Endophytic actinomycetes from mangrove plant \(\textit{Avicennia marina}\) in Quang Ninh province, Vietnam: distribution, cytotoxicity, and antioxidant activities
Author affiliations
DOI:
https://doi.org/10.15625/2615-9023/17492Keywords:
Avicennia, anticancer, antioxidant, Avicennia marina, mangrove, Streptomyces. cacaoiAbstract
Mangrove endophytes have recently gained considerable attention due to their diversity and abundance of novel bioactive secondary metabolites. Despite the fact that Streptomyces species are producers of more than 75% of commercialized antibiotics, Streptomyces associated with the extremely widespread mangrove plant Avicennia marina remain poorly characterized. In this study, nine actinomycetes were isolated from A. marina growing in a mangrove forest, as yet unexplored, of Quang Ninh province, Vietnam. Phylogenetic analysis of actinomycetes-specific 16S rRNA sequences indicated that they were subjected to five Streptomyces species including Streptomyces cacaoi, Streptomyces californicus, Streptomyces enissocaesillis, Streptomyces coelicoflavus, and Streptomyces variabilis, which have not been previously reported in mangrove plants. Among them, S. cacaoi AM1 showed strong inhibition effects against six tested pathogenic bacteria with inhibitory zones ranging from 7.5−22.3 mm. Using standard 3-(4,5-dimethythiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay, 100 µg/mL ethyl acetate extract of AM1 showed potent cytotoxicity against breast cancer MCF-7 and lung cancer A549 cell lines with cell viability of 16.5 ± 1.28% and 17.69 ± 2.3%, respectively. As for antioxidant activities, AM1 extract exhibited strong antioxidant activities against 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical (92.4 ± 0.004%) and superoxide anion radical (42.4 ± 0.019%), which were positively correlated to high polyphenol (84.3 ± 3.4 µg GAE/g FW) and flavonoid (34.9 ± 4.8 µg QE/g FW) contents. These findings indicated that S. cacaoi AM1 could be a promising reservoir of antibacterial, anticancer, and antioxidant agents. This is the first report of mangrove endophytic Streptomyces derived from A. marina.
Downloads
Metrics
References
Balouiri M., Sadiki M., Ibnsouda S. K., 2016. Methods for in vitro evaluating antimicrobial activity: A review. J. Pharm. Anal, 6(2): 71–79. https://doi.org/10.1016/j.jpha.2015.11.005
Belknap K. C., Park C. J., Barth B. M., Andam C. P., 2020. Genome mining of biosynthetic and chemotherapeutic gene clusters in Streptomyces bacteria. Sci. Rep, 10(1): 2003. https://doi.org/10.1038/ s41598-020-58904-9
da Silva M. H. R., Cueva-Yesquén L. G., Júnior S. B., Garcia V. L., Sartoratto A., de Angelis D. d. F., de Angelis D. A., 2020. Endophytic fungi from Passiflora incarnata: an antioxidant compound source. Arch. Microbiol, 202(10): 2779–2789. https://doi.org/10.1007/s00203-020-02001-y
Dholakiya R. N., Kumar R., Mishra A., Mody K. H., Jha B., 2017. Antibacterial and antioxidant activities of novel actinobacteria strain isolated from Gulf of Khambhat, Gujarat. Front. Microbiol, 8: 2420–2420. https://doi.org/10.3389/fmicb.2017.02420
Ding L., Maier A., Fiebig H. H., Lin W. H., Hertweck C., 2011. A family of multicyclic indolosesquiterpenes from a bacterial endophyte. Org. Biomol. Chem, 9(11): 4029–4031. https://doi.org/10.1039/c1ob05283g
Griffiths K., Aggarwal B. B., Singh R. B., Buttar H. S., Wilson D., De Meester F., 2016. Food antioxidants and their anti-inflammatory properties: A potential role in cardiovascular diseases and cancer prevention. Diseases (Basel, Switzerland), 4(3). https://doi.org/10.3390/ diseases4030028
Janaki T., 2019. Anticancer activity of Streptomyces cacaoi subsp cacaoi M20 against breast cancer (MCF-7) cell lines. Int. J. Chemtech Res. http://dx.doi.org/ 10.20902/IJCTR.2019.120415
Jiang Z. K., Tuo L., Huang D. L., Osterman I. A., Tyurin A. P., Liu S. W., Lukyanov D. A., Sergiev P. V., Dontsova O. A., Korshun V. A., Li F. N., Sun C. H., 2018. Diversity, novelty, and antimicrobial activity of endophytic actinobacteria from mangrove plants in Beilun Estuary National Nature Reserve of Guangxi, China. Front. Microbiol, 9: 868. https://doi.org/10.3389/fmicb.2018.00868
Kadaikunnan S., Rejiniemon T., Khaled J. M., Alharbi N. S., Mothana R., 2015. In-vitro antibacterial, antifungal, antioxidant and functional properties of Bacillus amyloliquefaciens. Ann. Clin. Microbiol. Antimicrob, 14: 9−9. https://doi.org/ 10.1186/s12941-015-0069-1
Kaweewan I., Hemmi H., Komaki H., Kodani S., 2020. Isolation and structure determination of a new antibacterial peptide pentaminomycin C from Streptomyces cacaoi subsp. cacaoi. J. Antibiot, 73(4): 224–229. https://doi.org/ 10.1038/s41429-019-0272-y
Khan N., Yılmaz S., Aksoy S., Uzel A., Tosun Ç., Kirmizibayrak P. B., Bedir E., 2019. Polyethers isolated from the marine actinobacterium Streptomyces cacaoi inhibit autophagy and induce apoptosis in cancer cells. Chem. Biol. Interact, 307: 167–178. https://doi.org/10.1016/j.cbi. 2019.04.035
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
Lanoot B., Vancanneyt M., Cleenwerck I., Wang L., Li W., Liu Z., Swings J., 2002. The search for synonyms among Streptomycetes by using SDS-PAGE of whole-cell proteins. Emendation of the species Streptomyces aurantiacus, Streptomyces cacaoi subsp. cacaoi, Streptomyces caeruleus and Streptomyces violaceus. Int. J. Syst. Evol. Microbiol, 52(Pt 3): 823–829. https://doi.org/ 10.1099/00207713-52-3-823
Li F., Liu S., Lu Q., Zheng H., Osterman I. A., Lukyanov D. A., Sergiev P. V., Dontsova O. A., Liu S., Ye J., Huang D., Sun C., 2019. Studies on antibacterial activity and diversity of cultivable actinobacteria isolated from mangrove soil in Futian and Maoweihai of China. Evid. Based. Complement. Alternat. Med, 2019: 3476567. https://doi.org/10.1155/2019/ 3476567
Momtazi-Borojeni A. A., Behbahani M., Sadeghi-Aliabadi H., 2013. Antiproliferative activity and apoptosis induction of crude extract and fractions of Avicennia marina. Iran J. Basic. Med. Sci, 16(11): 1203–1208.
Musa Z., Ma J., Egamberdieva D., Abdelshafy Mohamad O. A., Abaydulla G., Liu Y., Li W.-J., Li L., 2020. Diversity and antimicrobial potential of cultivable endophytic actinobacteria associated with the medicinal plant Thymus roseus. Front. Microbiol: 11. https://doi.org/10.3389/ fmicb.2020.00191
Okla M. K., Alatar A. A., Al-Amri S. S., Soufan W. H., Ahmad A., Abdel-Maksoud M. A., 2021. Antibacterial and antifungal activity of the extracts of different parts of Avicennia marina (Forssk.) Vierh. Plants, 10(2): 252. https://doi.org/10.3390/plants10020252
Pavan Kumar J. G. S., Gomathi A., Gothandam K. M., Vasconcelos V., 2018. Bioactivity assessment of Indian origin-mangrove actinobacteria against Candida albicans. Mar. Drugs, 16(2). https://doi.org/10.3390/md16020060
Petitjean A., Mathe E., Kato S., Ishioka C., Tavtigian S. V., Hainaut P., Olivier M., 2007. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum. Mutat, 28(6): 622–629. https://doi.org/10.1002/humu.20495
Quach N. T., Nguyen Q. H., Vu T. H. N., Le T. T. H., Ta T. T. T., Nguyen T. D., Van Doan T., Van Nguyen T., Dang T. T., Nguyen X. C., Chu H. H., Phi Q. T., 2021. Plant-derived bioactive compounds produced by Streptomyces variabilis LCP18 associated with Litsea cubeba (Lour.) Pers as potential target to combat human pathogenic bacteria and human cancer cell lines. Braz. J. Microbiol, 52(3): 1215–1224. https://doi.org/ 10.1007/s42770-021-00510-6
Rajoka M. S. R., Mehwish H. M., Hayat H. F., Hussain N., Sarwar S., Aslam H., Nadeem A., Shi J., 2019. Characterization, the antioxidant and antimicrobial activity of exopolysaccharide isolated from poultry origin Lactobacilli. Probiotics. Antimicrob. Proteins, 11(4): 1132−1142. doi: 10.1007/s12602-018-9494-8
Rani R., Arora S., Kaur J., Manhas R. K., 2018. Phenolic compounds as antioxidants and chemopreventive drugs from Streptomyces cellulosae strain TES17 isolated from rhizosphere of Camellia sinensis. BMC Complement. Altern. Med, 18(1): 82. https://doi.org/10.1186/s12906-018-2154-4
Salam N., Khieu T.-N., Liu M.-J., Vu T.-T., Chu-Ky S., Quach N.-T., Phi Q.-T., Narsing Rao M. P., Fontana A., Sarter S., Li W.-J., 2017. Endophytic actinobacteria associated with Dracaena cochinchinensis Lour.: isolation, diversity, and their cytotoxic activities. Biomed. Res. Int., 2017: 1308563. https://doi.org/ 10.1155/2017/1308563
Sangkanu S., Rukachaisirikul V., Suriyachadkun C., Phongpaichit S., 2017. Evaluation of antibacterial potential of mangrove sediment-derived actinomycetes. Microb. Pathog, 112: 303−312. https://doi.org/10.1016/ j.micpath.2017.10.010
Ser H. L., Palanisamy U. D., Yin W. F., Abd Malek S. N., Chan K. G., Goh B. H., Lee L. H., 2015. Presence of antioxidative agent, Pyrrolo[1,2-a]pyrazine-1,4-dione, hexahydro- in newly isolated Streptomyces mangrovisoli sp. nov. Front. Microbiol, 6: 854. https://doi.org/10.3389/ fmicb.2015.00854
Singh R., Dubey A. K., 2020. Isolation and characterization of a new endophytic actinobacterium Streptomyces californicus strain ADR1 as a promising source of anti-bacterial, anti-biofilm and antioxidant metabolites. Microorganisms, 8(6). https://doi.org/10.3390/microorganisms8060929
Taechowisan T., Peberdy J. F., Lumyong S., 2003. Isolation of endophytic actinomycetes from selected plants and their antifungal activity. World J. Microbiol. Biotechnol, 19(4): 381–385. https://doi.org/10.1023/A:1023901107182
Tan L. T.-H., Chan K.-G., Chan C. K., Khan T. M., Lee L. H., Goh B. H., 2018. Antioxidative potential of a Streptomyces sp. MUM292 isolated from mangrove soil. Biomed Res. Int, 2018: 4823126. https://doi.org/10.1155/2018/4823126
Tang Z., Qin Y., Chen W., Zhao Z., Lin W., Xiao Y., Chen H., Liu Y., Chen H., Bu T., Li Q., Cai Y., Yao H., Wan Y., 2021. Diversity, chemical constituents, and biological activities of endophytic fungi isolated from Ligusticum chuanxiong Hort. Front. Microbiol: 12. https://doi.org/ 10.3389/fmicb.2021.771000
Vu T. H. N., Nguyen Q. H., Dinh T. M. L., Quach N. T., Khieu T. N., Hoang H., Chu-Ky S., Vu T. T., Chu H. H., Lee J., Kang H., Li W. J., Phi Q. T., 2020. Endophytic actinomycetes associated with Cinnamomum cassia Presl in Hoa Binh province, Vietnam: Distribution, antimicrobial activity and, genetic features. J. Gen. Appl. Microbiol, 66(1): 24–31. https://doi.org/10.2323/ jgam.2019.04.004
Wang F., Xu M., Li Q., Sattler I., Lin W., 2010. p-Aminoacetophenonic acids produced by a mangrove endophyte Streptomyces sp. (strain HK10552). Molecules (Basel, Switzerland), 15(4): 2782–2790. https://doi.org/10.3390/ molecules15042782
Wang J. F., Liu S. S., Song Z. Q., Xu T. C., Liu C. S., Hou Y. G., Huang R., Wu S. H., 2020. Naturally occurring flavonoids and isoflavonoids and their microbial transformation: A review. Molecules (Basel, Switzerland), 25(21). doi: 10.3390/molecules25215112
Wang S.-S., Liu J.-M., Sun J., Sun Y.-F., Liu J.-N., Jia N., Fan B., Dai X.-F., 2019. Diversity of culture-independent bacteria and antimicrobial activity of culturable endophytic bacteria isolated from different Dendrobium stems. Sci. Rep, 9(1): 10389–10389. https://doi.org/10.1038/s41598-019-46863-9
Williams J. R., Yang R., Clifford J. L., Watson D., Campbell R., Getnet D., Kumar R., Hammamieh R., Jett M., 2019. Functional Heatmap: an automated and interactive pattern recognition tool to integrate time with multi-omics assays. BMC Bioinform, 20(1): 81. https://doi.org/ 10.1186/s12859-019-2657-0
Yang H., Deng J., Yuan Y., Fan D., Zhang Y., Zhang R., Han B., 2015. Two novel exopolysaccharides from Bacillus amyloliquefaciens C-1: antioxidation and effect on oxidative stress. Curr. Microbiol, 70(2): 298–306. https://doi.org/ 10.1007/s00284-014-0717-2