Echinosporin antibiotics isolated from Amycolatopsis strain and their antifungal activity against root-rot pathogens of the Panax notoginseng
Actinomycete strain YIM PH20520, isolated from the rhizosphere soil sample of Panax notoginseng collected in Wenshang, Yunnan Province, China, exhibited antifungal activity against root-rot pathogens of the Panax notoginseng. The structures of bioactive molecules, isolated from the ethyl acetate extract of the fermentation broth of the strain, were identified as echinosporin (1) and 7-deoxyechinosporin (2) based on extensive spectroscopic analyses. 1 exhibited antifungal activity against four tested root-rot pathogens of Panax notoginseng include Fusarium oxysporum, Fusarium solani, Alternaria panax, and Phoma herbarum with the MIC value at 64, 64, 32, and 64 μg/mL, respectively. 2 exhibited antifungal activities against F. oxysporum, F. solani, A. panax, and P. herbarum with the MIC value at 128, 128, 64, and 128 μg/mL, respectively. Based on the phylogenetic analyses, the closest phylogenetic relative of strain YIM PH20520 is Amycolatopsis speibonae JS72T (97.69%), so strain YIM PH20520 was identified as Amycolatopsis strain. To the best of our knowledge, this is the first report of echinosporin antibiotics isolated from Amycolatopsis strain besides Streptomyces strain and their antifungal activity against four tested root-rot pathogens of the Panax notoginseng. The results provide a reliable evidence for the following related biosynthetic investigations on Amycolatopsis strain YIM PH20520 due to echinosporins antibiotics’ unique tricyclic acetal-lactone structures.
This work was supported by the National Natural Science Foundation of China (Grant No. 31660532, 21562045, 31660004).
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Conflict of interest
The authors declare that they have no competing interests.
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Informed consent was obtained from all individual participants included in the study.
- Bala S, Khanna R, Dadhwal M, Prabagaran SR, Shivaji S, Cullum J, Lal R (2004) Reclassification of Amycolatopsis mediterranei DSM 46095 as Amycolatopsis rifamycinica sp. nov. Int J Syst Evol Microbiol 54:1145–1149Google Scholar
- Berdy J (2005) Bioactive microbial metabolites. J Antibiot 58:1–26Google Scholar
- Cui CB, Liu HB, Gu JY, Gu QQ, Cai B, Zhang DY, Zhu TJ (2007) Echinosporins as new cell cycle inhibitors and apoptosis inducers from marine-derived Streptomyces albogriseolus. Fitoterapia 78:238–240Google Scholar
- Dübeler A, Krastel P, Floss HG, Zeeck A (2002) Biosynthesis of the antibiotic echinosporin by a novel branch of the shikimate pathway. Eur J Org Chem 2002:983–987Google Scholar
- Everest GJ, Meyers PR (2011) Evaluation of the antibiotic biosynthetic potential of the genus Amycolatopsis and description of Amycolatopsis circi sp. nov., Amycolatopsis equina sp. nov. and Amycolatopsis hippodromi sp. Nov. J Appl Microbiol 111:300–311Google Scholar
- Everest GJ, le Roes-Hill M, Rohland J, Enslin S, Meyers PR (2014) Amycolatopsis roodepoortensis sp. nov. and Amycolatopsis speibonae sp. nov.: antibiotic-producing actinobacteria isolated from South African soils. J Antibiot 67:813–818Google Scholar
- Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376Google Scholar
- Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
- Flasz JT, Hale KJ (2012) A new stereocontrolled synthetic route to (-)-echinosporin from D-glucose via padwa allenylsulfone [3+2]-anionic cycloadditive elimination. Org Lett 14(12):3024–3027Google Scholar
- Hashizume H, Adachi H, Igarashi M, Nishimura Y, Akamatsu Y (2010) Biological activities of pargamicin A, a novel cyclic peptide antibiotic from Amycolatopsis sp. J Antibiot 63:279–283Google Scholar
- Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721Google Scholar
- Kinsella MA, Kalish VJ, Weinreb SM (1990) Approaches to the total synthesis of the antitumor antibiotic echinosporin. J Org Chem 55(1):105–111Google Scholar
- Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Biol 18:1–32Google Scholar
- Lazzarini A, Cavaletti L, Toppo G, Marinelli F (2000) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 78:399–405Google Scholar
- Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428Google Scholar
- Li YQ (2007) Research on anti-Botrytis elliptica of Lilium longiflorum components from the secondary metabolites of two actinomycetes. Yunnan University, Master ThesisGoogle Scholar
- Li YQ, Han L, Rong H, Li LY, Zhao LX, Wu LX, Xu LH, Jiang Y, Huang XS (2015) Diastaphenazine, a new dimeric phenazine from an endophytic Streptomyces diastaticus subsp. Ardesiacus. J Antibiot 68(3):210–212Google Scholar
- Mahalaxmi Y, Sathish T, Prakasham RS (2009) Development of balanced medium composition for improved rifamycin B production by isolated Amycolatopsis sp. RSP-3. Lett Appl Microbiol 49(5):533–538Google Scholar
- McCormick MH, McGuire JM, Pittenger GE, Pittenger RC, Stark WM (1955-1956) Vancomycin, a new antibiotic. I. Chemical and biologic properties. Antibiot Annu 3:606–611Google Scholar
- Morimoto M, Imai R (1985) Antitumor activity of echinosporin. J Antibiot 38(4):490–495Google Scholar
- Penkhrue W, Sujarit K, Kudo T, Ohkuma M, Masaki K, Aizawa T, Pathom-Aree W, Khanongnuch C, Lumyong S (2018) Amycolatopsis oliviviridis sp. nov., a novel polylactic acid-bioplastic-degrading actinomycete isolated from paddy soil. Int J Syst Evol Microbiol 68(5):1448–1454Google Scholar
- Saito A, Ooya T, Miyatsuchi D, Fuchigami H, Terakado K, Nakayama SY, Watanabe T, Nagata Y, Ando A (2009) Molecular characterization and antifungal activity of a family 46 chitosanase from Amycolatopsis sp. CsO-2. FEMS Microbiol Lett 293:79–84Google Scholar
- Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
- Sato T, Kawamoto I, Oka T, Okachi R (1982) A new antibiotic echinosporin (XK-213)-producing organism, isolation and characterization. J Antibiot 35(3):266–271Google Scholar
- Sensi P, Greco AM, Ballotta R (1959-1960) Rifomycin. I. Isolation and properties of rifomycin B and rifomycin complex. Antibiot Annu 7:262–270Google Scholar
- Sheng Y, Fotso S, Serrill JD, Shahab S, Santosa DA, Ishmael JE, Proteau PJ, Zabriskie TM, Mahmud T (2015) Succinylated apoptolidins from Amycolatopsis sp. ICBB 8242. Org Lett 17(10):2526–2529Google Scholar
- Smith AB III, Sulikowski GA, Fujimoto K (1989) Total synthesis of natural (-)-echinosporin. Determination of the absolute configuration. J Am Chem Soc 111:8039–8041Google Scholar
- Solecka J, Zajko J, Postek M, Rajnisz A (2012) Biologically active secondary metabolites from actinomycetes. Open Life Sci 7(3):373–390Google Scholar
- Stackebrandt E, Rainey FA, Ward-Rainey NL (1997) Proposal for a new hierarchic classification system, actinobacteria classis nov. Int J Syst Bacteriol 47:479–491Google Scholar
- 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. Mol Biol Evol 28:2731–2739Google Scholar
- Tan GY, Robinson S, Lacey E, Brown R, Kim W, Goodfellow M (2007) Amycolatopsis regifaucium sp. nov., a novel actinomycete that produces kigamicins. Int J Syst Evol Microbiol 57:2562–2567Google Scholar
- Tian SZ, Pu X, Luo GY, Zhao LX, Xu LH, Li WJ, Luo YG (2013) Isolation and characterization of new p-terphenyls with antifungal, antibacterial, and antioxidant activities from halophilic actinomycete Nocardiopsis gilva YIM 90087. J Agric Food Chem 61:3006–3012Google Scholar
- Zhang CW, Herath K, Jayasuriya H, Ondeyka JG, Zink DL, Occi J, Birdsall G, Venugopal J, Ushio M, Burgess B, Masurekar P, Barrett JF, Singh SB (2009) Thiazomycins, thiazolyl peptide antibiotics from Amycolatopsis fastidiosa. J Nat Prod 72(5):841–847Google Scholar