Abstract
The terrestrial actinomycete strain BCC71188 was identified as Streptomyces by its morphology (having spiral chain spore on the aerial mycelium), chemotaxonomy (containing LL-diaminopimelic acid in the cell wall), and 16S rRNA gene sequence analysis [showing high similarity values compared with Streptomyces samsunensis M1463T (99.85 %) and Streptomyces malaysiensis NBRC 16446T (99.40 %)]. The crude extract exhibited antimalarial against Plasmodium falciparum (IC50 0.19 μg/ml), anti-TB against Mycobacterial tuberculosis (MIC 6.25 μg/ml), and antibacterial against Bacillus cereus (MIC 1.56 μg/ml) activities. Therefore, chemical investigation was conducted by employing bioassay-guided method and led to the isolation of 19 compounds including two cyclic peptides (1–2), five macrolides (3–7), new naphthoquinone (8), nahuoic acid C (9), geldanamycin derivatives (10–13), cyclooctatin (14), germicidins A (15) and C (16), actinoramide A (17), abierixin, and 29-O-methylabierixin. These isolated compounds were evaluated for antimicrobial activity, such as antimalarial, anti-TB, and antibacterial activities, and for cytotoxicity against both cancerous (MCF-7, KB, NCI-H187) and non-cancerous (Vero) cells. Compounds 1–7, 10–14 exhibited antimalarial (IC50 0.22–7.14 μg/ml), and elaiophylin analogs (4–6) displayed anti-TB (MIC 0.78–12.00 μg/ml) and B. cereus (MIC 0.78–3.13 μg/ml) activities. Compounds 1, 2, 14, and abierixin displayed weak cytotoxicity, indicating a potential for antimicrobial agents.
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References
Aoki Y, Matsumoto D, Kawaide H, Natsume M (2011) Physiological role of germicidins in spore germination and hyphal elongation in Streptomyces coelicolor A3(2). J Antibiot 64(9):607–611. doi:10.1038/ja.2011.59
Aoyagi T, Aoyama T, Kojima F, Hattori S, Honma Y, Hamada M, Takeuchi T (1992) Cyclooctatin, a new inhibitor of lysophospholipase, produced by Streptomyces melanosporofaciens MI614-43F2. Taxonomy, production, isolation, physico-chemical properties and biological activities. J Antibiot 45(10):1587–1591
Aoyama T, Naganawa H, Muraoka Y, Aoyagi T, Takeuchi T (1992) The structure of cyclooctatin, a new inhibitor of lysophospholipase. J Antibiot 45(10):1703–1704
Arai M (1960) Azalomycins B and F, two new antibiotics. I. Production and isolation. J Antibiot 13:46–50
Arai T (1975) Culture media for actinomycetes. The Society for Actinomycetes Japan, Tokyo, pp. 1–131
Bindseil KU, Zeeck A (1993) Chemistry of unusual macrolides. 1. Preparation of the aglycons of concanamycin A and elaiophylin. J Org Chem 58(20):5487–5492. doi:10.1021/jo00072a036
Bunbamrung N, Dramae A, Srichomthong K, Supothina S, Pittayakhajonwut P (2014) Streptophenazines I–L from Streptomyces sp. BCC21835. Phytochem Lett 10:91–94
Carr G, Williams DE, Diaz-Marrero AR, Patrick BO, Bottriell H, Balgi AD, Donohue E, Roberge M, Andersen RJ (2010) Bafilomycins produced in culture by Streptomyces spp. isolated from marine habitats are potent inhibitors of autophagy. J Nat Prod 73:422–427
Changsen C, Franzblau SG, Palittapongarnpim P (2003) Improved green fluorescent protein reporter gene-based microplate screening for antituberculosis compounds by utilizing an acetamidase promoter. Antimicrob Agents Chemother 47(12):3682–3687
Chater KF, Chandra G (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 30(5):651–672. doi:10.1111/j.1574-6976.2006.00033.x
David L, Leal Ayala H, Tabet JC (1985) Abierixin, a new polyether antibiotic. Production, structural determination and biological activities. J Antibiot 38(12):1655–1663
DeBoer C, Meulman PA, Wnuk RJ, Peterson DH (1970) Geldanamycin, a new antibiotic. J Antibiot 23(9):442–447
Desjardins RE, Canfield CJ, Haynes JD, Chulay JD (1979) Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16(6):710–718
Ding L, Ndejouong Ble S, Maier A, Fiebig HH, Hertweck C (2012) Elaiomycins D-F, antimicrobial and cytotoxic azoxides from Streptomyces sp. strain HKI0708. J Nat Prod 75:1729–1734
Dramae A, Nithithanasilp S, Choowong W, Rachtawee P, Prabpai S, Kongsaeree P, Pittayakhajonwut P (2013) Antimalarial 20-membered macrolides from Streptomyces sp. BCC33756. Tetrahedron 69(38):8205–8208. doi:10.1016/j.tet.2013.07.034
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. doi:10.2307/2408678
Frobel K, Muller H, Bischoff E, Salcher O, de Jong A, Berschauer F, Scheer M (1990) Efomycin G and it’s use as yield promoter in animals. US Patent US 4927810:22
Genilloud O, Gonzalez I, Salazar O, Martin J, Tormo JR, Vicente F (2011) Current approaches to exploit actinomycetes as a source of novel natural products. J Ind Microbiol Biotechnol 38(3):375–389. doi:10.1007/s10295-010-0882-7
Hammann P, Kretzschmar G, Seibert G (1990) Secondary metabolites by chemical screening. 7. I. Elaiophylin derivatives and their biological activities. J Antibiot 43(11):1431–1440
Inahashi Y, Matsumoto A, Danbara H, Omura S, Takahashi Y (2010) Phytohabitans suffuscus gen. nov., sp. nov., an actinomycete of the family Micromonosporaceae isolated from plant roots. Int J Syst Evol Microbiol 60(Pt 11):2652–2658. doi:10.1099/ijs.0.016477-0
Intaraudom C, Bunbamrung N, Dramae A, Danwisetkanjana K, Rachtawee P, Pittayakhajonwut P (2015) Antimalarial and antimycobacterial agents from Streptomyces sp. BCC27095. Tetrahedron Lett 56(49):6875–6877. doi:10.1016/j.tetlet.2015.10.098
Kaiser H, Keller-Schierlein W (1981) Stoffwechselprodukte von mikroorganismen. 202. Mitteilung. Strukturaufklärung von elaiophylin: Spektroskopische untersuchungen und abbau. Helv Chim Acta 64(2):407–424. doi:10.1002/hlca.19810640206
Kawamoto I, Oka T, Nara T (1981) Cell wall composition of Micromonospora olivoasterospora, Micromonospora sagamiensis, and related organisms. J Bacteriol 146(2):527–534
Kelly K (1964) Inter-society color council–national bureau of standard color name charts illustrated with centroid colors. US Government Printing Office, Washington, DC
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120
Kretschmer A, Dorgerloh M, Deeg M, Hagenmaier H (1985) The structures of novel insecticidal macrolides: bafilomycins D and E, and oxohygrolidin. Agric Biol Chem 49(8):2509–2511. doi:10.1271/bbb1961.49.2509
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Chichester, pp. 115–148
Lee H-S, Shin HJ, Jang KH, Kim TS, Oh K-B, Shin J (2005) Cyclic peptides of the nocardamine class from a marine-derived bacterium of the genus Streptomyces. J Nat Prod 68(4):623–625. doi:10.1021/np040220g
Lin L, Ni S, Wu L, Wang Y, Wang Y, Tao P, He W, Wang X (2011) Novel 4,5-dihydro-thiazinogeldanamycin in a gdmP mutant strain of Streptomyces hygroscopicus 17997. Biosci Biotechnol Biochem 75(10):2042–2045. doi:10.1271/bbb.110361
Lu C, Li Y, Deng J, Li S, Shen Y, Wang H, Shen Y (2013) Hygrocins C-G, cytotoxic naphthoquinone ansamycins from gdmAI-disrupted Streptomyces sp. LZ35. J Nat Prod 76(12):2175–2179. doi:10.1021/np400474s
Maehr H, Benz W, Smallheer J, Williams Thomas H (1977) Mikrobielle produkte, I NMR-spektren von nocardamin und massenspektrum des tri-O-methyl-nocardamins/Microbiological products, I NMR spectra of nocardamine and mass spectra of tri-O-methyl-nocardamine. Z Naturforsch B 32(8):937–942. doi:10.1515/znb-1977-0819
Manfio GP, Zakrzewska-Czerwinska J, Atalan E, Goodfellow M (1995) Towards minimal standards for the description of Streptomyces species. Biotekhnologia 7:242–253
Nair MG, Chandra A, Thorogood DL, Ammermann E, Walker N, Kiehs K (1994) Gopalamicin, an antifungal macrodiolide produced by soil actinomycetes. J Agric Food Chem 42(10):2308–2310. doi:10.1021/jf00046a043
Nam SJ, Kauffman CA, Jensen PR, Fenical W (2011) Isolation and characterization of actinoramides A-C, highly modified peptides from a marine Streptomyces sp. Tetrahedron 67(35):6707–6712. doi:10.1016/j.tet.2011.04.051
Nong XH, Zhang XY, Xu XY, Wang J, Qi SH (2016) Nahuoic acids B-E, polyhydroxy polyketides from the marine-derived Streptomyces sp. SCSGAA 0027. J Nat Prod 79:141–148
O’Brien J, Wilson I, Orton T, Pognan F (2000) Investigation of the alamar blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 267(17):5421–5426
Park S-H, Moon K, Bang H-S, Kim S-H, Kim D-G, Oh K-B, Shin J, Oh D-C (2012) Tripartilactam, a cyclobutane-bearing tricyclic lactam from a Streptomyces sp. in a dung beetle’s brood ball. Org Lett 14(5):1258–1261. doi:10.1021/ol300108z
Petersen F, Zahner H, Metzger JW, Freund S, Hummel RP (1993) Germicidin, an autoregulative germination inhibitor of Streptomyces viridochromogenes NRRL B-1551. J Antibiot 46(7):1126–1138
Raju R, Gromyko O, Fedorenko V, Luzhetskyy A, Plaza A, Müller R (2012) Juniperolide A: a new polyketide isolated from a terrestrial actinomycete, Streptomyces sp. Org Lett 14(23):5860–5863. doi:10.1021/ol302766z
Raju R, Gromyko O, Fedorenko V, Luzketskyy A, Muller R (2015) Albaflavenol B, a new sesquiterpene isolated from the terrestrial actinomycete, Streptomyces sp. J Antibiot 68(4):286–288. doi:10.1038/ja.2014.138
Ritzau M, Heinze S, Fleck WF, Dahse HM, Grafe U (1998) New macrodiolide antibiotics, 11-O-monomethyl- and 11, 11-O-dimethylelaiophylins, from Streptomyces sp. HKI-0113 and HKI-0114. J Nat Prod 61(11):1337–1339. doi:10.1021/np9800351
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321–324
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340. doi:10.1099/00207713-16-3-313
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 28:226–231
Stead P, Latif S, Blackaby AP, Sidebottom PJ, Deakin A, Taylor NL, Life P, Spaull J, Burrell F, Jones R, Lewis J, Davidson I, Mander T (2000) Discovery of novel ansamycins possessing potent inhibitory activity in a cell-based oncostatin M signalling assay. J Antibiot 53(7):657–663
Supong K, Thawai C, Suwanborirux K, Choowong W, Supothina S, Pittayakhajonwut P (2012) Antimalarial and antitubercular C-glycosylated benz [α] anthraquinones from the marine-derived Streptomyces sp. BCC45596. Phytochem Lett 5(3):651–656. doi:10.1016/j.phytol.2012.06.015
Supong K, Thawai C, Choowong W, Kittiwongwattana C, Thanaboripat D, Laosinwattana C, Koohakan P, Parinthawong N, Pittayakhajonwut P (2016) Antimicrobial compounds from endophytic Streptomyces sp. BCC72023 isolated from rice (Oryza sativa L.). Res Microbiol. doi:10.1016/j.resmic.2016.01.004
Tamaoka J (1994) Determination of DNA base composition. In: Goodfellow M, O’Donnel AG (eds) Chemical methods in prokaryotic systematics. John Wiley & Sons, Chichester, pp. 463–470
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6 molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. doi:10.1093/molbev/mst197
Thompson JD, Higgins DG, Gobson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882
Ueki M, Suzuki R, Takamatsu S, Takagi H, Uramoto M, Ikeda H, Osada H (2009) Nocardamin production by Streptomyces avermitilis. Actinomycetologica 23(2):34–39. doi:10.3209/saj.SAJ230203
Wang GY, Graziani E, Waters B, Pan W, Li X, McDermott J, Meurer G, Saxena G, Andersen RJ, Davies J (2000) Novel natural products from soil DNA libraries in a streptomycete host. Org Lett 2(16):2401–2404
Wang X, Shaaban KA, Elshahawi SI, Ponomareva LV, Sunkara M, Zhang Y, Copley GC, Hower JC, Morris AJ, Kharel MK, Thorson JS (2013) Frenolicins C-G, pyranonaphthoquinones from Streptomyces sp. RM-4-15. J Nat Prod 76(8):1441–1447. doi:10.1021/np400231r
Williams ST, Cross T (1971) Actinomycetes. In: Booth C (ed) Methods in microbiology vol 4. Academic Press, London, pp. 295–334
Williams DE, Dalisay DS, Patrick BO, Matainaho T, Andrusiak K, Deshpande R, Myers CL, Piotrowski JS, Boone C, Yoshida M, Andersen RJ (2011) Padanamides A and B, highly modified linear tetrapeptides produced in culture by a Streptomyces sp. isolated from a marine sediment. Org Lett 13(15):3936–3939. doi:10.1021/ol2014494
Wu Z, Bai L, Wang M, Shen Y (2009) Structure–antibacterial relationship of nigericin derivatives. Chem Nat Comp 45(3):333–337. doi:10.1007/s10600-009-9350-x
Wu CZ, Jang JH, Ahn JS, Hong YS (2012) New geldanamycin analogs from Streptomyces hygroscopicus. J Microbiol Biotechnol 22(11):1478–1481
Wu C, Tan Y, Gan M, Wang Y, Guan Y, Hu X, Zhou H, Shang X, You X, Yang Z, Xiao C (2013) Identification of elaiophylin derivatives from the marine-derived actinomycete Streptomyces sp. 7-145 using PCR-based screening. J Nat Prod 76(11):2153–2157. doi:10.1021/np4006794
Yin M, Lu T, Zhao L-X, Chen Y, Huang S-X, Lohman JR, Xu L-H, Jiang C-L, Shen B (2011) The missing C-17 O-methyltransferase in geldanamycin biosynthesis. Org Lett 13(14):3726–3729. doi:10.1021/ol201383w
Zhao GS, Li SR, Wang YY, Hao HL, Shen YM, Lu CH (2013) 16,17-Dihydroxycyclooctatin, a new diterpene from Streptomyces sp. LZ35. Drug Discov Ther 7(5):185–188
Acknowledgments
The National Center for Genetic Engineering and Biotechnology (BIOTEC) and Grant for International Research Integration: Research Pyramid, Rachadapiseksomphot Endowment Fund (GCURP_58_01_33_01), Chulalongkorn University are acknowledged for the financial support. K.S. also thanks Rachadapiseksomphot Endowment Fund from Chulalongkorn University for his postdoctoral fellowship.
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This study was funded by the National Center for Genetic Engineering and Biotechnology (BIOTEC) and Rachadapiseksomphot Endowment Fund from Chulalongkorn University (GCURP_58_01_33_01).
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Supong, K., Sripreechasak, P., Tanasupawat, S. et al. Investigation on antimicrobial agents of the terrestrial Streptomyces sp. BCC71188. Appl Microbiol Biotechnol 101, 533–543 (2017). https://doi.org/10.1007/s00253-016-7804-1
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DOI: https://doi.org/10.1007/s00253-016-7804-1