Isolation and identification of actinomycetes from rhizosphere soil samples of mangrove forests in Quanzhou Bay and secondary metabolites of Streptomyces sp. W444
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1.Quanzhou Medical College, Quanzhou, Fujian, China;2.Fujian Institute of Microbiology, Fuzhou, Fujian, China;3.Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, Fujian, China

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This work was supported by the Science and Technology Project of Quanzhou City (2023NS082), the Key Science and Technology Project of Quanzhou Medical College (XJK2210A), the Scientific Research Foundation of Third Institute of Oceanography, Ministry of Natural Resources (HY202304), and the Research-based Teaching Project of Quanzhou Medical College (XJJK2308).

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    Abstract:

    Objective To isolate and identify actinomycetes from two mangrove soil samples in Quanzhou Bay as well as secondary metabolites from the target strain Streptomyces sp. W444 with antifungal activity.Methods The rhizosphere soil samples of two different mangrove plants were collected from Luoyang River in Quanzhou Bay. Actinomycetes were isolated from the soil samples by the dilution plating method. The isolates were classified by the phylogenetic tree constructed based on 16S rRNA gene sequences. The antifungal activities of the isolates were examined by the agar diffusion method. The target strain Streptomyces sp. W444 was subjected to fermentation scale-up for the isolation of secondary metabolites. Furthermore, the biosynthetic gene clusters were analyzed to deduce the biosynthetic pathway of staurosporine.Results A total of 56 strains of actinomycetes were isolated from mangrove soil samples and categorized into 8 genera belonging to 6 families of 6 orders. Among them, Streptomyces and Micromonospora were dominant, with the relative abundance of 41.0% and 33.9%, respectively. Strain Streptomyces sp. W444 exhibited excellent antifungal activity, and three indoles (staurosporine, K252c, and streptochlorin) were isolated and identified from this strain. The biosynthetic gene cluster of staurosporine was localized in the genome of Streptomyces sp. W444 by bioinformatics analysis. The biosynthetic pathway of staurosporine was then proposed.Conclusion Actinomycetes in the rhizosphere soil of mangrove plants in Quanzhou Bay had high diversity and contained potential natural product resources. Staurosporine, K252c, and streptochlorin were isolated from strain W444. These findings lay a solid foundation for studying the diversity and secondary metabolites of cultivable actinomycetes in mangrove forests in Quanzhou Bay.

    Reference
    [1] RODRIGUES ML, NOSANCHUK JD. Fungal diseases as neglected pathogens: a wake-up call to public health officials[J]. PLoS Neglected Tropical Diseases, 2020, 14(2): e0007964.
    [2] FISHER MC, ALASTRUEY-IZQUIERDO A, BERMAN J, BICANIC T, BIGNELL EM, BOWYER P, BROMLEY M, BRüGGEMANN R, GARBER G, CORNELY OA, GURR SJ, HARRISON TS, KUIJPER E, RHODES J, SHEPPARD DC, WARRIS A, WHITE PL, XU JP, ZWAAN B, VERWEIJ PE. Tackling the emerging threat of antifungal resistance to human health[J]. Nature Reviews Microbiology, 2022, 20(9): 557-571.
    [3] REVIE NM, IYER KR, ROBBINS N, COWEN LE. Antifungal drug resistance: evolution, mechanisms and impact[J]. Current Opinion in Microbiology, 2018, 45:70-76.
    [4] RüTTEN A, KIRCHNER T, MUSIOL-KROLL EM. Overview on strategies and assays for antibiotic discovery[J]. Pharmaceuticals, 2022, 15(10): 1302.
    [5] ALAM K, MAZUMDER A, SIKDAR S, ZHAO YM, HAO JF, SONG CY, WANG YY, SARKAR R, ISLAM S, ZHANG YM, LI AY. Streptomyces: the biofactory of secondary metabolites[J]. Frontiers in Microbiology, 2022, 13: 968053.
    [6] OSSAI J, KHATABI B, NYBO SE, KHAREL MK. Renewed interests in the discovery of bioactive actinomycete metabolites driven by emerging technologies[J]. Journal of Applied Microbiology, 2022, 132(1): 59-77.
    [7] de LIMA JúNIOR AA, de SOUSA EC, de OLIVEIRA THB, de SANTANA RCF, da SILVA SKR, COELHO LCBB. Genus Streptomyces: recent advances for biotechnological purposes[J]. Biotechnology and Applied Biochemistry, 2023, 70(4): 1504-1517.
    [8] KIM ES. recent advances of actinomycetes[J]. Biomolecules, 2021, 11(2): 134.
    [9] 徐静, 邹仁健, 陈红军, 温珍昌. 红树林放线菌生物多样性及其抗菌活性代谢产物研究进展[J]. 广东海洋大学学报, 2022, 42(6): 143-152.XU J, ZOU RJ, CHEN HJ, WEN ZC. Research progress on biodiversity and antimicrobial metabolites from mangrove actinomycetes[J]. Journal of Guandong Ocean University, 2022, 42(6): 143-152 (in Chinese).
    [10] 林鹏, 张瑜斌, 邓爱英, 庄铁诚. 九龙江口红树林土壤微生物的类群及抗菌活性[J]. 海洋学报, 2005, 27(3): 133-141.LIN P, ZHANG YB, DENG AY, ZHUANG TC. Microflora and antimicrobial activities of soil microorganisms in mangrove forests in the Jiulong Estuary[J]. Acta Oceanologica Sinica, 2005, 27(3): 133-141 (in Chinese).
    [11] WANG Z, YIN JL, BAI M, YANG J, JIANG CP, YI XX, LIU YH, GAO CH. new polyene macrolide compounds from mangrove-derived strain Streptomyces hiroshimensis GXIMD 06359: isolation, antifungal activity, and mechanism against Talaromyces marneffei[J]. Marine Drugs, 2024, 22(1): 38.
    [12] WANG WL, SONG TF, CHAI WY, CHEN L, CHEN L, LIAN XY, ZHANG ZZ. Rare polyene-polyol macrolides fromMangrove-derived Streptomyces sp. ZQ4BG[J]. Scientific Reports, 2017, 7: 1703.
    [13] CHE Q, LI T, LIU XF, YAO TT, LI J, GU QQ, LI DH, LI WL, ZHU TJ. Genome scanning inspired isolation of reedsmycins A-F, polyene-polyol macrolides from Streptomyces sp. CHQ-64[J]. RSC Advances, 2015, 5(29): 22777-22782.
    [14] ZENG QF, HUANG HQ, ZHU J, FANG Z, SUN QG, BAO SX. A new nematicidal compound produced by Streptomyces albogriseolus HA10002[J]. Antonie Van Leeuwenhoek, 2013, 103(5): 1107-1111.
    [15] 许敬华, 李意敏, 丁思龙, 张秋芳, 陈永山. 泉州湾红树林人工种植过程根际微生物群落结构演变特征[J]. 湿地科学与管理, 2023, 19(1): 9-14.XU JH, LI YM, DING SL, ZHANG QF, CHEN YS. Characteristics of rhizosphere microbial community structure evolution during mangrove plantation[J]. Wetland Science & Management, 2023, 19(1): 9-14 (in Chinese).
    [16] MIN LL, WANG WZ, OREN A, LAI QL, HUANG ZB. Coraliomargarita parva sp. nov., isolated from mangrove sediment and genome-based analysis of the class Opitutae revealed five novel families: Coraliomargaritaceae fam. nov., Pelagicoccaceae fam. nov., Cerasicoccaeae fam. nov., Oceanipulchritudinaceae fam. nov., and Alterococcaeae fam. nov.[J]. Frontiers in Microbiology, 2023, 14: 1202141.
    [17] HU YZ, GUO Y, LAI QL, DONG L, HUANG ZB. Draconibacterium mangrovi sp. nov., isolated from mangrove sediment[J]. International Journal of Systematic and Evolutionary Microbiology, 2020, 70(8): 4816-4821.
    [18] 梁效伟. 台湾海峡海洋沉积物放线菌的多样性及次级代谢产物生物合成基因筛选[D]. 福州: 福建医科大学硕士学位论文, 2012.LIANG XW. Diversity of actinomycetes in marine sediments of Taiwan Province strait and screening of biosynthesis genes of secondary metabolites[D]. Fuzhou: Master's Thesis of Fujian Medical University, 2012 (in Chinese).
    [19] WATANABE H, AMANO S, YOSHIDA J, SASAKI T, HATSU M, TAKEUCHI Y, KAJII K, SHOMURA T, SEZAKI M. A new antibiotic SF2583A, 4-chloro-5-(3′-indolyl)oxazole, produced by Streptomyces[J]. Meiji Seika Kenkyu Nenpo, 1988, 27: 55-62.
    [20] YASUZAWA T, IIDA T, YOSHIDA M, HIRAYAMA N, TAKAHASHI M, SHIRAHATA K, SANO H. The structures of the novel protein kinase C inhibitors K-252a, b, c and d[J]. The Journal of Antibiotics, 1986, 39(8): 1072-1078.
    [21] DE FARIA AF, MARTINEZ DST, MEIRA SMM, DE MORAES ACM, BRANDELLI A, FILHO AGS, ALVES OL. Anti-adhesion and antibacterial activity of silver nanoparticles supported on graphene oxide sheets[J]. Colloids and Surfaces B: Biointerfaces, 2014, 113: 115-124.
    [22] LI XB, TANG JS, GAO H, DING R, LI J, HONG K, YAO XS. A new staurosporine analog from actinomycetes Streptomyces sp. (172614)[J]. Journal of Asian Natural Products Research, 2011, 13(8): 765-769.
    [23] BLIN K, SHAW S, AUGUSTIJN HE, REITZ ZL, BIERMANN F, ALANJARY M, FETTER A, TERLOUW BR, METCALF WW, HELFRICH EJN, van WEZEL GP, MEDEMA MH, WEBER T. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation[J]. Nucleic Acids Research, 2023, 51(W1): W46-W50.
    [24] ONAKA H, TANIGUCHI SI, IGARASHI Y, FURUMAI T. Cloning of the staurosporine biosynthetic gene cluster from Streptomyces sp. TP-A0274 and its heterologous expression in Streptomyces lividans[J]. The Journal of Antibiotics, 2002, 55(12): 1063-1071.
    [25] GROOM K, BHATTACHARYA A, ZECHEL DL. Rebeccamycin and staurosporine biosynthesis: insight into the mechanisms of the flavin-dependent monooxygenases RebC and StaC[J]. Chembiochem, 2011, 12(3): 396-400.
    [26] SALAS AP, ZHU LL, SáNCHEZ C, BRA?A AF, ROHR J, MéNDEZ C, SALAS JA. Deciphering the late steps in the biosynthesis of the anti-tumour indolocarbazole staurosporine: sugar donor substrate flexibility of the StaG glycosyltransferase[J]. Molecular Microbiology, 2005, 58(1): 17-27.
    [27] HOWARD-JONES AR, WALSH CT. Staurosporine and rebeccamycin aglycones are assembled by the oxidative action of StaP, StaC, and RebC on chromopyrrolic acid[J]. Journal of the American Chemical Society, 2006, 128(37): 12289-12298.
    [28] HOLGUIN G, VAZQUEZ P, BASHAN Y. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview[J]. Biology and Fertility of Soils, 2001, 33(4): 265-278.
    [29] 颜利, 王金坑, 蒋金龙, 傅世锋, 戴娟娟, 欧阳玉蓉. 海洋生物多样性保护空间规划分区体系构建及其在泉州湾的应用[J]. 台湾海峡, 2012, 31(2): 238-245.YAN L, WANG JK, JIANG JL, FU SF, DAI JJ, OUYANG YR. Spatial plan zoning system for marine biodiversity conservation and a case study of the Quanzhou Bay[J]. Journal of Oceanography in Taiwan Strait, 2012, 31(2): 238-245 (in Chinese).
    [30] 何洁, 张道锋, 徐盈, 张晓梅, 唐蜀昆, 徐丽华, 李文均. 印度洋红树林沉积物可培养海洋放线菌多样性及其活性[J]. 微生物学报, 2012, 52(10): 1195-1202.HE J, ZHANG DF, XU Y, ZHANG XM, TANG SK, XU LH, LI WJ. Diversity and bioactivities of culturable marine actinobacteria isolated from mangrove sediment in Indian Ocean[J]. Acta Microbiologica Sinica, 2012, 52(10): 1195-1202 (in Chinese).
    [31] 何子邦, 李顺莲, 吴友浪, 陈明胜, 庹利. 广西沿海红树林土壤放线菌多样性、新颖性及抗菌活性研究[J]. 中国抗生素杂志, 2022, 47(5): 463-473.HE ZB, LI SL, WU YL, CHEN MS, TUO L. Diversity, novelty, and antibiotic activity of actinobacteria isolated from mangrove soil in Guangxi[J]. Chinese Journal of Antibiotics, 2022, 47(5): 463-473 (in Chinese).
    [32] XU L, LIU RS, FANG JB, ZHANG NJ, PU FQ, LEI Z, DING WJ, JIANG YJ. Cytotoxic and antifungal staurosporine derivatives from marine-derived actinomycete Streptomyces sp. ZS-A121[J]. Chemistry & Biodiversity, 2024, 21(2): e202301712.
    [33] MCALPINE JB, KARWOWSKI JP, JACKSON M, MULLALLY MM, HOCHLOWSKI JE, PREMACHANDRAN U, BURRES NS. MLR-52, (4′-demethylamino-4′,5′-dihydroxystaurosporine), a new inhibitor of protein kinase C with immunosuppressive activity[J]. The Journal of Antibiotics, 1994, 47(3): 281-288.
    [34] ZHOU B, HU ZJ, ZHANG HJ, LI JQ, DING WJ, MA ZJ. Bioactive staurosporine derivatives from the Streptomyces sp. NB-A13[J]. Bioorganic Chemistry, 2019, 82: 33-40.
    [35] XIAO F, LI HY, XU MY, LI T, WANG J, SUN CM, HONG K, LI WL. staurosporine derivatives generated by pathway engineering in a heterologous host and their cytotoxic selectivity[J]. Journal of Natural Products, 2018, 81(8): 1745-1751.
    [36] ZHANG MZ, CHEN Q, MULHOLLAND N, BEATTIE D, IRWIN D, GU YC, YANG GF, CLOUGH J. Synthesis and fungicidal activity of novel pimprinine analogues[J]. European Journal of Medicinal Chemistry, 2012, 53: 283-291.
    [37] 王冕, 郝晓萌, 李娇, 胡媛媛, 关艳, 王以光, 甘茂罗, 肖春玲. 海洋链霉菌IMB3-202产生的吲哚咔唑生物碱[J]. 中国医药生物技术, 2018, 13(2): 137-144.WANG M, HAO XM, LI J, HU YY, GUAN Y, WANG YG, GAN ML, XIAO CL. Identification of indolocarbazoles from the marine-derived Streptomyces sp. IMB3-202[J]. Chinese Medicinal Biotechnology, 2018, 13(2): 137-144(in Chinese).
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ZHANG Wenzhou, CHEN Linlin, LIN Shuisen, LIN Yangjun, ZHUANG Yue’e, XIE Zhixin, JIANG Hong, LIAN Yunyang, LUO Zhuhua, PENG Fei. Isolation and identification of actinomycetes from rhizosphere soil samples of mangrove forests in Quanzhou Bay and secondary metabolites of Streptomyces sp. W444. [J]. Acta Microbiologica Sinica, 2025, 65(2): 597-613

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  • Received:September 23,2024
  • Online: February 18,2025
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