Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities

doi:10.1007/s13659-024-00481-9

Natural Products and Bioprospecting ›› 2024, Vol. 14 ›› Issue (6): 61-61.DOI: 10.1007/s13659-024-00481-9

• ORIGINAL ARTICLES • Previous Articles

Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities

Lu Cao¹, Jun-Feng Tan¹, Zeng-Guang Zhang¹, Jun-Wei Yang¹, Yu Mu¹, Zhi-Long Zhao², Yi Jiang³, Xue-Shi Huang¹, Li Han¹

1. Institute of Microbial Pharmaceuticals, College of Life and Health Sciences, Northeastern University, Shenyang 110819, China;
2. Pharmacological Laboratory, Liaoning Provincial Institute of Drug Inspection and Testing, Shenyang 110036, China;
3. Yunnan Institute of Microbiology, Yunnan University, Kunming 650091, China

Received:2024-09-02 Online:2024-12-13 Published:2024-12-24
Contact: Yi Jiang,E-mail:jiangyi@ynu.edu.cn;Xue-Shi Huang,E-mail:huangxs@mail.neu.edu.cn;Li Han,E-mail:hanli@mail.neu.edu.cn
Supported by:
This work was supported by National Natural Science Foundation of China (Grant No. 32060001), the Fundamental Research Funds for the Central Universities, China (No. N2320001) and the Construction Project of Liaoning Provincial Key Laboratory, China (2022JH13/10200026).

Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities

Lu Cao¹, Jun-Feng Tan¹, Zeng-Guang Zhang¹, Jun-Wei Yang¹, Yu Mu¹, Zhi-Long Zhao², Yi Jiang³, Xue-Shi Huang¹, Li Han¹

1. Institute of Microbial Pharmaceuticals, College of Life and Health Sciences, Northeastern University, Shenyang 110819, China;
2. Pharmacological Laboratory, Liaoning Provincial Institute of Drug Inspection and Testing, Shenyang 110036, China;
3. Yunnan Institute of Microbiology, Yunnan University, Kunming 650091, China

通讯作者: Yi Jiang,E-mail:jiangyi@ynu.edu.cn;Xue-Shi Huang,E-mail:huangxs@mail.neu.edu.cn;Li Han,E-mail:hanli@mail.neu.edu.cn
基金资助:
This work was supported by National Natural Science Foundation of China (Grant No. 32060001), the Fundamental Research Funds for the Central Universities, China (No. N2320001) and the Construction Project of Liaoning Provincial Key Laboratory, China (2022JH13/10200026).

Abstract

Abstract: Thirty-six structurally diverse sesquiterpenoids, including caryolanes (1-12), germacranes (13-16), isodaucane (17), cadinanes (18-22), epicubenols (23, 24), oplopanane (25), pallenanes (26, 27), and eudesmanes (28-36), were isolated from the fermentation broth of Streptomyces fulvorobeus derived from Elephas maximus feces. Pallenane is a kind of rarely reported sesquiterpene with a distinctive C5/C3 bicyclic skeleton and was firstly found from microbial source. The structures of fifteen new compounds (1-4, 13-15, 17, 18, 22, 23, 25-28) were established through detailed spectroscopic data analysis, which included data from experimental and calculated ECD spectra as well as Mosher’s reagent derivative method. Compound 34 exhibited moderate antifungal activity against Cryptococcus neoformans and Cryptococcus gattii with MIC values of 50 μg/mL. It effectively inhibited biofilm formation and destroyed the preformed biofilm, as well as hindered the adhesion of Cryptococcus species. The current work would enrich the chemical diversity of sesquiterpenoid family.

Key words: Sesquiterpenoids, Streptomyces fulvorobeus, Fermentation, Antifungal activity

摘要： Thirty-six structurally diverse sesquiterpenoids, including caryolanes (1-12), germacranes (13-16), isodaucane (17), cadinanes (18-22), epicubenols (23, 24), oplopanane (25), pallenanes (26, 27), and eudesmanes (28-36), were isolated from the fermentation broth of Streptomyces fulvorobeus derived from Elephas maximus feces. Pallenane is a kind of rarely reported sesquiterpene with a distinctive C5/C3 bicyclic skeleton and was firstly found from microbial source. The structures of fifteen new compounds (1-4, 13-15, 17, 18, 22, 23, 25-28) were established through detailed spectroscopic data analysis, which included data from experimental and calculated ECD spectra as well as Mosher’s reagent derivative method. Compound 34 exhibited moderate antifungal activity against Cryptococcus neoformans and Cryptococcus gattii with MIC values of 50 μg/mL. It effectively inhibited biofilm formation and destroyed the preformed biofilm, as well as hindered the adhesion of Cryptococcus species. The current work would enrich the chemical diversity of sesquiterpenoid family.

关键词: Sesquiterpenoids, Streptomyces fulvorobeus, Fermentation, Antifungal activity

Lu Cao, Jun-Feng Tan, Zeng-Guang Zhang, Jun-Wei Yang, Yu Mu, Zhi-Long Zhao, Yi Jiang, Xue-Shi Huang, Li Han. Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities[J]. Natural Products and Bioprospecting, 2024, 14(6): 61-61.

References

[1] Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242-9.
[2] Bartolini I, Risaliti M, Ringressi MN, Melli F, Nannini G, Amedei A, Muiesan P, Taddei A. Role of gut microbiota-immunity axis in patients undergoing surgery for colorectal cancer: focus on short and long-term outcomes. World J Gastroenterol. 2020;26(20):2498-513.
[3] Ma J, Piao X, Mahfuz S, Long S, Wang J. The interaction among gut microbes, the intestinal barrier and short chain fatty acids. Anim Nutr. 2022;9:159-74.
[4] Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229-41.
[5] Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101(44):15718-23.
[6] Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut? Trends Microbiol. 2004;12(12):562-8.
[7] Wu C, Chen T, Xu W, Zhang T, Pei Y, Yang Y, Zhang F, Guo H, Wang Q, Wang L, Zhao B. The maintenance of microbial community in human fecal samples by a cost effective preservation buffer. Sci Rep. 2021;11(1):13453.
[8] Chen X, Li QY, Li GD, Xu FJ, Han L, Jiang Y, Huang XS, Jiang CL. The distal gut bacterial community of some primates and carnivora. Curr Microbiol. 2018;75(2):213-22.
[9] Ding N, Jiang Y, Han L, Chen X, Ma J, Qu X, Mu Y, Liu J, Li L, Jiang C, Huang X. Bafilomycins and odoriferous sesquiterpenoids from Streptomyces albolongus isolated from Elephas maximus feces. J Nat Prod. 2016;79(4):799-805.
[10] Ding N, Han L, Jiang Y, Li G, Liu J, Mu Y, Huang X. Sesquiterpenoids from Streptomyces anulatus isolated from Giraffa camelopardalis feces. Magn Reson Chem. 2018;56(5):352-9.
[11] Zhang J, Jiang Y, Cao Y, Liu J, Zheng D, Chen X, Han L, Jiang C, Huang X. Violapyrones A-G, α-pyrone derivatives from Streptomyces violascens isolated from Hylobates hoolock feces. J Nat Prod. 2013;76(11):2126-30.
[12] Ma J, Lei H, Chen X, Bi X, Jiang Y, Han L, Huang X. New anti-inflammatory metabolites produced by Streptomyces violaceoruber isolated from Equus burchelli feces. J Antibiot. 2017;70(10):991-4.
[13] Mu Y, Yu X, Zheng Z, Liu W, Li G, Liu J, Jiang Y, Han L, Huang X. New metabolites produced by Streptomyces badius isolated from Giraffa camelopardalis feces. Magn Reson Chem. 2019;57(12):1150-7.
[14] Zheng D, Han L, Qu X, Chen X, Zhong J, Bi X, Liu J, Jiang Y, Jiang C, Huang X. Cytotoxic fusicoccane-type diterpenoids from Streptomyces violascens isolated from Ailuropoda melanoleuca feces. J Nat Prod. 2017;80(4):837-44.
[15] Zheng D, Ding N, Jiang Y, Zhang J, Ma J, Chen X, Liu J, Han L, Huang X. Albaflavenoid, a new tricyclic sesquiterpenoid from Streptomyces violascens. J Antibiot. 2016;69(10):773-5.
[16] Dickschat JS. Bacterial terpene cyclases. Nat Prod Rep. 2016;33(1):87-110.
[17] Wu QX, Shi YP, Jia ZJ. Eudesmane sesquiterpenoids from the Asteraceae family. Nat Prod Rep. 2006;23(5):699-734.
[18] Rinkel J, Rabe P, Garbeva P, Dickschat JS. Lessons from 1,3-hydride shifts in sesquiterpene cyclizations. Angew Chem Int Ed Engl. 2016;55(43):13593-6.
[19] Ding L, Goerls H, Dornblut K, Lin W, Maier A, Fiebig HH, Hertweck C. Bacaryolanes A--C, rare bacterial caryolanes from a mangrove endophyte. J Nat Prod. 2015;78(12):2963-7.
[20] Chen S, Yang Q, Zhang X, Wang Z, Xu HM, Dong LB. Discovery of diverse sesquiterpenoids from Crossiella cryophila through genome mining and NMR tracking. J Nat Prod. 2024;87(2):195-206.
[21] Yamada Y, Kuzuyama T, Komatsu M, Shin-Ya K, Omura S, Cane DE, Ikeda H. Terpene synthases are widely distributed in bacteria. Proc Natl Acad Sci USA. 2015;112(3):857-62.
[22] Citron CA, Gleitzmann J, Laurenzano G, Pukall R, Dickschat JS. Terpenoids are widespread in actinomycetes: a correlation of secondary metabolism and genome data. ChemBioChem. 2012;13(2):202-14.
[23] Rudolf JD, Alsup TA, Xu B, Li Z. Bacterial terpenome. Nat Prod Rep. 2021;38(5):905-80.
[24] Tsuda M, Toriyabe Y, Endo T, Kobayashi J. Application of modified mosher’s method for primary alcohols with a methyl group at C2 position. Chem Pharm Bull. 2003;51(4):448-51.
[25] Nakano C, Horinouchi S, Ohnishi Y. Characterization of a novel sesquiterpene cyclase involved in (+)-caryolan-1-ol biosynthesis in Streptomyces griseus. J Biol Chem. 2011;286(32):27980-7.
[26] Guan S, Grabley S, Groth I, Lin W, Christner A, Guo D, Sattler I. Structure determination of germacrane-type sesquiterpene alcohols from an endophyte Streptomyces griseus subsp. Magn Reson Chem. 2005;43(12):1028-31.
[27] Kato R, Saito H, Ikeuchi K, Suzuki T, Tanino K. Total synthesis and structural revision of the 6,11-epoxyisodaucane natural sesquiterpene using an anionic 8π electrocyclic reaction. Org Lett. 2022;24(43):7939-43.
[28] Lu S, Hu J, Xie X, Huang R, He J. Sesquiterpenoids isolated from feces-residing Streptomyces sp. inhibit the cellular entry of influenza a viruses. Nat Prod Res. 2022;36(24):6286-96.
[29] Kuo YH, Chen CH, Chien SC, Lin YL. Five new cadinane-type sesquiterpenes from the heartwood of Chamaecyparis obtusa var. formosana. J Nat Prod. 2002;65(1):25-8.
[30] Zhang Y, Jiang K, Zhai YM, Tan JJ, Meng DL, Guo SL, Qu SJ, Tan CH. Sesquiterpenoids and their glycosides from Gynura procumbens. Helv Chim Acta. 2014;97(3):369-74.
[31] Yang JL, Zhao YM, Shi YP. Sesquiterpenoids from the rhizomes of Homalomena occulta. Nat Prod Bioprospect. 2016;6(4):211-6.
[32] Piers E, Gavai AV. A (Z)-ethylidenecyclopentane annulation method. Total syntheses of (±)-anhydrooplopanone, (±)-oplopanone, and (±)-8-epi-oplopanone. J Org Chem. 1990;55(8):2380-90.
[33] Ahmed AA, Jakupovic J, Bohlmann F. Dihydroxypallenone, a sesquiterpene with a new carbon skeletonerom pallenisspinosa. Phytochemistry. 1990;29(10):3355-8.
[34] Appendino G, Jakupovic J, Jakupovic S. Sesquiterpenoids from Pallenis spinosa. Phytochemistry. 1997;46(6):1039-43.
[35] Yang Z, Yang Y, Yang X, Zhang Y, Zhao L, Xu L, Ding Z. Sesquiterpenes from the secondary metabolites of Streptomyces sp. (YIM 56130). Chem Pharm Bull. 2011;59(11):1430-3.
[36] Heymann H, Tezuka Y, Kikuchi T, Supriyatna S. Constituents of Sindora sumatrana MIQ. I. Isolation and NMR spectral analysis of sesquiterpenes from the dried pods. Chem Pharm Bull. 1994;42(1):138-46.
[37] Chen QJ, Ouyang MA, Tan QW, Zhang ZK, Wu ZJ, Lin QY. Constituents from the seeds of Brucea javanica with inhibitory activity of Tobacco mosaic virus. J Asian Nat Prod Res. 2009;11(6):539-47.
[38] Ding L, Görls H, Hertweck C. Plant-like cadinane sesquiterpenes from an actinobacterial mangrove endophyte. Magn Reson Chem. 2021;59(1):34-42.
[39] Tan Z, Zhao J, Liu J, Zhang M, Chen R, Xie K, Dai J. Sesquiterpenoids from the cultured mycelia of Ganoderma capense. Fitoterapia. 2017;118:73-9.
[40] Nagashima F, Kishi K, Hamada Y, Takaoka S, Asakawa Y. ent-Verticillane-type diterpenoids from the Japanese liverwort Jackiella javanica. Phytochemistry. 2005;66(14):1662-70.
[41] Li X, Yang M, Han YF, Gao K. New sesquiterpenes from Erigeron annus. Planta Med. 2005;71(3):268-72.
[42] Wu S, Wang Y, Liu N, Dong G, Sheng C. Tackling fungal resistance by biofilm inhibitors. J Med Chem. 2017;60(6):2193-211.
[43] Forsyth CB, Mathews HL. Lymphocyte adhesion to Candida albicans. Infect Immun. 2002;70(2):517-27.
[44] Xu W, Tan J, Mu Y, Zheng D, Huang X, Li L. New antimicrobial terpenoids and phloroglucinol glucosides from Syzygium szemaoense. Bioorg Chem. 2020;103:104242.
[45] Tan J, Zhang Z, Zheng D, Mu Y, Cao B, Yang J, Han L, Huang X. Structure-activity relationship and biofilm formation-related gene targets of oleanolic acid-type saponins from Pulsatilla chinensis against Candida albicans. Bioorg Chem. 2024;146:107311.

Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities

Discovery of structurally diverse sesquiterpenoids from Streptomyces fulvorobeus isolated from Elephas maximus feces and their antifungal activities

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Babalwa Tembeni, Olusola Emmanuel Idowu, Rachid Benrkia, Salima Boutahiri, Opeyemi Joshua Olatunji. Biotransformation of selected secondary metabolites by Alternaria species and the pharmaceutical, food and agricultural application of biotransformation products [J]. Natural Products and Bioprospecting, 2024, 14(5): 46-46.
[2]	Yin-Zhong Fan, Chun Tian, Shun-Yao Tong, Qing Liu, Fan Xu, Bao-Bao Shi, Hong-Lian Ai, Ji-Kai Liu. The antifungal properties of terpenoids from the endophytic fungus Bipolaris eleusines [J]. Natural Products and Bioprospecting, 2023, 13(6): 43-43.
[3]	Jin-Ning Chu, Premanand Krishnan, Kuan-Hon Lim. A comprehensive review on the chemical constituents, sesquiterpenoid biosynthesis and biological activities of Sarcandra glabra [J]. Natural Products and Bioprospecting, 2023, 13(6): 53-53.
[4]	Teresa S. Catalá, Linn G. Speidel, Arlette Wenzel-Storjohann, Thorsten Dittmar, Deniz Tasdemir. Bioactivity profile of dissolved organic matter and its relation to molecular composition [J]. Natural Products and Bioprospecting, 2023, 13(5): 32-32.
[5]	Yun Zhao, Qiong Jin, Zi-Jiao Wang, Xing-Yu Tao, Xiao-Dong Luo. Quality assurance of postharvest grapes against Botrytis cinerea by terbinafine [J]. Natural Products and Bioprospecting, 2023, 13(4): 25-25.
[6]	Sitian Zhang, Shuyuan Mo, Fengli Li, Yaxin Zhang, Jianping Wang, Zhengxi Hu, Yonghui Zhang. Drimane sesquiterpenoids from a wetland soil-derived fungus Aspergillus calidoustus TJ403-EL05 [J]. Natural Products and Bioprospecting, 2022, 12(4): 27-27.
[7]	Xin Zhang, Yun-Bao Ma, Xiao-Feng He, Tian-Ze Li, Chang-An Geng, Li-Hua Su, Shuang Tang, Zhen Gao, Ji-Jun Chen. Artemyrianosins A–J, cytotoxic germacrane-type sesquiterpene lactones from Artemisia myriantha [J]. Natural Products and Bioprospecting, 2022, 12(3): 16-16.
[8]	Shui-Mei Zhang, Kun Hu, Xiao-Nian Li, Han-Dong Sun, Pema-Tenzin Puno. Lignans and sesquiterpenoids from the stems of Schisandra bicolor var. tuberculata [J]. Natural Products and Bioprospecting, 2022, 12(3): 19-19.
[9]	Lu Zhang, Ping Yi, Hui Yan, Xiao-Nian Li, Meng-Yuan Xia, Jun Yang, Ji-Feng Luo, Yue-Qiu He, Yue-Hu Wang. Five new 2-(2-phenylethyl)chromone derivatives and three new sesquiterpenoids from the heartwood of Aquilaria sinensis, an aromatic medicine in China [J]. Natural Products and Bioprospecting, 2022, 12(1): 1-14.
[10]	Shu-Ya Wei, Dong-Bao Hu, Meng-Yuan Xia, Ji-Feng Luo, Hui Yan, Jing-Hua Yang, Yun-Song Wang, Yue-Hu Wang. Sesquiterpenoids and 2-(2-Phenylethyl) chromone Derivatives from the Resinous Heartwood of Aquilaria sinensis [J]. Natural Products and Bioprospecting, 2021, 11(5): 545-555.
[11]	Shuang Tang, Yun-Bao Ma, Chang-An Geng, Cheng Shen, Tian-Ze Li, Xue-Mei Zhang, Li-Hua Su, Zhen Gao, Jing Hu, Ji-Jun Chen. Artemyrianins A-G from Artemisia myriantha and Their Cytotoxicity Against HepG2 Cells [J]. Natural Products and Bioprospecting, 2020, 10(4): 251-260.
[12]	Cheng Shen, Xiao-Yan Huang, Chang-An Geng, Tian-Ze Li, Shuang Tang, Li-Hua Su, Zhen Gao, Xue-Mei Zhang, Jing Hu, Ji-Jun Chen. Artemlavanins A and B from Artemisia lavandulaefolia and Their Cytotoxicity Against Hepatic Stellate Cell Line LX2 [J]. Natural Products and Bioprospecting, 2020, 10(4): 243-250.
[13]	Jun-Li Yang, Lei-Lei Liu, Yan-Ping Shi. Two New Eudesmane Sesquiterpenoids from the Flowers of Chrysanthemum indicum [J]. Natural Products and Bioprospecting, 2019, 9(2): 145-148.
[14]	Michel Feussi Tala, Jianchun Qin, Joseph T. Ndongo, Hartmut Laatsch. New Azulene-Type Sesquiterpenoids from the Fruiting Bodies of Lactarius deliciosus [J]. Natural Products and Bioprospecting, 2017, 7(3): 269-273.
[15]	Jun-Li Yang, Ya-Min Zhao, Yan-Ping Shi. Sesquiterpenoids from the Rhizomes of Homalomena occulta [J]. Natural Products and Bioprospecting, 2016, 6(4): 211-216.