Im, Y., & Kim, J. S. (2023). Pathogenesis and defense mechanism while Beauveria bassiana JEF-410 infects poultry red mite, Dermanyssus gallinae. PLOS One, 18, e0280410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sobotnik, J., Kudlikova-Krizkova, I., Vancova, M., Munzbergova, Z., & Hubert, J. (2008). Chitin in the peritrophic membrane of Acarus siro (Acari: Acaridae) as a target for novel acaricides. Journal of Economic Entomology, 101, 1028–1033.

    Article  CAS  PubMed  Google Scholar 

  54. Subbanna, A. R. N. S., Stanley, J., Rajasekhara, H., Mishra, K. K., Pattanayak, A. & Bhowmick, R. (2019). Perspectives of microbial metabolites as pesticides in agricultural pest management. In J.- M. Merillon, & K. G. Ramawat (Eds.), Co-evolution of secondary metabolites (pp. 1–28). Cham: Springer International Publishing.

Download references

Acknowledgements

Authors are thankful to the authorities of Alagappa University, Karaikudi, for awarding Post-Doctoral Fellowship and the Head, Department of Animal Health and Management, Alagappa University, Karaikudi, for his encouragement and support. Authors thank Dr. P. Kumar, Assistant professor, Department of Animal Health and Management, Alagappa University, Karaikudi for FTIR analysis.

Funding

This research has been sponsored under RUSA 2.0 PDF by Alagappa University. The authors acknowledge RUSA Scheme Phase 2.0 grant [F-24–51/2014–U, Policy (TNMulti-Gen), Department of Education, Govt. of India. Dt. 09.10.2018].

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. KR: conceptualization, methodology, resources, investigation, software, data curation, formal analysis, writing—original draft; MK: methodology; KK: reviewing; KE: supervision, administration; SS: assisting. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Kumar Rajendran or Kannapiran Ethiraj.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable

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 (DOC 46 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

Rajendran, K., Krishnamoorthy, M., Karuppiah, K. et al. Chitinase from Streptomyces mutabilis as an Effective Eco-friendly Biocontrol Agent. Appl Biochem Biotechnol 196, 18–31 (2024). https://doi.org/10.1007/s12010-023-04489-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-023-04489-8

Keywords

Navigation