Abstract
Actinobacteria is a prolific producer of complex natural products; we isolated a potential marine Streptomyces sp. PM49 strain from Bay of Bengal coastal area of India. The strain PM49 exhibited highly efficient antibacterial properties on multidrug-resistant pathogens with a zone of inhibition of 14–17 mm. SSF was adopted for the production of the secondary metabolites from PM49 with ISP2; utilizing agricultural wastes for compound extraction was also attempted. Bioactive fraction of Rf value 0.69 resolved using chloroform and ethyl acetate (1:1, v/v) was obtained and subjected to further analysis. Based on UV, IR, ESI-MS, and 1H and 13C NMR spectral analysis, it was revealed that the compound is closely similar to cyslabdan with a molecular mass of 467.66 corresponding to the molecular formula C25H41NO5S. ESBL and MBL production was screened in the hospital test isolates of Pseudomonas aeruginosa, Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus. PCR amplification in the phenotypically positive strains was positive for bla IMP, bla SHV, bla CTX-M, and mec genes. The β-lactamase enzyme from tested strains had cephalosporinase activity with a 31-kDa protein and isolated compound from the strain possessing β-lactamase inhibitory potential. MIC of the active fraction was 16–32 μg/ml on ATCC strains; the ceftazidime and meropenem sensitive and resistant test strains showed MIC of 64–256 μg/ml. The Streptomyces sp. PM49 aerial mycelium was rectiflexibile; the 16S rRNA showed 99 % identity with Streptomyces rochei and submitted at Genbank with accession no JX904061.1.
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Lee, K., Chong, Y., Shin, H. B., Kim, Y. A., Yong, D., & Yum, J. H. (2001). Modified Hodge and EDTA disk synergy test to screen metallo beta lactamases producing strains of Pseudomonas spp and Acinetobacter spp. Clinical Microbiology and Infection, 7, 88–91.
Maninder, K., & Aruna, A. (2013). Occurrence of CTX-M, SHV and the TEM genes among the extended spectrum â-lactamase producing isolates of Enterobacteriaceae in a tertiary care hospital of North India. Journal of Clinical Diagnostic Research, 7(4), 642–645.
Andrea, M. H., Kristine, M. H., Marion, S. H., Vernon, E. A., & Robert, A. B. (2002). Amino acid substitutions at Ambler position Gly238 in the SHV-1 β-lactamase: exploring sequence requirements for resistance to penicillins and cephalosporins. Antimicrobial Agents and Chemotherapy, 46(12), 3971–3977.
Wright, G. D. (2005). Bacterial resistance to antibiotics: enzymatic degradation and modification. Advanced Drug Delivery Review, 57, 1451–1470.
Fenical, W., & Jensen, P. R. (2006). Developing a new resource for drug discovery: marine actinomycete bacteria. Nature Chemical Biology, 2, 666–673.
Wu, S. J., Fotso, S., Li, F., Qin, S., & Laatsch, H. (2007). Amorphane sesquiterpenes from a marine Streptomyces sp. Journal of Natural Products, 70, 304–306.
Atsushi, F., Yong, P. K., Hideaki, H., Kazuro, S., Hiroshi, T., & Satoshi, O. (2008). Cyslabdan, a new potentiator of imipenem activity against methicillin-resistant Staphylococcus aureus, produced by Streptomyces sp. K04-0144 II. Biological activities. Journal of Antibiotics, 61(1), 7–10.
Eccleston, G. P., Brooks, P. R., & Kurtboke, D. I. (2008). The occurrence of bioactive Micromonosporae in aquatic habitats of the Sunshine Coast in Australia. Marine Drugs, 6, 243–261.
Yilmaz, E. B., Yavuz, M., & Kizil, M. (2008). Molecular characterization of rhizosphere soil Streptomycetes isolated from indigenous Turkish plants and their antimicrobial activity. World Journal of Microbiology and Biotechnology, 24, 1461–1470.
Kelman, D., Kashman, Y., Rosenberg, E., Kushmaro, A., & Loya, Y. (2006). Antimicrobial activity of red sea corals. Marine Biology, 149, 357–363.
Usha, R., Ananthaselvi, P., Venil, C. K., & Palaniswamy, M. (2010). Antimicrobial and antiangiogenesis activity of Streptomyces parvulus KUAP106 from mangrove soil. European Journal of Biological Sciences, 2, 77–83.
Sahin, N., & Ugur, A. (2003). Investigation of the antimicrobial activity of some Streptomyces isolates. Turkish Journal of Biology, 27, 73–78.
Augustine, S., Bhavasar, S. P., & Kapadnis, B. P. (2005). A non polyene antifungal antibiotic from Streptomyces albidofalvus PU 23. Journal of Bioscience, 30, 201–211.
Lee, K., Lee, W. G., Uh, Y., Ha, G. Y., Chong, Y., et al. (2003). VIM and IMP type metallo-beta-lactamase producing Pseudomonas spp. and Acinetobacter spp. in Korean hospitals. Emergency Infectious Diseases, 9(7), 868–871.
Zhang, Z., Li, M., Zhou, D., Ruan, F., Lu, Y., et al. (2006). Detection of extended-spectrum b-lactamases in clinical isolates of Pseudomonas aeruginosa. Antimicrobial Agents Chemotherapy, 50(9), 2990–2995.
Perez-Perez, F. J., & Hanson, N. D. (2002). Detection of plasmid-mediated AmpC ß-lactamase genes in clinical isolates by using multiplex PCR. Journal of Clinical Microbiology, 40, 2153–2162.
Wang, Z., & Benkovic, S. J. (1998). Purification, characterization, and kinetic studies of a soluble Bacteroides fragilis metallo-β-lactamase that provides multiple antibiotic resistance. Journal of Biological Chemistry, 273(35), 22402–22408.
Falagas, M. E., & Bliziotis, I. A. (2007). Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? International Journal of Antimicrobial Agents, 29, 630–636.
Feng, Y. C., Siu, L. K., Chang, P. F., Min Hua, H., & Monto, H. (2001). Diversity of SHV and TEM β-lactamases in Klebsiella pneumoniae: gene evolution in Northern Taiwan and two novel β-lactamases, SHV-25 and SHV-26. Antimicrobial Agents and Chemotherapy, 45(9), 2407–2413.
Andrews, J. M. (2001). Determination of minimum inhibitory concentration. Journal of Antimicrobial and Chemothereapy, 48(Suppl. 1), 5–16.
Sibanda, T., & Okoh, A. I. (2008). In vitro antibacterial regimes of crude aqueous and acetone extracts of Garcinia kola seeds. Journal of Biological Science, 8, 149–154.
Sathish Kumar, S.R., & Kokati, V.B.R. (2012). In-vitro antimicrobial activity of marine actinobacteria against multidrug resistance Staphylococcus aureus. Asia Pacific Journal of Tropical Biomedicine, S1802–S1807.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
De Pestel, D. D., Benninger, M. S., Danziger, L., LaPlante, K. L., May, C., Luskin, A., Pichichero, M., & Hadley, J. A. (2003). Cephalosporin use in treatment of patients with penicillin allergies. Journal of American Pharmaceutical Association, 48, 530–540.
Valan Arasu, M., 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.
Zhonghui, Z., Wei, Z., Yaojian, H., Zhiyuan, Y., Jun, L., Huirong, C., & Wenjin, S. (2000). Detection of antitumor and antimicrobial activities in marine organism associated actinomycetes isolated from the Taiwan Strait, China. FEMS Microbiology Letters, 188, 87–91.
Gupta, M. D., & Kulkarni, P. R. (2002). A study of antifungal antibiotic production by Streptomyces chattanoogensis MTCC 3423 using full factorial design. Letters in Applied Microbiology, 35, 22–26.
El-Naggar, M. Y., EL-Assar, S. A., & Abdul Gawad, S. M. (2009). Solid state fermentation for the production of meroparamycin by Streptomyces sp. strain MAR01. Journal of Microbiology and Biotechnology, 19(5), 468–473.
Remya, M., & Vijayakumar, R. (2008). Isolation and characterization of marine antagonistic actinomycetes from west coast of India. Journal of Medicine and Biology, 15, 13–19.
Sekiguchi, M., Shiraish, N., Kobinata, K., Kudo, T., Yamaguchi, I., Osada, H., & Isono, K. (2007). RS-22A and C: new macrolide antibiotics from Streptomyces violaceusniger, taxonomy, fermentation, isolation and biological activities. Journal of Antibiotics, 48(4), 289–292.
Joseph, G. P., Stephane, B., Jean, M. F., Pierre, N., Bathelemy, N., Anatole, A., et al. (2007). Screening of some medicinal plants from cameroon for beta-lactamase inhibitory activity. Phytotherapy Research. Phytotherapy Research, 21(3), 284–287.
Masashi, T., Masaaki, Y., Seiko, O., Yasushi, T., Yasutake, H., Yuzuru, M., Ayumi, S., Hironori, F., Yasushi, O., & Junichi, K. (2005). Brasilibactin A, a cytotoxic compound from actinomycete Nocardia brasiliensis. Journal of Natural Products, 68(3), 462–464.
Siddhartha, R. C., Raymond, E. K., David, N. B., & Wu Kuand, Y. (1996). Methicillin-resistant Staphylococcus aureus: S. Antimicrobial Agents and Chemotherapy, 40(9), 2075–2079.
Mark, S. B. (2005). Natural products to drugs: natural product derived compounds in clinical trials. Natural Products Reports, 22, 162–195.
Venkata, R., Murali, K., Murali, Y. N., & Sri Rami, R. D. (2012). Novel pyridinium compound from marine actinomycete, Amycolatopsis alba var. nov. DVR D4 showing antimicrobial and cytotoxic activities in vitro. Microbiology Research, 167(6), 346–351.
Sathish Kumar, S.R., & Kokati, V.B.R. (2012). In-vitro antimicrobial activity of marine actinobacteria against multidrug resistance Staphylococcus aureus. Asia Pacific Journal of Tropical Biomedicine, S1802-S1807.
Ekrem, K., & Mettem, Y. C. (2006). Comparison of staphylococcal beta-lactamase detection. FABAD Journal of Pharmaceutical Science, 31, 79–84.
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., et al. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36, 465–469.
Julain, D., & Dorothy, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417–433.
Acknowledgments
The authors are indebted to the microbiology staff members and physicians of the tertiary care hospital, Bangalore, for helping us in collecting the samples and providing ATCC strains, and they also acknowledge the technicians for their help. The authors also thank the Vice-Chancellor and Registrar of Periyar University, Salem, for their support and encouragement. This work was supported by the Indian Council of Medical Research [ICMR] New Delhi, India (ICMR letter no. 5/8/5/24/9/2011—ECD-I, dt.19.12.11).
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Shanthi, J., Senthil, A., Gopikrishnan, V. et al. Characterization of a Potential β-Lactamase Inhibitory Metabolite from a Marine Streptomyces sp. PM49 Active Against Multidrug-Resistant Pathogens. Appl Biochem Biotechnol 175, 3696–3708 (2015). https://doi.org/10.1007/s12010-015-1538-x
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DOI: https://doi.org/10.1007/s12010-015-1538-x