Identification of Antibiotic Compounds from Thai Mangrove Soil-derived Streptomyces iconiensis

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Konthorn Kachanuban
Pengcheng Yan
Peng Fu
Weiming Zhu
Pongtep Wilaipun

Abstract

The recent lack of discovery of novel antibiotics and the increase of antibiotic-resistant microorganisms present significant problems in infectious disease therapy. The mangrove forest ecosystem is an important natural source of novel organisms that have high potential to produce bioactive compounds. This study focuses on screening and identification of antimicrobial compound-producing actinobacteria from mangrove sediment samples, determination of some optimal parameters for antimicrobial compound production, as well as characterization of the antimicrobial compounds produced. Among a total of 22 isolates isolated from seven sediment samples, Streptomyces iconiensis OUCMDZ-5511, which was identified by colony morphology and 16S rRNA gene sequence, displayed the broadest antimicrobial spectrum against eight target indicator bacteria. An ethyl acetate (EtOAc) extract from culture broth of S. iconiensis OUCMDZ-5511 had the highest antibacterial activity against Bacillus subtilis ATCC 6051, determined by agar well diffusion method, when this strain was cultured in A1 broth with initial pH of 9.0 and 0% NaCl. According to bioassay-guided chromatography, three interesting antimicrobial compounds, namely 2(3H)-benzothiazolone, indole-3-acetic acid and lumichrome were obtained from culture broth EtOAc extract of S. iconiensis OUCMDZ-5511 after purification by HPLC and structure identification by ESI-MS and NMR. However, only lumichrome showed broad-spectrum antibacterial activity against Salmonella Weltevreden, Staphylococcus aureus, B. subtilis, Micrococcus luteus and Escherichia coli, with MIC and MBC values ranging from 0.125 to 0.5 mg·mL-1 and 0.25 to 1.0 mg·mL-1, respectively. Notably, this study is the pioneer report on identification of 2(3H)-benzothiazolone, indole-3-acetic acid, and lumichrome in EtOAc extract from culture broth of S. iconiensis.

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Abidin, Z.A.Z., N.A. Malek, Z. Zainuddin and A.J.K. Chowdhury. 2015. Selective isolation and antagonistic activity of actinomycetes from mangrove forest of Pahang, Malaysia. Frontiers in Life Science 9(1): 24-31.

Abd-Alla, M.H., E.S.A. El-Sayed and A.H.M. Rasmey. 2013. Indole-3-acetic acid (IAA) production by Streptomyces atrovirens isolated from rhizospheric soil in Egypt. Journal of Biology and Earth Sciences 3(2): 182-193.

Abozenadah, H., A. Bishop, S. Bittner, O. Lopez, C. Wiley and P.M. Flatt. 2017. Chapter 6 A brief history of natural products and organic chemistry [M]. In Consumer chemistry: how organic chemistry impacts our lives. CC BY-NC-SA. https://wou.edu/chemistry/courses/online-chemistry-textbooks/ch105-consumer-chemistry/. Cited 18 Jan 2022.

Ahmad, S.M., A.O. El-Gendy, R.R. Ahned, H.M. Hassan, H.M. El-Kabbany and A.G. Merdash. 2017. Exploring the antimicrobial and antitumor potentials of Streptomyces sp. AGM12-1 isolated from Egyptian soil. Frontiers in Microbiology 8(438): 1-11.

Akond, M.A., M.N. Jahan, N. Sultana and F. Rahman. 2016. Effect of temperature, pH and NaCl on the isolates of actinomycetes from straw and compost samples from Savar, Dhaka, Bangladesh. American Journal of Microbiology and Immunology 1(2): 10-15.

Beomkoo, C., O.H. Kwon, J. Shin and K.B. Oh. 2019. Inhibitory effects of Streptomyces sp. MBTH32 metabolites on Sortase A and Sortase A-mediated cell clumping of Staphylococcus aureus to fibrinogen. Microbiology and Biotechnology 29(10): 1603-1606.

Biswas, K., D. Bhattarcharya, M. Saha, J. Mukherjee and S. Karmakar. 2022. Evaluation of antimicrobial activity of the extract of Streptomyces euryhalinus isolated from the Indian Sundarbans. Archives of Microbiology 34(2022): 1-9.

Brock, T.D. 1961. Chloramphenicol. Bacteriological Review 25: 32-48.

Chanthasena, P. and N. Nantapong. 2016. Biodiversity of antimicrobial-producing actinomycetes strains isolated from dry dipterocarp forest soil in northeast Thailand. Biological and Applied Sciences 59: e16150674. DOI:10.1590/1678-4324-2016150674.

Chen, Y., W. Mao, Y. Gao, X. Teng, W. Zhu, Y. Chen, C. Zhao, N. Li, C. Wang, M. Yan, J. Shan, C. Lin and T. Guo. 2013. Structural elucidation of an extracellular polysaccharide produced by the marine fungus Aspergillus versicolor. Carbohydrate Polymers 93(2): 478-483.

Cho, Y., G.I. Jang, C.Y. Hwang, E.H. Kim and B.C. Cho. 2013. Nocardioides salsibiostraticola sp. nov., isolated from biofilm formed in coastal seawater. International Journal of Systematic and Evolutionary Microbiology 63(10): 3800-3806.

Das, B. and S. Patra. 2017. Antimicrobials: Meeting the challenges of antibiotic resistance through nanotechnology. In: Nanostructures for Antimicrobial Therapy. (eds. F. Anton and M.G. Alexandru), pp. 1-22. Elsevier, Bucharest, Romania.

Debbab, A., A.H. Aly, W.H. Lin and P. Proksch. 2010. Bioactive compounds from marine bacteria and fungi. Microbial Biotechnology 3(5): 544-563.

Demet, T., K. Guven, C. Sproer, H.P. Klenk and N. Sahin. 2014. Streptomyces iconiensis sp.Nov. and Streptomyces smyrnaeus sp. Nov., two halotolerant actinomycetes isolated from a salt lake and saltern. International Journal of Systematic and Evolutionary Microbiology 64(9): 3126-3133.

Ding, Z.G., J.Y. Zhao, P.W. Yang, M.G. Li, R. Huang, X.L. Cui and M.L. Wen. 2009. 1H and 13C NMR assignment of eight nitrogen containing compounds from Nocardia alba sp.nov (YIM 30243T). Magnetic Resonance in Chemistry 47(4): 366-370.

Fu, P. and J.B. MacMillan. 2015. Thiasporines A-C, thiazine and thiazole derivatives from a marine-derived Actinomycetospora chloral. Journal of Natural Products 78(3): 1-4.

Grasso, L.L., D.C. Martino and R. Alduina. 2016. Actinobacteria - basics and biotechnological applications. In: Production of antibacterial compounds from actinomycetes (ed. D. Dhanasekaran, and Y. Jiang), pp. 177-198. IntechOpen, London, UK.

Groenhagen, U., M. Maczka, J.S. Dickschat and S. Schulz. 2014. Streptopyridines, volatile pyridine alkaloids produced by Streptomyces sp. FORM5. Beilstein Journal of Organic Chemistry 10: 1421-1432.

Higgens, C.E. and R.E. Kastner. 1971. Streptomyces clavuligerus sp. nov., a β-lactam antibiotic producer. International Journal of Systematic and Evolutionary Microbiology 21(4): 326-331.

Hozzein, W.N. and M. Goodfellow. 2007. Nonomuraea aegyptia sp. nov., a novel actinomycete isolated from a sand dune. Antonie van Leeuwenhoek 92(2): 165-171.

Hudzicki, J. 2009. Kirby-bauer disk diffusion susceptibility test protocol. https://www.asm.org/getattachment/2594ce26-bd44-47f6-8287-0657aa9185ad/Kirby-Bauer-Disk-Diffusion-Susceptibility-Test-Protocol-pdf.pdf. Cited 16 Oct 2021.

Itoh, T. and T. Mase. 2007. A novel practical synthesis of benzothiazoles via Pd-catalyzed thiol cross-coupling. Organic Letters 9(18): 3687-3689.

Jamkhandi, C.M. and J.I. Disouza. 2012. Asian Journal of Biochemical and Pharmaceutical Research 3(2): 123-130.

Jiang, Y., Q. Li, X. Chen and C. Jiang. 2016. Actinobacteria-basic and biotechnological application: Isolation and cultivation methods of actinobacteria. IntechOpen, London, UK. 398 pp.

Joachim, J.H., C.D. Bader, M. Remškar, K. Cirnski and R. Müller. 2018. Concepts and methods to access novel antibiotics from actinomycetes. Antibiotics 7(2): 44. DOI:10.3390/antibiotics7020044.

Kariminik, A. and F. Baniasadi. 2010. Pageantagonistic activity of actinomycetes on some gram negative and gram positive bacteria. World Applied Sciences Journal 8(7): 828-832.

Kumar, A. and R. Naraian. 2019. Producers of bioactive compounds. In: New and Future Developments in Microbial Biotechnology and Bioengineering (eds. B.P. Singh, V.K. Gupta and A.K. Passari), pp. 205-221. Elsevier, Amsterdam, Netherlands.

Lam, K.S. 2006. Discovery of novel metabolites from marine actinomycetes. Current Opinion in Microbiology 9(3): 245-251.

Lee, L.H., N. Zainal, A.S. Azman, S.K. Eng, B.H. Goh, W.F. Yin, N.S.A. Mutalib and K.G. Chan. 2014. Diversity and antimicrobial activities of actinobacteria isolated from tropical mangrove sediments in Malaysia. The Scientific World Journal 2014: 698178. DOI:10.1155/2014/698178.

Li, Y., M. Wang, Z.Z. Sun and B.B. Xie. 2021. Comparative genomic insights into the taxonomic classification, diversity, and secondary metabolic potentials of Kitasatospora, a genus closely related to Streptomyces. Frontiers in Microbiology 12: 1-13.

Madden, T. 2003. The NCBI Handbook [Internet]. In: The BLAST Sequence Analysis Tool. (eds. J. McEntyre and J. Ostell), pp. 229-240. National Center for Biotechnology Information (US), Bethesda, USA.

Manteca, Á. and P. Yagüe, 2019. Streptomyces as a source of antimicrobials: novel approaches to activate cryptic secondary metabolite pathways. https://www.intechopen.com/chapters/64272. Cited 19 Aug 2022.

Meanwell, R.J.L. and G. Shama. 2008. Production of streptomycin from chitin using Streptomyces griseus in bioreactors of different configuration. Bioresource Technology 99(13): 5634-5639.

Muzyed, S., M.M. Howlader and R. Tuvikene. 2021. Fermentation optimization, purification and biochemical characterization of ι-carrageenase from marine bacterium Cellulophaga baltica. International Journal of Biological Macromolecules 166(1): 789-797.

Ng, Y.K., M.P. Hodson, A.K. Hewavitharana, U. Bose, P.N. Shaw and J.A. Fuerst. 2014. Effects of salinity on antibiotic production in sponge-derived Salinispora actinobacteria. Journal of Applied Microbiology 117(1): 109-25.

Pang, H., X. Xin, J. He, B. Cui, D. Guo, S. Liu, Z. Yan, C. Liu, X. Wang and J. Nan. 2020. Effect of NaCl concentration on microbiological properties in NaCl assistant anaerobic fermentation: hydrolase activity and microbial community distribution. Frontiers in Microbiology 11(1): 589222. DOI:10.3389/fmicb.2020.589222.

Petroski, M.D. and R.J. Deshaies. 2005. Function and regulation of cullin-RING ubiquitin ligases. Plant Cell 6(1): 9-20.

Pettit, R.K. 2011. Small-molecule elicitation of microbial secondary metabolites. Microbial Biotechnology 4(4): 471-478.

Phongsopitanun, W., K. Suwanborirux and S. Tanasupawat. 2014. Identification and antimicrobial activity of Streptomyces strains from Thai mangrove sediment. The Thai Journal of Pharmaceutical Sciences 38(1): 1-56.

Phongsopitanun, W., K. Suwanborirux and S. Tanasupawat. 2019. Distribution and antimicrobial activity of Thai marine actinomycetes. Journal of Applied Pharmaceutical Science 9(2): 129-134.

Plangsom, K. and P. Kanjanavas. 2015. Antibacterial activity of ethanolic extracts of Houttuynia cordata thunb., Allium sativum and Amomum krervanh pierre on some bacteria. Huachiew Chalermprakiet Science and Technology Journal 1(2): 1-10.

Quinn, G.A., A.M. Banat, A.M. Abdelhameed and I.M. Banat. 2020. Streptomyces from traditional medicine: sources of new innovations in antibiotic discovery. Journal of Medical Microbiology 69: 1040-1048.

Retnowati, Y., L. Sembiring, S. Moeljopawiro, T. Djohan, S. Endang and E.S. Soetarto. 2017. Diversity of antibiotic-producing actinomycetes in mangrove forest of Torosiaje, Gorontalo, Indonesia. Biodiversitas 18(3): 1453-1461.

Richard, H.B. 2015. Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other actinomycetes. Journal of Industrial Microbiology and Biotechnology 43(2-3): 343-370.

Rolfe, M.D., C.J. Rice, S. Lucchini, C. Pin, A. Thompson, A.D.S. Cameron, M. Alston, M.F. Stringer, R.P. Betts, J. Baranyi, M.W. Peck and C.D. Hinton. 2012. Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. Journal of Bacteriology 194: 686-701.

Ruan, C.Y., L. Zhang, W.W. Ye, X.C Xie, R. Srivibool, K. Duangmal, W. Pathom-aree, Z.X. Deng and K. Hong. 2015. Streptomyces ferrugineus sp. nov., isolated from mangrove soil in Thailand. Antonie van Leeuwenhoek 107(1): 39-45.

Saeed, S., N. Rashid, G. Jones, M. Ali and R. Hussain. 2010. Synthesis, characterization and biological evaluation of some thiourea derivatives bearing benzothiazole moiety as potential antimicrobial and anticancer agents. European Journal of Medicinal Chemistry 45(4): 1323-1331.

Sharma, P.C., A. Sinhmar, A. Sharma, H. Rajak and D.P. Pathak. 2012. Medicinal significance of benzothiazole scaffold: an insight view. Journal of Enzyme Inhibition and Medicinal Chemistry 28(2): 240-266.

Shirling, E.B. and D. Gottlieb. 1966. Method for characterization of Streptomyces species. Systematic Bacteriology 16(3): 313-340.

Sripreechasak, P., S. Tanasupawat, A. Matsumoto, Y. Inahashi, K. Suwanborirux and Y. Takahashi. 2013. Identification and antimicrobial activity of actinobacteria from soils in southern Thailand. Tropical Biomedicine 30(1): 46-55.

Stefano, R., S.A. Jackson, S. Patry and A.D.W. Dobson. 2018. Extending the “one strain many compounds” (OSMAC) principle to marine microorganisms. Marine Drugs 16(7): 244. DOI:10.3390/md16070244.

Sylvia, M., S.M. Essayag, C.H.D. Capriles, C. Perez, M.T. Colella, C. Olaizola and Y. Ontiveros. 2004. Well diffusion for antifungal susceptibility testing. Infectious Diseases 8(1): 39-45.

Wang, D., C. Wang, P. Gui, H. Liu, S.M.H. Khalaf, E.A. Elsayed, M.A.M. Wadaan, W.N. Hozzein and W. Zhu. 2017. Identification, bioactivity, and productivity of actinomycins from the marine-derived Streptomyces heliomycini. Frontiers in Microbiology 8: 1147. DOI:10.3389/fmicb.2017.01147.

Watanachote, J., N. Siranonthana, R. Watanadilok and P. Phakdee. 2017. Optimization of culture conditions for antimicrobial compounds from Streptomyces parvulus isolated from mangrove sediment. Khon Kaen Agriculture Journal 45(1): 865-871.

Watanachote, J., P. Sillapachai and N. Siranonthana. 2018. Screening of hydrolytic enzyme activity of actinomycetes isolated from mangrove sediment for application in agriculture. Khon Kaen Agriculture Journal 46(1): 1081-1086.

Watve, M.G., R. Tickoo, M.M. Jog and B.D. Bhole. 2001. How many antibiotics are produced by the genus Streptomyces? Archives of Microbiology 176(5): 386-390.

Wipa, C., N. Kuncharoen, S. Tanasupawat and P. Chanvorachotes. 2019. Lumichrome inhibits human lung cancer cell growth and induces apoptosis via a p53-dependent mechanism. Nutrition and Cancer 71(8): 1390-1402.

Zhou, Y., Y.B. Sun, H.W. He, J.T. Feng, X. Zhang and L.R. Han. 2017. Optimization of medium compositions to improve a novel glycoprotein production by Streptomyces kanasenisi ZX01. AMB Express 7(6): 1-9.