Skip to main content

Advertisement

Log in

Potential Bioactive Compounds from Marine Streptomyces sp. and Their In Vitro Antibiofilm and Antibacterial Activities Against Antimicrobial-Resistant Clinical Pathogens

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

Abstract

Antimicrobial resistance issues have risen dramatically in recent years, posing a severe concern to humans worldwide. The urgent need to find novel compounds for pharmaceutical applications prompts the research of under-explored environments such as marine ecosystems. The present study was designed to discover novel secondary metabolites, and we have isolated about 30 actinomycetes from the marine soil samples collected in Thondi (Ramanathapuram, Tamil Nadu, India), where most isolates are associated with the genus Streptomyces. Out of 30, one potentially active strain (Streptomyces sp. SRMA3) was identified using primary and secondary screening methods against the drug-resistant clinical pathogens. The active metabolites extracted from the selected active isolate were subjected to partial purification and characterization using Fourier transform infrared spectrophotometer (FTIR) and gas chromatography-mass spectroscopy (GC-MS) analysis. The minimum inhibitory concentration (MIC) value was determined for the active metabolite. Further, the partially purified active fraction was revealed for its antibacterial and antibiofilm activity against drug-resistant clinical pathogens. Light and fluorescence microscopy detected the viability and adhesion of the biofilm-forming drug-resistant pathogens. Growth curve analysis showed that the active metabolite has the potential to inhibit drug-resistant pathogens. The synergistic effect of active metabolite with commercial antibiotics also revealed that it could enhance the activity of antibiotics in antimicrobial resistance pathogens. This study shows that the isolated Streptomyces sp. SRMA3 is a potentially active strain, and the metabolite derived from this strain has a good antibacterial and antibiofilm activity against antimicrobially resistant clinical pathogens and could be used for various biotechnological applications.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

All the data are available within the manuscript and its supporting information.

References

  1. Goodfellow, M., & Williams, S. (1983). Ecology of actinomycetes. Annual Review of Microbiology, 37, 189–216.

    Article  CAS  PubMed  Google Scholar 

  2. Catalano, A., Iacopetta, D., Ceramella, J., Scumaci, D., Giuzio, F., Saturnino, C., Aquaro, S., Rosano, C., & Sinicropi, M. S. (2022). Multidrug resistance (MDR): A widespread phenomenon in pharmacological therapies. Molecules, 27, 616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Alqahtani, S. S., Moni, S. S., Sultan, M. H., Bakkari, M. A., Madkhali, O. A., Alshahrani, S., Makeen, H. A., Menachery, S. J., ur Rehman, Z., Alam, M. S. (2022) Potential bioactive secondary metabolites of Actinomycetes sp. isolated from rocky soils of the heritage village Rijal Alma, Saudi Arabia. Arabian Journal of Chemistry, 15, 103793.

  4. Zhu, Y., Huang, W. E., & Yang, Q. (2022). Clinical perspective of antimicrobial resistance in bacteria. Infection and Drug Resistance, 15, 735–746.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rafailidis, P. I., & Kofteridis, D. (2022). Proposed amendments regarding the definitions of multidrug-resistant and extensively drug-resistant bacteria. Expert Review of Anti-Infective Therapy, 20, 139–146.

    Article  CAS  PubMed  Google Scholar 

  6. Khajure, P. V., & Rathod, J. (2011). Antimicrobial and cytotoxic potential of the compound secreted by marine bacteria collected from the Karwar Coast, West Coast of India. Indonesian Journal of Biotechnology, 16, 60–65.

    Google Scholar 

  7. Mothana, A. A., Al-Shamahy, H. A., Mothana, R. A., Khaled, J. M., Al-Rehaily, A. J., Al-Mahdi, A. Y., & Lindequist, U. (2022). Streptomyces sp. 1S1 isolated from Southern coast of the Red Sea as a renewable natural resource of several bioactive compounds. Saudi Pharmaceutical Journal, 30, 162–171.

    Article  CAS  PubMed  Google Scholar 

  8. Ghosh, S., Sarkar, T., Pati, S., Kari, Z. A., Edinur, H. A., & Chakraborty, R. (2022). Novel bioactive compounds from marine sources as a tool for functional food development. Frontiers in Marine Science, 9(10), 3389.

    Google Scholar 

  9. Singh, V., & Tripathi, C. (2011). Olivanic acid production in fed batch cultivation by Streptomyces olivaceus MTCC 6820. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 2, 726–731.

    CAS  Google Scholar 

  10. Praveen, V., Tripathi, D., Tripathi, C. K., & Bihari, V. (2008). Nutritional regulation of actinomycin-D production by a new isolate of Streptomyces sindenensis using statistical methods. Indian Journal of Experimental Biology46, 138–144.

  11. Ossai, J., Khatabi, B., Nybo, S. E., & Kharel, M. K. (2022). Renewed interests in the discovery of bioactive actinomycete metabolites driven by emerging technologies. Journal of Applied Microbiology, 132, 59–77.

    Article  PubMed  Google Scholar 

  12. Singh, V., Haque, S., Singh, H., Verma, J., Vibha, K., Singh, R., Jawed, A., & Tripathi, C. (2016). Isolation, screening, and identification of novel isolates of actinomycetes from India for antimicrobial applications. Frontiers in Microbiology, 7, 1921.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bugni, T. S., & Ireland, C. M. (2004). Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Natural Product Reports, 21, 143–163.

    Article  CAS  PubMed  Google Scholar 

  14. Hifnawy, M. S., Hassan, H. M., Mohammed, R. M., Fouda, M., Sayed, A. M., Hamed, A. A., Abou Zid, F. S., Rateb, M. E., Alhadrami, H. A., & Abdelmohsen, U. R. (2020). Induction of antibacterial metabolites by co-cultivation of two red-sea-sponge-associated Actinomycetes Micromonospora sp. UR56 and Actinokinespora sp. EG49. Marine Drugs, 18, 243.

    Article  CAS  Google Scholar 

  15. Selim, M. S. M., Abdelhamid, S. A., & Mohamed, S. S. (2021). Secondary metabolites and biodiversity of actinomycetes. Journal, Genetic Engineering & Biotechnology, 19, 1–13.

    Article  Google Scholar 

  16. Dewi, T. K., Agustiani, D., & Antonius, S. (2017). Secondary metabolites production by Actinomycetes and their antifungal activity. KnE Life Sciences, 256–264.

  17. Dror, B., Jurkevitch, E., & Cytryn, E. (2020). State-of-the-art methodologies to identify antimicrobial secondary metabolites in soil bacterial communities—A review. Soil Biology and Biochemistry, 147, 107838.

    Article  CAS  Google Scholar 

  18. Ōmura, S., Ikeda, H., Ishikawa, J., Hanamoto, A., Takahashi, C., Shinose, M., Takahashi, Y., Horikawa, H., Nakazawa, H., & Osonoe, T. (2001). Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proceedings of the National Academy of Sciences, 98, 12215–12220.

    Article  Google Scholar 

  19. Khan, S. T., Komaki, H., Motohashi, K., Kozone, I., Mukai, A., Takagi, M., & Shin-ya, K. (2011). Streptomyces associated with a marine sponge Haliclona sp.: Biosynthetic genes for secondary metabolites and products. Environmental Microbiology, 13, 391–403.

    Article  CAS  PubMed  Google Scholar 

  20. Hutchings, M. I., Truman, A. W., & Wilkinson, B. (2019). Antibiotics: Past, present and future. Current Opinion in Microbiology, 51, 72–80.

    Article  CAS  PubMed  Google Scholar 

  21. Hu, Y., Chen, J., Hu, G., Yu, J., Zhu, X., Lin, Y., Chen, S., & Yuan, J. (2015). Statistical research on the bioactivity of new marine natural products discovered during the 28 years from 1985 to 2012. Marine Drugs, 13, 202–221.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ahsan, T., Chen, J., Zhao, X., Irfan, M., & Wu, Y. (2017). Extraction and identification of bioactive compounds (eicosane and dibutyl phthalate) produced by Streptomyces strain KX852460 for the biological control of Rhizoctonia solani AG-3 strain KX852461 to control target spot disease in tobacco leaf. AMB Express, 7, 1–9.

    Article  CAS  Google Scholar 

  23. Ghosh, S., Lahiri, D., Nag, M., Dey, A., Sarkar, T., Biswas, R., ... & Ray, R. R. (2022). Analysis of antibiofilm activities of bioactive compounds from Honeyweed (Leonurus sibiricus) against P. aeruginosa: An in vitro and in silico approach. Applied Biochemistry and Biotechnology, 1–17

  24. Oja, T., San Martin Galindo, P., Taguchi, T., Manner, S., Vuorela, P. M., Ichinose, K., Metsä-Ketelä, M., & Fallarero, A. (2015). Effective antibiofilm polyketides against Staphylococcus aureus from the pyranonaphthoquinone biosynthetic pathways of Streptomyces species. Antimicrobial Agents and Chemotherapy, 59, 6046–6052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Suzuki, N., Ohtaguro, N., Yoshida, Y., Hirai, M., Matsuo, H., Yamada, Y., Imamura, N., & Tsuchiya, T. (2015). A compound inhibits biofilm formation of Staphylococcus aureus from Streptomyces. Biological and Pharmaceutical Bulletin, 38, 889–892.

    Article  CAS  PubMed  Google Scholar 

  26. Lahiri, D., Nag, M., Sarkar, T., Dutta, B., & Ray, R. R. (2021). Antibiofilm activity of α-amylase from Bacillus subtilis and prediction of the optimized conditions for biofilm removal by response surface methodology (RSM) and artificial neural network (ANN). Applied Biochemistry and Biotechnology, 193, 1853–1872.

    Article  CAS  PubMed  Google Scholar 

  27. Parsek, M. R., & Greenberg, E. P. (2000). Acyl-homoserine lactone quorum sensing in gram-negative bacteria: A signaling mechanism involved in associations with higher organisms. Proceedings of the National Academy of Sciences, 97, 8789–8793.

    Article  CAS  Google Scholar 

  28. Madigan, M. T., Martinko, J. M., & Parker, J. (2006). Brock biology of microorganisms. Pearson Prentice Hall.

    Google Scholar 

  29. Wu, R.-Y. (1984). Studies on the Streptomyces SC4. II Taxonomic and biological characteristics of Streptomyces strain SC4. Botanical Bulletin of Academia Sinica, 25, 111–123.

    CAS  Google Scholar 

  30. Islam, A., & Hernández, F. L. (1966). Methods for characterization of Streptomyces species. METHODS, 16, 313–340.

    Google Scholar 

  31. Parte, A., Whitman, W. B., Goodfellow, M., Kämpfer, P., Busse, H.-J., Trujillo, M. E., Ludwig, W., & Suzuki, K.-I. (2012). Bergey’s manual of systematic bacteriology (5th ed.). The Actinobacteria, Springer Science & Business Media.

    Google Scholar 

  32. Holt, J. G., Krieg, N. R., Sneath, P. H. (1994) Bergey’s manual of determinative bacterology.

  33. Sarkar, T., Bharadwaj, K. K., Salauddin, M., Pati, S., & Chakraborty, R. (2022). Phytochemical characterization, antioxidant, anti-inflammatory, anti-diabetic properties, molecular docking, pharmacokinetic profiling, and network pharmacology analysis of the major phytoconstituents of raw and differently dried mangifera indica (himsagar cultivar): An in vitro and in silico investigations. Applied Biochemistry and Biotechnology, 194, 950–987.

    Article  CAS  PubMed  Google Scholar 

  34. Pati, S., Chatterji, A., Dash, B. P., Raveen Nelson, B., Sarkar, T., Shahimi, S., Atan Edinur, H., Manan, B. A., & T. S., Jena, P., Mohanta, Y. K. (2020). Structural characterization and antioxidant potential of chitosan by γ-irradiation from the carapace of horseshoe crab. Polymers, 12, 2361.

    Article  CAS  PubMed Central  Google Scholar 

  35. Rahuman, H. B. H., Dhandapani, R., Palanivel, V., Thangavelu, S., Paramasivam, R., & Muthupandian, S. (2021). Bioengineered phytomolecules-capped silver nanoparticles using Carissa carandas leaf extract to embed on to urinary catheter to combat UTI pathogens. PLoS One, 16, e0256748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Agarwala, M., Barman, T., Gogoi, D., Choudhury, B., Pal, A. R., & Yadav, R. (2014). Highly effective antibiofilm coating of silver–polymer nanocomposite on polymeric medical devices deposited by one step plasma process. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 102, 1223–1235.

    Article  CAS  Google Scholar 

  37. Rab, E., Kekos, D., Roussis, V., & Ioannou, E. (2017). α-pyrone polyketides from Streptomyces ambofaciens BI0048, an endophytic actinobacterial strain isolated from the red alga Laurencia glandulifera. Marine Drugs, 15, 389.

    Article  PubMed Central  CAS  Google Scholar 

  38. Singh, V., Haque, S., Khare, S., Tiwari, A. K., Katiyar, D., Banerjee, B., Kumari, K., & Tripathi, C. (2018). Isolation and purification of antibacterial compound from Streptomyces levis collected from soil sample of north India. PLoS One, 13, e0200500.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Daigham, G. E., & Mahfouz, A. Y. (2020). Isolation, characterization, and screening of actinomycetes producing bioactive compounds from Egyptian soil. Egyptian Pharmaceutical Journal, 19, 381.

    Article  Google Scholar 

  40. Benhadj, M., Gacemi-Kirane, D., Menasria, T., Guebla, K., & Ahmane, Z. (2019). Screening of rare actinomycetes isolated from natural wetland ecosystem (Fetzara Lake, northeastern Algeria) for hydrolytic enzymes and antimicrobial activities. Journal of King Saud University-Science, 31, 706–712.

    Article  Google Scholar 

  41. Balachandar, R., Karmegam, N., Saravanan, M., Subbaiya, R., & Gurumoorthy, P. (2018). Synthesis of bioactive compounds from vermicast isolated actinomycetes species and its antimicrobial activity against human pathogenic bacteria. Microbial Pathogenesis, 121, 155–165.

    Article  CAS  PubMed  Google Scholar 

  42. Ganesan, P., Reegan, A. D., David, R. H. A., Gandhi, M. R., Paulraj, M. G., Al-Dhabi, N. A., & Ignacimuthu, S. (2017). Antimicrobial activity of some actinomycetes from Western Ghats of Tamil Nadu, India. Alexandria Journal of Medicine, 53, 101–110.

    Article  Google Scholar 

  43. Toté, K., Berghe, D. V., Deschacht, M., De Wit, K., Maes, L., & Cos, P. (2009). Inhibitory efficacy of various antibiotics on matrix and viable mass of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. International Journal of Antimicrobial Agents, 33, 525–531.

    Article  PubMed  CAS  Google Scholar 

  44. Çetinkaya, S., Yenidünya, A. F., Arslan, K., Arslan, D., Doğan, Ö., & Daştan, T. (2020). Secondary metabolites of an of Streptomyces griseorubens isolate are predominantly pyrrole-and linoleic-acid like compounds. Journal of Oleo Science, 69, 1273–1280.

    Article  PubMed  CAS  Google Scholar 

  45. Ogundare, A., Ekundayo, F., & Banji-Onisile, F. (2015). Antimicrobial activities of Streptomyces species isolated from various soil samples in Federal University of Technology, Akure environment. IOSR-JPBS, 4, 22–30.

    Google Scholar 

  46. Abirami, M., Gopal, J., & Kannabiran, K. (2015). Extraction and identification of antibacterial compound from marine Streptomyces sp. VITAK1 isolated from the coast of Andaman and Nicobar Islands,India. Applied Biochemistry and Microbiology, 51, 406–410.

    Article  CAS  Google Scholar 

  47. Agoramoorthy, G., Chandrasekaran, M., Venkatesalu, V., & Hsu, M. (2007). Antibacterial and antifungal activities of fatty acid methyl esters of the blind-your-eye mangrove from India. Brazilian Journal of Microbiology, 38, 739–742.

    Article  Google Scholar 

  48. Al-Juhaimi, F. Y., Özcan, M. M., Mohamed Ahmed, I. A., Alsawmahia, O. N., Özcan, M. M., Ghafoor, K., & Babiker, E. E. (2022). Bioactive compounds, antioxidant activity, fatty acid composition, and antimicrobial activity of propolis from different locations in Turkey. Journal of Apicultural Research, 61, 246–254.

    Article  Google Scholar 

  49. Davidson, W. S., Saxena, R., & Gupta, R. (1999). The fungistatic action of oleic acid. Current Science, 1137–1140.

  50. Sandoval-Montemayor, N. E., García, A., Elizondo-Treviño, E., Garza-González, E., Alvarez, L., & del Rayo Camacho-Corona, M. (2012). Chemical composition of hexane extract of Citrus aurantifolia and anti-Mycobacterium tuberculosis activity of some of its constituents. Molecules, 17, 11173–11184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Medical Microbiology Laboratory Unit at Department of Microbiology, Alagappa University, for providing research facilities to carry out this research work.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, writing original draft, writing review and editing, methodology, project administration, software, visualization, data curation, resources: Ranjithkumar Dhandapani; validation: Ragul Paramasivam, Palanivel Velmurugan; formal analysis: Latha Ragunathan; supervision: Sathiamoorthi Thangavelu, and Saravanan Muthupandian

Corresponding authors

Correspondence to Sathiamoorthi Thangavelu or Saravanan Muthupandian.

Ethics declarations

Ethical Approval

Not applicable

Consent to Participate

Not applicable

Consent for Publication

Not applicable

Competing Interest

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

ESM 1

(DOCX 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dhandapani, R., Thangavelu, S., Ragunathan, L. et al. Potential Bioactive Compounds from Marine Streptomyces sp. and Their In Vitro Antibiofilm and Antibacterial Activities Against Antimicrobial-Resistant Clinical Pathogens. Appl Biochem Biotechnol 194, 4702–4723 (2022). https://doi.org/10.1007/s12010-022-04072-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04072-7

Keywords

Navigation