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Terpenoid bioactive compound from Streptomyces rochei (M32): taxonomy, fermentation and biological activities

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Abstract

The present study emphasized the production of biologically active terpenoid compound from Streptomyces rochei M32, which was isolated from Western Ghats ecosystem, South India. The presence of resistant genes like mecA, vanA of Staphylococcus aureus and bla SHV, bla TEM of Pseudomonas aeruginosa was confirmed by molecular studies. The isolated compound from Streptomyces rochei M32 inhibited wide range of standard and clinical drug resistant pathogens and enteric pathogens. The rice bran supplemented basal medium influenced the active compound production on 8th day of fermentation and yielded 1875 mg of crude extract from 10 g of rice bran substrate. Purification and characterization of crude ethyl acetate extract was achieved by preparative thin layer chromatography. The active fraction was identified as terpenoid class compound by chemical screening. Based on the results of spectral studies (NMR, LC–MS, FTIR, etc.), the active compound was tentatively identified as 1, 19-bis (3-hydroxyazetidin-1-yl) nonadeca-5, 14-diene-1, 8, 12, 19-tetraone with molecular weight 462.41 g/mol. Minimum inhibitory concentration value ranges between 7.6 and 31.2 µg/mL against test organisms was observed. The cytotoxicity results on cervical cancer (HeLa) cell line showed IC50 value of 2.034 µg/mL. The corresponding compound is not previously reported from any microbial resources.

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References

  • Arasu MV, Duraipandiyan V, Agastian P, Ignacimuthu S (2009) In-vitro antimicrobial activity of Streptomyces spp. ERI-3 isolated from Western Ghats rock soil (India). J Mycol Med 19:22–28. doi:10.1016/j.mycmed.2008.12.002

    Article  Google Scholar 

  • Arasu MV, Ignacimuthu S, Agastian P (2012) Actinomycetes from Western Ghats of Tamil Nadu with its antimicrobial properties. Asian Pac J Trop Biomed 2:830–837. doi:10.1016/S2221-1691(12)60320-7

    Article  Google Scholar 

  • Arasu MV, Duraipandiyan V, Ignacimuthu S (2013) Antibacterial and antifungal activities of polyketide metabolite from marine Streptomyces sp. AP-123 and its cytotoxic effect. Chemosphere 90(2):479–487. doi:10.1016/j.chemosphere.2012.08.006

    Article  CAS  Google Scholar 

  • Balachandran C, Duraipandiyan V, Emi N, Ignacimuthu S (2015) Antimicrobial and cytotoxic properties of Streptomyces sp. (ERINLG-51) isolated from Southern Western Ghats. South Indian J Biol Sci 1(1):7–14

    Google Scholar 

  • Barrios GJ (2012) Solid-state fermentation: physiology of solid medium, its molecular basis and applications. Proc Biochem 47:175–185. doi:10.1016/j.procbio.2011.11.016

    Article  Google Scholar 

  • Barrios GJ, Mejia A (1996) Production of secondary metabolites by solid-state fermentation. Biotechnol Annu Rev 2:85–121. doi:10.1016/S1387-2656(08)70007-3

    Article  Google Scholar 

  • Berdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395. doi:10.1038/ja.2012.27

    Article  CAS  Google Scholar 

  • Carmichael J, William G, Graff D, Gazdar AF (1987) Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 47:936–942

    CAS  Google Scholar 

  • Cars O, Hedin A, Heddini A (2011) The global need for effective antibiotics—moving towards concerted action. Drug Resist Updat 14:68–69. doi:10.1016/j.drup.2011.02.006

    Article  Google Scholar 

  • Choma IM, Grzelak EM (2011) Bioautography detection in thin—layer chromatography. J Chromatogr A 1218:2684–2691. doi:10.1016/j.chroma.2010.12.069

    Article  CAS  Google Scholar 

  • Eccleston GP, Brooks PR, Kurtboke DI (2008) The occurrence of bioactive Micromonosporae in aquatic habitats of the sunshine coast in Australia. Mar Drugs 6:243–261. doi:10.3390/md20080012

    Article  CAS  Google Scholar 

  • Forouzanfar MH, Foreman KJ, Delossantos AM (2011) Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 378:1461–1484. doi:10.1016/S0140-6736(11)61351-2

    Article  Google Scholar 

  • Gallagher KA, Fenical W, Jensen PR (2010) Hybrid isoprenoid secondary metabolite production in terrestrial and marine actinomycetes. Curr Opin Biotechnol 21:794–800. doi:10.1016/j.copbio.2010.09.010

    Article  CAS  Google Scholar 

  • Genilloud O (2014) The re-emerging role of microbial natural products in antibiotic discovery. Antonie Van Leeuwenhoek 106:173–188. doi:10.1007/s10482-014-0204-6

    Article  CAS  Google Scholar 

  • Goodfellow M, Williams E (1986) New strategies for the selective isolation of industrially important bacteria. Biotechnol Genet Eng Rev 4:213

    Article  CAS  Google Scholar 

  • Gopinath BV, Charya MAS (2013) Characterization of antibacterial compounds produced by the actinomycetes using NMR spectral analysis. Int J Pharm Sci Res 4:25–35

    Article  Google Scholar 

  • Hardt IH, Jensen PR, Fenical W (2000) Neomarinone, and new cytotoxic marinone derivatives, produced by a marine filamentous bacterium (actinomycetales). Tetrahedron Lett 41:2073–2076. doi:10.1016/S0040-4039(00)00117-9

    Article  CAS  Google Scholar 

  • Harindran J, Gupte TE, Naik SR (1999) HA-1-92, A new antifungal antibiotic produced by Streptomyces CDRIL-312: fermentation, isolation, purification and biological activity. World J Microbiol Biotechnol 15:425–430. doi:10.1023/A:1008934808486

    Article  CAS  Google Scholar 

  • Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319–322. doi:10.2323/jgam.29.319

    Article  CAS  Google Scholar 

  • Holkar S, Begde D, Nashikkar N, Kadam T, Upadhyay A (2013) Rhodomycin analogues from Streptomyces purpurascens: isolation, characterization and biological activities. Springer Plus 2(1):93. doi:10.1186/2193-1801-2-93

    Article  Google Scholar 

  • Hozzein WN, Goodfellow M (2007) Streptomyces synnematoformans sp. nov., a novel actinomycete isolated from a sand dune soil in Egypt. Int J Syst Evol Microbiol 57:2009–2013. doi:10.1099/ijs.0.65037-0

    Article  CAS  Google Scholar 

  • Jiang X, Zhang Z, Li M, Zhou D, Ruan F, Lu Y (2006) Detection of extended-spectrum β—lactamases in clinical isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 50:2990–2995. doi:10.1128/AAC.01511-05

    Article  CAS  Google Scholar 

  • Karuppiah V, Aarthi C, Sivakumar K, Kannan L (2013) Statistical optimization and anticancer activity of a red pigment isolated from Streptomyces sp. PM4. Asian Pac J Trop Biomed 3:650–656. doi:10.1016/S2221-1691(13)60131-8

    Article  CAS  Google Scholar 

  • Lee CH, Lim H, Moon S, Shin C, Kim S, Kim BJ, Lim Y (2007) Novel anticancer agent, benzyldihydroxyoctenone, isolated from Streptomyces sp. causes G1 cell cycle arrest and induces apoptosis of HeLa cells. Cancer Sci 98:795–802. doi:10.1111/j.1349-7006.2007.00473.x

    Article  CAS  Google Scholar 

  • Li XZ, Nikaido H, Poole K (1995) Role of MexA-MexB-OprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39:1948–1953. doi:10.1128/AAC.39.9.1948

    Article  CAS  Google Scholar 

  • Manivasagan P, Sivasankar P, Venkatesan J, Senthilkumar K, Sivakumar K, Kim SK (2013) Production and characterization of an extracellular polysaccharide from Streptomyces violaceus MM72. Int J Biol Macromol 59:29–38. doi:10.1016/j.ijbiomac.2013.04.012

    Article  CAS  Google Scholar 

  • Manivasagan P, Venkatesan V, Sivakumar K, Se-Kwon K (2014) Pharmaceutically active secondary metabolites of marine actinobacteria. Microbiol Res 169:262–278. doi:10.1016/j.micres.2013.07.014

    Article  CAS  Google Scholar 

  • Motohashi K, Irie K, Toda T, Matsuo Y, Kasai H, Sue M, Furihata K, Seto H (2008) Studies on terpenoids produced by actinomycetes. 5-dimethylallylindole-3-carboxylic Acid and A80915G-8”-acid produced by marine-derived Streptomyces sp. MS239. J Antibiot 61:75–80. doi:10.1038/ja.2008.113

    Article  CAS  Google Scholar 

  • Nachtigall J, Kulik A, Helaly S, Bull AT, Goodfellow M, Asenjo JA, Maier A, Wiese J, Imhoff JF, Sussmuth RD, Fiedler HP (2011) Atacamycins A-C, 22-membered antitumor macrolactones produced by Streptomyces sp. C38. J Antibiot 64:775–780. doi:10.1038/ja.2011.96

    Article  CAS  Google Scholar 

  • Naggar EI, Moustafa Y, Samy AE, Sahar MA (2009) Solid-state fermentation for the production of meroparamycin by Streptomyces sp. strain MAR01. J Microbiol Biotechnol 19:468–474. doi:10.4014/jmb.0807.457

    Article  Google Scholar 

  • Nampoothiri KN, Ramkumar B, Pandey A (2013) Western Ghats of India: rich source of microbial diversity. J Sci Indus Res 72:617–623

    Google Scholar 

  • Pathirana C, Jensen PR, Fenical W (1992) Marinone and debromomarinone—antibiotic sesquiterpenoid naphthoquinones of a new structure class from a marine bacterium. Tetrahedron Lett 33:7663–7666. doi:10.1016/0040-4039(93)88010-G

    Article  CAS  Google Scholar 

  • Qin S, Xing K, Jiang JH, Xu LH, Li WJ (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol 89:457–473. doi:10.1007/s00253-010-2923-6

    Article  CAS  Google Scholar 

  • Radhakrishnan M, Gopikrishnan V, Suresh A, Selvakumar N, Balagurunathan R, Kumar Vanaja (2013) Characterization and phylogenetic analysis of antituberculous compound producing actinomycete strain D25 isolated from Thar Desert soil, Rajasthan. Bioinformation 9:18–22

    Article  Google Scholar 

  • Radhakrishnan M, Anuradha Raman V, Bharathi S, Balagurunathan R, Kumar Vanaja (2014a) Anti MRSA and antitubercular activity of phenoxazinone containing molecule from Borra caves Streptomyces sp. BCA1. Int J Pharm Sci Res 5:5342–5348

    Google Scholar 

  • Radhakrishnan M, Gopikrishnan V, Balaji S, Balagurunathan R, Kumar Vanaja (2014b) Bioactive potential of actinomycetes from less explored ecosystems against Mycobacterium tuberculosis and other non-mycobacterial pathogens. Int Sch Res Not 812974:1–9. doi:10.1155/2014/812974

    Google Scholar 

  • Radhakrishnan M, Pazhanimurugan R, Gopikrishnan V, Balagurunathan R, Kumar Vanaja (2014c) Streptomyces sp. D25 isolated from Thar Desert soil, Rajasthan producing pigmented antituberculosis compound only in solid culture. J Pure Appl Microbiol 8:333–337

    Google Scholar 

  • Rather SA, Kumar S, Rah B, Arif M, Ali A, Qazi P (2014) A potent cytotoxic metabolite from terrestrial actinomycete, Streptomyces collinus. Med Chem Res 23:382–387. doi:10.1007/s00044-013-0640-2

    Article  CAS  Google Scholar 

  • Rios JL, Recio MC, Villar A (1988) Screening methods for natural products with antimicrobial activity—a review of the literature. J Ethnapharmacol 23:127–149. doi:10.1016/0378-8741(88)90001-3

    Article  CAS  Google Scholar 

  • Ruoyu M, Teng D, Wang X, Xi D, Zhang Y, Hu X, Yang Y, Wang J (2013) Design, expression, and characterization of a novel targeted plectasin against methicillin-resistant Staphylococcus aureus. Appl Microbiol Biotechnol 97:3991–4002. doi:10.1007/s00253-012-4508-z

    Article  Google Scholar 

  • Sathiyanarayanan G, Gandhimathi R, Sabarathnam B, Kiran GS, Selvin J (2014) Optimization and production of pyrrolidone antimicrobial agent from marine sponge-associated Streptomyces sp. MAPS15. Bioprocess Biosyst Eng 37:561–573. doi:10.1007/s00449-013-1023-2

    Article  CAS  Google Scholar 

  • Sharma D, Kaur T, Chadha BS, Manhas RK (2011) Antimicrobial activity of actinomycetes against multidrug resistant Staphylococcus aureus, E. coli and various other pathogens. Trop J Pharm Res 10:801–803. doi:10.4314/tjpr.v10i6.14

    Article  Google Scholar 

  • Shiriling EB, Gottlieb D (1996) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 6:313–340. doi:10.1099/00207713-16-3-313

    Google Scholar 

  • Shomura T, Yoshida J, Amano S, Ojima MK, Inouye S, Niida T (1993) Studies on Actinomycetales producing antibiotics only on agar culture. I. Screening, taxonomy and morphology-productivity relationship of Streptomyces halstedii, strain SF-1993. J Antibiot 32:427–435. doi:10.7164/antibiotics.32.427

    Article  Google Scholar 

  • Tadayonia M, Sheikh Zeinoddin M, Soleimanian-Zad S (2015) Isolation of bioactive polysaccharide from acorn and evaluation of its functional properties. Int J Biol Macromol 72:179–184. doi:10.1016/j.ijbiomac.2014.08.015

    Article  Google Scholar 

  • Ulrich M, Lankes U, Fischpera K, Frimmel FH (2009) The concentration of polysaccharides and proteins in EPS of Pseudomonas putida and Aureobasidum pullulans as revealed by 13C CPMAS NMR spectroscopy. Appl Microbiol Biotechnol 85:197–206. doi:10.1007/s00253-009-2218-y

    Article  Google Scholar 

  • Velayudam S, Murugan K (2015) Sequential optimization approach for enhanced production of antimicrobial compound from Streptomyces rochei BKM-4. South Indian J Biol Sci 1(2):72–79

    Google Scholar 

  • Wielders CLC, Fluit AC, Brisse S, Verhoef J, Schmitz FJ (2002) mecA gene is widely disseminated in Staphylococcus aureus population. J Clin Microbiol 40:3970–3975. doi:10.1128/JCM.40.11.3970-3975.2002

    Article  CAS  Google Scholar 

  • Yamashita N, Ya KS, Furihata K, Hayakawa Y, Seto H (1998) New ravidomycin analogues, FE35A and FE35B apoptosis inducers produced by Streptomyces rochei. J Antibiot 51:1105–1108. doi:10.7164/antibiotics.51.1105

    Article  CAS  Google Scholar 

  • Yang SS, Ling MY (1989) Tetracycline production with sweet potato residue by solid state fermentation. Biotechnol Bioeng 33:1021–1028. doi:10.1002/bit.260330811

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Vice Chancellor and the Registrar of the Periyar University, Salem for providing all of the facilities to carry out this work. One of the author, R. Pazhani Murugan, wishes to thank the UGC-BSR, New Delhi for financial supportive of present study.

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Authors and Affiliations

  1. Actinobacterial Research Laboratory, Department of Microbiology, Periyar University, Periyar Palkalai Nagar, Salem, Tamil Nadu, 636 011, India

    Raasaiyah Pazhanimurugan, Thangavel Shanmugasundaram & Ramasamy Balagurunathan

  2. Centre for Drug Discovery and Development, Sathyabama University, Jeppiar Nagar, Chennai, Tamil Nadu, 600 119, India

    Manikkam Radhakrishnan & Venugopal Gopikrishnan

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  1. Raasaiyah Pazhanimurugan
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  2. Manikkam Radhakrishnan
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  3. Thangavel Shanmugasundaram
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  4. Venugopal Gopikrishnan
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  5. Ramasamy Balagurunathan
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Correspondence to Ramasamy Balagurunathan.

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Pazhanimurugan, R., Radhakrishnan, M., Shanmugasundaram, T. et al. Terpenoid bioactive compound from Streptomyces rochei (M32): taxonomy, fermentation and biological activities. World J Microbiol Biotechnol 32, 161 (2016). https://doi.org/10.1007/s11274-016-2121-5

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