Marine Sediment-Derived Streptomyces Strain Produces Angucycline Antibiotics against Multidrug-Resistant Staphylococcus aureus Harboring SCCmec Type 1 Gene
Abstract
:1. Introduction
2. Materials and Methods
2.1. Collection of Marine Sediments
2.2. Culture-Dependent Isolation
2.3. Identification of Strain DSD011 by Phylogenetic Marker Genes Using Small Subunit rRNA (i.e., 16s rRNA) and Protein Coding Genes (atpD, recA, rpoB, and trpB) Sequence Analyses
2.4. PCR-Based Screening for Secondary Metabolite Biosynthetic Genes
2.5. Phenotypic Characterization
2.5.1. Salt Tolerance
2.5.2. Carbon Utilization Test
2.5.3. Scanning Electron Microscopy
2.6. Cultivation and Extraction of Biomass
2.7. Antibacterial Assay
2.7.1. Multidrug-Resistant Staphylococcus aureus (MRSA)
2.7.2. Disk Diffusion Assay of the Crude Extract
2.7.3. Antibacterial Activity by Microbroth Susceptibility Assay
2.7.4. Minimum Inhibitory Concentration
2.8. Targeted Chromatographic Isolation
2.8.1. Gel Filtration Chromatography
2.8.2. Flash Column Chromatography
2.8.3. High-Performance Liquid Chromatography (HPLC)
2.9. LCMS, MS/MS and Global Natural Product Social Molecular Networking (GNPS)
3. Results and Discussion
3.1. Isolation and Phenotypic Characterization of Actinomycete Strain DSD011
3.2. Genomic Characterization and Phylogenetic Analysis of Antibiotic Producing Actinomycete Strain DSD011
3.3. Screening for Polyketide Synthase (PKS) and Non-Ribosomal Peptide Synthetase (NRPS) Secondary Metabolite Biosynthetic Genes
3.4. Isolation and Identification of Antibiotic Compounds 1 and 2
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Singh, S.; Thumar, J.; Gohel, S.; Kikani, B.; Shukla, R.; Sharma, A.; Dangar, K. Actinomycetes from marine habitats and their enzymatic potential. Mar. Enzym. Biocatal. Sources Biocatal. Charact. Bioprocesses Mar. Enzym. 2013, 191–214. [Google Scholar] [CrossRef]
- Tamelander, T.; Spilling, K.; Winder, M. Organic matter export to the seafloor in the Baltic Sea: Drivers of change and future projections. Ambio 2017, 46, 842–851. [Google Scholar] [CrossRef]
- Whitman, W.B.; Coleman, D.C.; Wiebe, W.J. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 1998, 95, 6578–6583. [Google Scholar] [CrossRef] [Green Version]
- Morono, Y.; Ito, M.; Hoshino, T.; Terada, T.; Hori, T.; Ikehara, M.; D’Hondt, S.; Inagaki, F. Aerobic microbial life persists in oxic marine sediment as old as 101.5 million years. Nat. Commun. 2020, 11, 3626. [Google Scholar] [CrossRef]
- Bar-On, Y.M.; Phillips, R.; Milo, R. The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 2018, 115, 6506–6511. [Google Scholar] [CrossRef] [Green Version]
- Kallmeyer, J.; Pockalny, R.; Adhikari, R.R.; Smith, D.C.; D’Hondt, S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc. Natl. Acad. Sci. USA 2012, 109, 16213–16216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jose, P.A.; Jha, B. Intertidal marine sediment harbours actinobacteria with promising bioactive and biosynthetic potential. Sci. Rep. 2017, 7, 10041. [Google Scholar] [CrossRef] [PubMed]
- Jensen, P.R.; Dwight, R.; Fenical, W. Distribution of actinomycetes in near-shore tropical marine sediments. Appl. Environ. Microbiol. 1991, 57, 1102–1108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peng, A.; Qu, X.; Liu, F.; Li, X.; Li, E.; Xie, W. Angucycline glycosides from an intertidal sediments strain streptomyces sp. and their cytotoxic activity against hepatoma carcinoma cells. Mar. Drugs 2018, 16, 470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prieto-Davó, A.; Villarreal-Gómez, L.J.; Forschner-Dancause, S.; Bull, A.T.; Stach, J.E.; Smith, D.C.; Rowley, D.C.; Jensen, P.R. Targeted search for actinomycetes from nearshore and deep-sea marine sediments. FEMS Microbiol. Ecol. 2013, 84, 510–518. [Google Scholar] [CrossRef]
- Wagner, M.; Abdel-Mageed, W.M.; Ebel, R.; Bull, A.T.; Goodfellow, M.; Fiedler, H.P.; Jaspars, M. Dermacozines H-J isolated from a deep-sea strain of Dermacoccus abyssi from Mariana Trench sediments. J. Nat. Prod. 2014, 77, 416–420. [Google Scholar] [CrossRef] [PubMed]
- Meena, B.; Anburajan, L.; Vinithkumar, N.V.; Kirubagaran, R.; Dharani, G. Biodiversity and antibacterial potential of cultivable halophilic actinobacteria from the deep sea sediments of active volcanic Barren Island. Microb. Pathog. 2019, 132, 129–136. [Google Scholar] [CrossRef] [PubMed]
- Stach, J.E.; Maldonado, L.A.; Masson, D.G.; Ward, A.C.; Goodfellow, M.; Bull, A.T. Statistical approaches for estimating actinobacterial diversity in marine sediments. Appl. Environ. Microbiol. 2003, 69, 6189–6200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barka, E.A.; Vatsa, P.; Sanchez, L.; Gaveau-Vaillant, N.; Jacquard, C.; Meier-Kolthoff, J.P.; Klenk, H.P.; Clément, C.; Ouhdouch, Y.; van Wezel, G.P. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 2016, 80, 1–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mayfield, C.I.; Williams, S.T.; Ruddick, S.M.; Hatfield, H.L. Studies on the ecology of actinomycetes in soil IV. Observations on the form and growth of Streptomycetes in soil. Soil Biol. Biochem. 1972, 4, 79–91. [Google Scholar] [CrossRef]
- Cross, T. Aquatic actinomycetes: A critical survey of the occurrence, growth and role of actinomycetes in aquatic habitats. J. Appl. Bacteriol. 1981, 50, 397–423. [Google Scholar] [CrossRef] [PubMed]
- Soliev, A.B.; Hosokawa, K.; Enomoto, K. Bioactive pigments from marine bacteria: Applications and physiological roles. Evid. Based Complement. Alternat. Med. 2011, 2011, 670349. [Google Scholar] [CrossRef] [PubMed]
- Hassan, S.S.U.; Shaikh, A.L. Marine actinobacteria as a drug treasure house. Biomed. Pharmacother. 2017, 87, 46–57. [Google Scholar] [CrossRef]
- Dalisay, D.S.; Williams, D.E.; Wang, X.L.; Centko, R.; Chen, J.; Andersen, R.J. Marine sediment-derived Streptomyces bacteria from British Columbia, Canada are a promising microbiota resource for the discovery of antimicrobial natural products. PLoS ONE 2013, 8, e77078. [Google Scholar] [CrossRef]
- Valli, S.; Suvathi, S.S.; Aysha, O.S.; Nirmala, P.; Vinoth, K.P.; Reena, A. Antimicrobial potential of Actinomycetes species isolated from marine environment. Asian Pac. J. Trop. Biomed. 2012, 2, 469–473. [Google Scholar] [CrossRef] [Green Version]
- Manivasagan, P.; Kang, K.H.; Sivakumar, K.; Li-Chan, E.C.; Oh, H.M.; Kim, S.K. Marine actinobacteria: An important source of bioactive natural products. Environ. Toxicol. Pharmacol. 2014, 38, 172–188. [Google Scholar] [CrossRef] [PubMed]
- Claverías, F.P.; Undabarrena, A.; González, M.; Seeger, M.; Cámara, B. Culturable diversity and antimicrobial activity of Actinobacteria from marine sediments in Valparaíso bay, Chile. Front. Microbiol. 2015, 6, 737. [Google Scholar] [CrossRef] [PubMed]
- Velasco-Alzate, K.Y.; Bauermeister, A.; Tangerina, M.M.P.; Lotufo, T.M.C.; Ferreira, M.J.P.; Jimenez, P.C.; Padilla, G.; Lopes, N.P.; Costa-Lotufo, L.V. Marine bacteria from Rocas Atoll as a rich source of pharmacologically active compounds. Mar. Drugs 2019, 17, 671. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paderog, M.J.V.; Suarez, A.F.L.; Sabido, E.M.; Low, Z.J.; Saludes, J.P.; Dalisay, D.S. Anthracycline shunt metabolites from Philippine marine sediment-derived Streptomyces destroy cell membrane integrity of multidrug-resistant Staphylococcus aureus. Front. Microbiol. 2020, 11, 743. [Google Scholar] [CrossRef] [Green Version]
- Stincone, P.; Brandelli, A. Marine bacteria as source of antimicrobial compounds. Crit. Rev. Biotechnol. 2020, 40, 306–319. [Google Scholar] [CrossRef]
- Ibrahimi, M.; Korichi, W.; Hafidi, M.; Lemee, L.; Ouhdouch, Y.; Loqman, S. Marine Actinobacteria: Screening for predation leads to the discovery of potential new drugs against multidrug-resistant bacteria. Antibiotics 2020, 9, 91. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.C.; Cullum, R.; Hebishy, A.M.S.; Mohamed, H.A.; Faraag, A.H.I.; Salah, N.M.; Abdelfattah, M.S.; Fenical, W. Mersaquinone, a new tetracene derivative from the marine-derived Streptomyces sp. EG1 exhibiting activity against methicillin-resistant Staphylococcus aureus (MRSA). Antibiotics 2020, 9, 252. [Google Scholar] [CrossRef]
- Elmallah, M.I.Y.; Cogo, S.; Constantinescu, A.A.; Elifio-Esposito, S.; Abdelfattah, M.S.; Micheau, O. Marine Actinomycetes-derived secondary metabolites overcome trail-resistance via the intrinsic pathway through downregulation of survivin and XIAP. Cells 2020, 9, 1760. [Google Scholar] [CrossRef]
- Williams, D.E.; Dalisay, D.S.; Chen, J.; Polishchuck, E.A.; Patrick, B.O.; Narula, G.; Ko, M.; Av-Gay, Y.; Li, H.; Magarvey, N.; et al. Aminorifamycins and sporalactams produced in culture by a micromonospora sp. isolated from a northeastern-pacific marine sediment are potent antibiotics. Org. Lett. 2017, 19, 766–769. [Google Scholar] [CrossRef]
- Liang, L.; Haltli, B.A.; Kerr, R.G. Draft genome sequence of Streptomyces sp. strain Rknd-216, an antibiotic producer isolated from marine sediment in Prince Edward Island, Canada. Microbiol. Resour. Announc. 2019, 8, e00870–e00919. [Google Scholar] [CrossRef] [Green Version]
- Sproule, A.; Correa, H.; Decken, A.; Haltli, B.; Berrué, F.; Overy, D.P.; Kerr, R.G. Terrosamycins A and B, bioactive polyether ionophores from Streptomyces sp. RKND004 from Prince Edward Island sediment. Mar. Drugs 2019, 17, 347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Han, Y.; Wang, Y.; Yang, Y.; Chen, H. Shellmycin A-D, Novel Bioactive Tetrahydroanthra-γ-pyrone antibiotics from marine Streptomyces sp. Shell-016. Mar. Drugs 2020, 18, 58. [Google Scholar] [CrossRef] [Green Version]
- Zhou, W.; Fang, H.; Wu, Q.; Wang, X.; Liu, R.; Li, F.; Xiao, J.; Yuan, L.; Zhou, Z.; Ma, J.; et al. Ilamycin E, a natural product of marine actinomycete, inhibits triple-negative breast cancer partially through ER stress-CHOP-Bcl-2. Int. J. Biol. Sci. 2019, 15, 1723–1732. [Google Scholar] [CrossRef]
- Feling, R.H.; Buchanan, G.O.; Mincer, T.J.; Kauffman, C.A.; Jensen, P.R.; Fenical, W. Salinosporamide A: A highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora. Angew. Chem. Int. Ed. 2003, 4, 355–357. [Google Scholar] [CrossRef] [PubMed]
- Raninga, P.V.; Lee, A.; Sinha, D.; Dong, L.F.; Datta, K.K.; Lu, X.; Kalita-de Croft, P.; Dutt, M.; Hill, M.; Pouliot, N.; et al. Marizomib suppresses triple-negative breast cancer via proteasome and oxidative phosphorylation inhibition. Theranostics 2020, 10, 5259–5275. [Google Scholar] [CrossRef]
- Harrison, S.J.; Mainwaring, P.; Price, T.; Millward, M.J.; Padrik, P.; Underhill, C.R.; Cannell, P.K.; Reich, S.D.; Trikha, M.; Spencer, A. Phase I clinical trial of Marizomib (npi-0052) in patients with advanced malignancies including multiple myeloma: Study NPI-0052-102 Final Results. Clin. Cancer Res. 2016, 22, 4559–4566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kashfi, R.; Kelsey, C.; Gang, D.J.; Call, D.R.; Gang, D.R. Metabolomic diversity and identification of antibacterial activities of bacteria isolated from marine sediments in Hawai’i and Puerto Rico. Front. Mol. Biosci. 2020, 7, 23. [Google Scholar] [CrossRef] [PubMed]
- Gozari, M.; Zaheri, A.; Jahromi, S.T.; Karimzadeh, R. Screening and characterization of marine actinomycetes from the northern Oman Sea sediments for cytotoxic and antimicrobial activity. Int. Microbiol. 2019, 22, 521–530. [Google Scholar] [CrossRef]
- Parera-Valadez, Y.; Yam-Puc, A.; López-Aguiar, L.K.; Borges-Argáez, R.; Figueroa-Saldivar, M.A.; Cáceres-Farfán, M.; Márquez-Velázquez, N.A.; Prieto-Davó, A. Ecological strategies behind the selection of cultivable Actinomycete strains from the Yucatan Peninsula for the discovery of secondary metabolites with antibiotic activity. Microb. Ecol. 2019, 77, 839–851. [Google Scholar] [CrossRef] [PubMed]
- Quintero, M.; Velásquez, A.; Jutinico, L.M.; Jiménez-Vergara, E.; Blandón, L.M.; Martinez, K.; Lee, H.S.; Gómez-León, J. Bioprospecting from marine coastal sediments of Colombian Caribbean: Screening and study of antimicrobial activity. J. Appl. Microbiol. 2018, 125, 753–765. [Google Scholar] [CrossRef] [PubMed]
- Yang, N.; Song, F. Bioprospecting of novel and bioactive compounds from marine actinomycetes isolated from South China Sea sediments. Curr. Microbiol. 2018, 75, 142–149. [Google Scholar] [CrossRef] [PubMed]
- Prieto-Davó, A.; Dias, T.; Gomes, S.E.; Rodrigues, S.; Parera-Valadez, Y.; Borralho, P.M.; Pereira, F.; Rodrigues, C.M.; Santos-Sanches, I.; Gaudêncio, S.P. The Madeira Archipelago as a significant source of marine-derived Actinomycete diversity with anticancer and antimicrobial potential. Front. Microbiol. 2016, 7, 1594. [Google Scholar] [CrossRef] [PubMed]
- Tangerina, M.M.; Correa, H.; Haltli, B.; Vilegas, W.; Kerr, R.G. Bioprospecting from cultivable bacterial communities of marine sediment and invertebrates from the underexplored Ubatuba region of Brazil. Arch. Microbiol. 2017, 199, 155–169. [Google Scholar] [CrossRef] [Green Version]
- Undabarrena, A.; Beltrametti, F.; Claverías, F.P.; González, M.; Moore, E.R.; Seeger, M.; Cámara, B. Exploring the diversity and antimicrobial potential of marine actinobacteria from the Comau Fjord in Northern Patagonia, Chile. Front. Microbiol. 2016, 7, 1135. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Yang, J.; Yu, J.; Li, J.; Yuan, J.; Wong, N.K.; Ju, J. Chlorinated bis-indole alkaloids from deep-sea derived Streptomyces sp. SCSIO 11791 with antibacterial and cytotoxic activities. J. Antibiot. 2020, 73, 542–547. [Google Scholar] [CrossRef]
- Mincer, T.J.; Jensen, P.R.; Kauffman, C.A.; Fenical, W. Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl. Environ. Microbiol. 2002, 68, 5005–5011. [Google Scholar] [CrossRef] [Green Version]
- Johnson, M.; Zaretskaya, I.; Raytselis, Y.; Merezhuk, Y.; McGinnis, S.; Madden, T.L. NCBI BLAST: A better web interface. Nucleic. Acids. Res. 2008, 36, W5–W9. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
- Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16, 111–120. [Google Scholar] [CrossRef]
- Guo, Y.; Zheng, W.; Rong, X.; Huang, Y. A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: Use of multilocus sequence analysis for Streptomycete systematics. Int. J. Syst. Evol. Microbiol. 2008, 58, 149–159. [Google Scholar] [CrossRef]
- Ginolhac, A.; Jarrin, C.; Robe, P.; Perrière, G.; Vogel, T.M.; Simonet, P.; Nalin, R. Type I polyketide synthases may have evolved through horizontal gene transfer. J. Mol. Evol. 2005, 60, 716–725. [Google Scholar] [CrossRef] [PubMed]
- Izumikawa, M.; Murata, M.; Tachibana, K.; Ebizuka, Y.; Fujii, I. Cloning of modular type I polyketide synthase genes from salinomycin producing strain of Streptomyces albus. Bioorg. Med. Chem. 2003, 11, 3401–3405. [Google Scholar] [CrossRef]
- Al-Amoudi, S.; Essack, M.; Simões, M.F.; Bougouffa, S.; Soloviev, I.; Archer, J.A.; Lafi, F.F.; Bajic, V.B. Bioprospecting Red Sea coastal ecosystems for culturable microorganisms and their antimicrobial potential. Mar. Drugs 2016, 14, 165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zothanpuia; Passari, A.K.; Gupta, V.K.; Singh, B.P. Detection of antibiotic-resistant bacteria endowed with antimicrobial activity from a freshwater lake and their phylogenetic affiliation. PeerJ 2016, 4, e2103. [Google Scholar] [CrossRef] [PubMed]
- Wawrik, B.; Kerkhof, L.; Zylstra, G.J.; Kukor, J.J. Identification of unique type II polyketide synthase genes in soil. Appl. Environ. Microbiol. 2005, 71, 2232–2238. [Google Scholar] [CrossRef] [Green Version]
- Ayuso-Sacido, A.; Genilloud, O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: Detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb. Ecol. 2005, 49, 10–24. [Google Scholar] [CrossRef]
- Mathew, B.T.; Torky, Y.; Amin, A.; Mourad, A.I.; Ayyash, M.M.; El-Keblawy, A.; Hilal-Alnaqbi, A.; AbuQamar, S.F.; El-Tarabily, K.A. Halotolerant marine rhizosphere-competent Actinobacteria promote Salicornia bigelovii growth and seed production using seawater irrigation. Front. Microbiol. 2020, 11, 552. [Google Scholar] [CrossRef]
- Kavitha, A.; Savithri, H.S. Biological significance of marine actinobacteria of east coast of Andhra Pradesh, India. Front. Microbiol. 2017, 8, 1201. [Google Scholar] [CrossRef] [Green Version]
- Staphylococcus Aureus Subsp. Aureus (ATCC® BAA-44™). Available online: https://atcc.org/Products/All/BAA-44.aspx#documentation (accessed on 15 August 2020).
- Andrews, J.M. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 2001, 48, 5–16. [Google Scholar] [CrossRef] [Green Version]
- Wang, M.; Carver, J.J.; Phelan, V.V.; Sanchez, L.M.; Garg, N.; Peng, Y. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat. Biotechnol. 2016, 34, 828–837. [Google Scholar] [CrossRef] [Green Version]
- Kemung, H.M.; Tan, L.T.; Khan, T.M.; Chan, K.G.; Pusparajah, P.; Goh, B.H.; Lee, L.H. Streptomyces as a prominent resource of future anti-MRSA drugs. Front. Microbiol. 2018, 9, 2221. [Google Scholar] [CrossRef] [PubMed]
- Saitou, N.; Nei, M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4, 406–425. [Google Scholar] [PubMed]
- Rong, X.; Huang, Y. Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst. Appl. Microbiol. 2012, 35, 7–18. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Han, L.; Yu, M.; Cao, P.; Li, D.; Guo, X.; Liu, Y.; Wang, X.; Xiang, W. Characterization of Streptomyces sporangiiformans sp. nov., a novel soil Actinomycete with antibacterial activity against Ralstonia solanacearum. Microorganisms 2019, 7, 360. [Google Scholar] [CrossRef] [Green Version]
- Huang, X.; Kong, F.; Zhou, S.; Huang, D.; Zheng, J.; Zhu, W. Streptomyces tirandamycinicus sp. nov., a novel marine sponge-derived Actinobacterium with antibacterial potential against Streptococcus agalactiae. Front. Microbiol. 2019, 10, 482. [Google Scholar] [CrossRef] [Green Version]
- Labeda, D.P. Multilocus sequence analysis of phytopathogenic species of the genus Streptomyces. Int. J. Syst. Evol. Microbiol. 2011, 61, 2525–2531. [Google Scholar] [CrossRef] [Green Version]
- Johnson, J.S.; Spakowicz, D.J.; Hong, B.Y.; Petersen, L.M.; Demkowicz, P.; Chen, L.; Leopold, S.R.; Hanson, B.M.; Agresta, H.O.; Gerstein, M.; et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat. Commun. 2019, 10, 5029. [Google Scholar] [CrossRef] [Green Version]
- Cornell, C.R.; Marasini, D.; Fakhr, M.K. Draft genome sequences of megaplasmid-bearing Streptomyces sp. strains BF-3 and 4F, isolated from the Great Salt Plains of Oklahoma. Genome Announc. 2018, 14, e00208–e00218. [Google Scholar] [CrossRef] [Green Version]
- Hertweck, C.; Luzhetskyy, A.; Rebets, Y.; Bechthold, A. Type II polyketide synthases: Gaining a deeper insight into enzymatic teamwork. Nat. Prod. Rep. 2007, 24, 162–190. [Google Scholar] [CrossRef]
- Katz, L.; Baltz, R.H. Natural product discovery: Past, present, and future. J. Ind. Microbiol. Biotechnol. 2016, 43, 155–176. [Google Scholar] [CrossRef]
- Rohr, J.; Thiericke, R. Angucycline group antibiotics. Nat. Prod. Rep. 1992, 9, 103–137. [Google Scholar] [CrossRef] [PubMed]
- Kharel, M.K.; Pahari, P.; Shepherd, M.D.; Tibrewal, N.; Nybo, S.E.; Shaaban, K.A.; Rohr, J. Angucyclines: Biosynthesis, mode-of-action, new natural products, and synthesis. Nat. Prod. Rep. 2012, 29, 264–325. [Google Scholar] [CrossRef] [PubMed]
- Hu, Z.; Qin, L.; Wang, Q.; Ding, W.; Chen, Z.; Ma, Z. Angucycline antibiotics and its derivatives from marine-derived actinomycete Streptomyces sp. A6H. Nat. Prod. Res. 2016, 30, 2551–2558. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Duan, Y.; Cui, Z.; Wang, Z.; Li, Z.; Zhang, Y.; Ju, J.; Huang, H. Cytotoxic rearranged angucycline glycosides from deep sea-derived Streptomyces lusitanus SCSIO LR32. J. Antibiot. 2017, 70, 819–822. [Google Scholar] [CrossRef] [PubMed]
- Qu, X.Y.; Ren, J.W.; Peng, A.H.; Lin, S.Q.; Lu, D.D.; Du, Q.Q.; Liu, L.; Li, X.; Li, E.W.; Xie, W.D. Cytotoxic, anti-migration, and anti-invasion activities on breast cancer cells of angucycline glycosides isolated from a marine-derived Streptomyces sp. Mar. Drugs 2019, 17, 277. [Google Scholar] [CrossRef] [Green Version]
- Huang, H.; Yang, T.; Ren, X.; Liu, J.; Song, Y.; Sun, A.; Ma, J.; Wang, B.; Zhang, Y.; Huang, C.; et al. Cytotoxic angucycline class glycosides from the deep sea actinomycete Streptomyces lusitanus SCSIO LR32. J. Nat. Prod. 2012, 75, 202–208. [Google Scholar] [CrossRef]
Strain | Starch (1.0%) | Mannitol (0.05%) | Glucose (0.05%) | Trehalose (0.05%) | Raffinose (0.05%) |
---|---|---|---|---|---|
DSD011 | +++ | ++ | +++ | ++ | ++ |
Strain | 0 | 3 | 5 | 7 | 10 | 12 | 15 | 20 |
---|---|---|---|---|---|---|---|---|
DSD011 | +++ | +++ | +++ | ++ | - | - | - | - |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Sabido, E.M.; Tenebro, C.P.; Suarez, A.F.L.; Ong, S.D.C.; Trono, D.J.V.L.; Amago, D.S.; Evangelista, J.E., Jr.; Reynoso, A.M.Q.; Villalobos, I.G.M.; Alit, L.D.D.; et al. Marine Sediment-Derived Streptomyces Strain Produces Angucycline Antibiotics against Multidrug-Resistant Staphylococcus aureus Harboring SCCmec Type 1 Gene. J. Mar. Sci. Eng. 2020, 8, 734. https://doi.org/10.3390/jmse8100734
Sabido EM, Tenebro CP, Suarez AFL, Ong SDC, Trono DJVL, Amago DS, Evangelista JE Jr., Reynoso AMQ, Villalobos IGM, Alit LDD, et al. Marine Sediment-Derived Streptomyces Strain Produces Angucycline Antibiotics against Multidrug-Resistant Staphylococcus aureus Harboring SCCmec Type 1 Gene. Journal of Marine Science and Engineering. 2020; 8(10):734. https://doi.org/10.3390/jmse8100734
Chicago/Turabian StyleSabido, Edna M., Chuckcris P. Tenebro, Angelica Faith L. Suarez, Sarah Diane C. Ong, Dana Joanne Von L. Trono, Diana S. Amago, Jose E. Evangelista, Jr., Ann Marielle Q. Reynoso, Ivy Grace M. Villalobos, Luigi Dan D. Alit, and et al. 2020. "Marine Sediment-Derived Streptomyces Strain Produces Angucycline Antibiotics against Multidrug-Resistant Staphylococcus aureus Harboring SCCmec Type 1 Gene" Journal of Marine Science and Engineering 8, no. 10: 734. https://doi.org/10.3390/jmse8100734
APA StyleSabido, E. M., Tenebro, C. P., Suarez, A. F. L., Ong, S. D. C., Trono, D. J. V. L., Amago, D. S., Evangelista, J. E., Jr., Reynoso, A. M. Q., Villalobos, I. G. M., Alit, L. D. D., Surigao, C. F., Villanueva, C. A., Saludes, J. P., & Dalisay, D. S. (2020). Marine Sediment-Derived Streptomyces Strain Produces Angucycline Antibiotics against Multidrug-Resistant Staphylococcus aureus Harboring SCCmec Type 1 Gene. Journal of Marine Science and Engineering, 8(10), 734. https://doi.org/10.3390/jmse8100734