Abstract
Streptomyces have been reported as a remarkable source for bioactive secondary metabolites with complex structural and functional diversity. In this study, 35 isolates of genus Streptomyces were purified from rhizospheric and marine soils collected from previously unexplored habitats and screened for antimicrobial activities. One of these isolates, G1, when tested in vitro, was found highly active against wide range of microbes including Gram-positive, Gram-negative bacteria, and different fungal pathogens. It was identified as mesophilic, alkaliphilic, and moderately halotolerant as it showed optimum growth at temperature 30 °C, pH 8.0 in casein-starch-peptone-yeast extract-malt extract medium supplemented with 5% NaCl. Sequence analysis of the 16S rRNA gene indicated 100% identity of this isolate to Streptomyces fimbriatus. Moreover, maximum antimicrobial activity was achieved in starch nitrate medium supplemented with 1% glycerol as carbon and 0.03% soy meal as nitrogen source. The antimicrobial compounds produced by this isolate were extracted in methanol. Bioassay-guided fractionation through thin layer chromatography of methanolic extract resulted in the separation of a most active fraction with an Rf value of 0.46. This active fraction was characterized by FTIR and LCMS analysis and found similar to streptothricin D like antibiotic with m/z 758.42.
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Ahmad MS, El-Gendy AO, Ahmed RR, Hassan HM, El-Kabbany HM, Merdash AG (2017) Exploring the antimicrobial and antitumor potentials of Streptomyces sp. AGM12–1 isolated from Egyptian soil. Front Microbiology 8:438. https://doi.org/10.3389/fmicb.2017.00438
Anukool U, Gaze WH, Wellington EM (2004) In situ monitoring of streptothricin production by Streptomyces rochei F20 in soil and rhizosphere. App Environ Microbiol 70(9):5222–5228. https://doi.org/10.1128/AEM.70.9.5222-5228.2004
Arul Jose P, Satheeja Santhi V, Jebakumar SR (2011) Phylogenetic‐affiliation, antimicrobial potential and PKS gene sequence analysis of moderately halophilic Streptomyces sp. inhabiting an Indian saltpan. J Basic Microbiol 51 (4):348–356. https://doi.org/10.1002/jobm.201000253
Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65(8):385–395. https://doi.org/10.1038/ja.2012.27
Betancur LA, Naranjo-Gaybor SJ, Vinchira-Villarraga DM, Moreno-Sarmiento NC, Maldonado LA, Suarez-Moreno ZR, Acosta-González A, Padilla-Gonzalez GF, Puyana M, Castellanos L (2017) Marine Actinobacteria as a source of compounds for phytopathogen control: an integrative metabolic-profiling/bioactivity and taxonomical approach. PLoS One 12(2):e0170148. https://doi.org/10.1371/journal.pone.0170148
Bhave S, Shanbhag P, Sonawane S, Parab R, Mahajan G (2013) Isolation and characterization of halotolerant Streptomyces radiopugnans from Antarctica soil. Lett App Microbiol 56(5):348–355. https://doi.org/10.1111/lam.12054
Castro JF, Razmilic V, Gomez-Escribano JP, Andrews B, Asenjo JA, Bibb MJ (2015) Identification and heterologous expression of the chaxamycin biosynthesis gene cluster from Streptomyces leeuwenhoekii. App Environ Microbiol 81 (17):5820–5831.
Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proceedings of the Nat Acad of Sci 100(suppl 2):14555–14561. https://doi.org/10.1128/AEM.01039-15
Cumsille A, Undabarrena A, González V, Claverías F, Rojas C, Cámara B (2017) Biodiversity of actinobacteria from the South Pacific and the assessment of Streptomyces chemical diversity with metabolic profiling. Mar Drugs 15(9):286. https://doi.org/10.3390/md15090286
Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24(5):1073–1109. https://doi.org/10.1039/b514050c
Fernández-Moreno MA, Vallin C, Malpartida F (1997) Streptothricin biosynthesis is catalyzed by enzymes related to nonribosomal peptide bond formation. J Bacteriol 179(22):6929–6936. https://doi.org/10.1128/JB.179.22.6929-6936.1997
Forar LR, Ali E, Mahmoud S, Bengraa CH, Hacene H (2007) Screening, isolation and characterization of a novel antimicrobial producing actinomycete, strain RAF10. Biotechnol 6 (4): 489–496. https://scialert.net/abstract/?doi=biotech.2007.489.496
Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J System Evol Microbiol 24(1):54–63. https://doi.org/10.1099/00207713-24-1-54
Grammel N, Pankevych K, Demydchuk J, Lambrecht K, Saluz HP, Keller U, Krügel H (2002) A β-lysine adenylating enzyme and a β-lysine binding protein involved in poly β-lysine chain assembly in nourseothricin synthesis in Streptomyces noursei. Europ J Biochem 269(1):347–357. https://doi.org/10.1046/j.0014-2956.2001.02657.x
Horinouchi S, Furuya K, Nishiyama M, Suzuki H, Beppu T (1987) Nucleotide sequence of the streptothricin acetyltransferase gene from Streptomyces lavendulae and its expression in heterologous hosts. J Bacteriol 169(5):1929–1937. https://doi.org/10.1128/jb.169.5.1929-1937.1987
Huck TA, Porter N, Bushell ME (1991) Positive selection of antibiotic-producing soil isolates. Microbiol 137(10):2321–2329. https://doi.org/10.1099/00221287-137-10-2321
Ji Z, Wei S, Zhang J, Wu W, Wang M (2008) Identification of streptothricin class antibiotics in the early stage of antibiotics screening by electrospray ionization mass spectrometry. J Antibiot 61(11):660–667. https://doi.org/10.1038/ja.2008.93
Jonsbu E, Mcintyre M, Nielsen J (2002) The influence of carbon sources and morphology on nystatin production by Streptomyces noursei. J Biotechnol 95(2):133–144. https://doi.org/10.1016/s0168-1656(02)00003-2
Khaliq S, Ghauri MA, Akhtar K (2013) Isolation, identification and optimization of fermentation parameters for improved production of antimicrobial compounds from indigenous Streptomyces isolates. Afr J Microbiol Res 7(18):1874–1887. https://doi.org/10.5897/AJMR2012.2462
Kim BT, Lee JY, Lee YY, Kim OY, Chu JH, Goo YM (1994) N-Methylstreptothricin DA new streptothricin-group antibiotic from a Streptomyces spp. J Antibiot 47(11):1333–1336. https://doi.org/10.7164/antibiotics.47.1333
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33 (7):1870–1874. https://doi.org/10.1093/molbev/msw054
Küster E, Williams S (1964) Selection of media for isolation of Streptomycetes. Nat 202(4935):928–929. https://doi.org/10.1038/202928a0
Ladurner A, Zehl M, Grienke U, Hofstadler C, Faur N, Pereira FC, Berry D, Dirsch VM, Rollinger JM (2017) Allspice and clove as source of triterpene acids activating the G protein-coupled bile acid receptor TGR5. Front Pharmacol 8:468. https://doi.org/10.3389/fphar.2017.00468
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J System Evol Microbiol 20(4):435–443. https://doi.org/10.1099/00207713-20-4-435
Li J, Guo Z, Huang W, Meng X, Ai G, Tang G, Chen Y (2013) Mining of a streptothricin gene cluster from Streptomyces sp. TP-A0356 genome via heterologous expression. Sci Chi Life Sci 56 (7):619–627. https://doi.org/10.1007/s11427-013-4504-2
Liu D, Coloe S, Baird R, Pedersen J (2000) Rapid mini-preparation of fungal DNA for PCR. J Clinic Microbiol 38(1):471–471
Manivasagan P, Venkatesan J, Sivakumar K, Kim S-K (2014) Pharmaceutically active secondary metabolites of marine actinobacteria. Microbiol Res 169(4):262–278. https://doi.org/10.1016/j.micres.2013.07.014
Maruyama C, Toyoda J, Kato Y, Izumikawa M, Takagi M, Shin-ya K, Katano H, Utagawa T, Hamano Y (2012) A stand-alone adenylation domain forms amide bonds in streptothricin biosynthesis. Nat Chem Biol 8(9):791–797. https://doi.org/10.1038/nchembio.1040
Nah H-J, Pyeon H-R, Kang S-H, Choi S-S, Kim E-S (2017) Cloning and heterologous expression of a large-sized natural product biosynthetic gene cluster in Streptomyces species. Front Microbiol 8:394. https://doi.org/10.3389/fmicb.2017.00394
Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75(3):311–335. https://doi.org/10.1021/np200906s
Pitt JJ (2009) Principles and applications of liquid chromatography-mass spectrometry in clinical biochemistry. Clinic Biochem Rev 30(1):19
Pridham T, Gottlieb D (1948) The utilization of carbon compounds by some Actinomycetales as an aid for species determination. J Bacteriol 56(1):107. https://doi.org/10.1128/JB.56.1.107-114.1948
Rajeswari P, Jose PA, Amiya R, Jebakumar SRD (2015) Characterization of saltern based Streptomyces sp. and statistical media optimization for its improved antibacterial activity. Front Microbiol 5:753. https://doi.org/10.3389/fmicb.2014.00753
Reddy T, Mahmood S, Paris L, Reddy YHK, Wellington E, Idris MM (2011) Streptomyces hyderabadensis sp. nov., an actinomycete isolated from soil. Int J System Evolut Microbiol 61 (1):76–80.https://doi.org/10.1099/ijs.0.020446-0
Saadoun I, Muhana A (2008) Optimal production conditions, extraction, partial purification and characterization of inhibitory compound (s) produced by Streptomyces Ds-104 isolate against multi-drug resistant Candida albicans. Curr Trend Biotechnol Pharm 2(2):402–432
Sahana A, Das S, Saha R, Gupta M, Laskar S, Das D (2011) Identification and interaction of amino acids with leucine-anthracene reagent by TLC and spectrophotometry: experimental and theoretical studies. J Chromato Sci 49(8):652–655. https://doi.org/10.1093/chrsci/49.8.652
Ser HL, Tan WS, Ab Mutalib NS, Yin WF, Chan KG, Goh BH, Lee LH (2016) Draft genome sequence of mangrove-derived Streptomyces sp. MUSC 125 with antioxidant potential. Front Microbiol 7:1470.https://doi.org/10.3389/fmicb.2016.01470
Sharma P, Kalita MC, Thakur D (2016) Broad spectrum antimicrobial activity of forest-derived soil actinomycete, Nocardia sp. PB-52. Front Microbiol 7:347. https://doi.org/10.3389/fmicb.2016.00347
Shetty PR, Buddana SK, Tatipamula VB, Naga YVV, Ahmad J (2014) Production of polypeptide antibiotic from Streptomyces parvulus and its antibacterial activity. Braz J Microbiol 45(1):303–312. https://doi.org/10.1590/S1517-83822014005000022
Shirling ET, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J System Bacteriol 16(3):313–340. https://doi.org/10.1099/00207713-16-3-313
Shrivastava P, Kumar R, Yandigeri M (2017) In vitro biocontrol activity of halotolerant Streptomyces aureofaciens K20: a potent antagonist against Macrophomina phaseolina (Tassi) Goid. Saudi J Biol Sci 24(1):192–199. https://doi.org/10.1016/j.sjbs.2015.12.004
Singh LS, Sharma H, Talukdar NC (2014) Production of potent antimicrobial agent by actinomycete, Streptomyces sannanensis strain SU118 isolated from phoomdi in Loktak Lake of Manipur. India BMC Microbiol 14(1):278. https://doi.org/10.1186/s12866-014-0278-3
Vijayakumar R, Selvam KP, Muthukumar C, Thajuddin N, Panneerselvam A, Saravanamuthu R (2012) Antimicrobial potentiality of a halophilic strain of Streptomyces sp. VPTSA18 isolated from the saltpan environment of Vedaranyam, India. Annal Microbiol 62 (3):1039–1047. https://doi.org/10.1007/s13213-011-0345-z
Wang X, Huang L, Kang Z, Buchenauer H, Gao X (2010) Optimization of the fermentation process of actinomycete strain Hhs. 015T. J Biomed Biotechnol 2010
Wang Y, Fang X, An F, Wang G, Zhang X (2011) Improvement of antibiotic activity of Xenorhabdus bovienii by medium optimization using response surface methodology. Microb Cell Fact 10(1):98. https://doi.org/10.1155/2010/141876
Williams S, Goodfellow M, Wellington E, Vickers J, Alderson G, Sneath P, Sackin M, Mortimer A (1983) A probability matrix for identification of some Streptomycetes. Microbiol 129(6):1815–1830. https://doi.org/10.1099/00221287-129-6-1815
Xiang W, Liu C, Wang X, Du J, Xi L, Huang Y (2011) Actinoalloteichus nanshanensis sp. nov., isolated from the rhizosphere of a fig tree (Ficus religiosa). Int J System Evol Microbiol 61 (5):1165–1169.https://doi.org/10.1099/ijs.0.023283-0
Yagüe P, López-García MT, Rioseras B, Sánchez J, Manteca A (2013) Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives. FEMS Microbiol Lett 342(2):79–88. https://doi.org/10.1111/1574-6968.12128
Acknowledgements
We acknowledge Higher Education Commission (HEC), Pakistan, for providing opportunity to conduct a part of this research project in University of Freiburg, Germany, under International Research Initiative Program (IRSIP).
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This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors but a part of this research work has been done during IRSIP training program funded by HEC.
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Neelma Ashraf investigated, wrote original draft and editing. Andreas Bechthold participated in methodology, data curation, and editing. Munir Ahmad Anwar was involved in the investigation and editing of the manuscript. M. Afzal Ghauri reviewed and edited the manuscript. M. Sultan Anjum participated in formal analysis, reviewing and editing. Ali Nisar Khan was involved in methodology development and analysis. Kalsoom Akhtar was involved in writing-reviewing and editing. Shazia Khaliq being a supervisor was involved in conceptualization, administration of the project, provision of resources, writing, reviewing, and editing.
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Ashraf, N., Bechthold, A., Anwar, M.A. et al. Production of a broad spectrum streptothricin like antibiotic from halotolerant Streptomyces fimbriatus isolate G1 associated with marine sediments. Folia Microbiol 66, 639–649 (2021). https://doi.org/10.1007/s12223-021-00870-4
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DOI: https://doi.org/10.1007/s12223-021-00870-4