Antiplasmodial activity, biosynthetic gene clusters diversity, and secondary metabolite constituent of selected Indonesian Streptomyces
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EMA DAMAYANTI
https://orcid.org/0000-0002-4017-0499
PUSPITA LISDIYANTI
https://orcid.org/0000-0002-3498-7355
ANDINI SUNDOWO
https://orcid.org/0000-0002-7492-7218
SHANTI RATNAKOMALA
https://orcid.org/0000-0003-4576-4728
ACHMAD DINOTO
https://orcid.org/0000-0002-9182-7665
JAKA WIDADA
https://orcid.org/0000-0001-5012-3795
MUSTOFA
♥
https://orcid.org/0000-0001-9251-9851
Abstract
Abstract. Damayanti E, Lisdiyanti P, Sundowo A, Ratnakomala S, Dinoto A, Widada J, Mustofa. 2021. Antiplasmodial activity, biosynthetic gene clusters diversity, and secondary metabolite constituent of selected Indonesian Streptomyces. Biodiversitas 22: 3478-3487. Actinobacteria of the genus Streptomyces are known as the primary candidate antibiotics, but still limited for antiplasmodial drugs. This study aimed to investigate the antiplasmodial activity, the biosynthetic gene clusters (BGCs) diversity, and the secondary metabolites constituent of selected Indonesian Streptomyces. The bacteria were isolated from various habitats: karst soil (GMR22), mangrove sediments (BSE7F and SHP 22-7), and marine sediment (GMY01). Molecular identification by 16S rDNA sequencing were performed for confirmation and morphological characterization by scanning electron microscope (SEM) were performed for identification. In vitro antiplasmodial assay was performed on human Plasmodium falciparum FCR-3. The BGCs which encode secondary metabolites were analysed using antiSMASH version 5 based on available whole genome sequence (WGS) data. The secondary metabolites were obtained from liquid fermentation followed by extraction using methanol and ethyl acetate. The secondary metabolites constituent was determined by liquid chromatography tandem mass spectrometry (LC-MS/MS). The molecular identification showed that GMR22 had similarity to Streptomyces lactacystinicus (98.02%), while BSE7F was similar to Streptomyces althioticus (97.06%), SHP 22-7 was similar to Streptomyces rochei (94.84%), and GMY01 to Streptomyces odonnellii (98.57%). All of isolates had morphological characteristics as the genus Streptomyces bacteria. The highest Plasmodium inhibition (81.84 ± 3.5%) was demonstrated by ethyl acetate extract of marine-derived Streptomyces sp. GMY01 (12.5 µg/mL). Non-ribosomal polyketide synthetase (NRPS), polyketide synthase (PKS) and hybrid of NRPS-PKS were the major BGCs in all Streptomyces. Majority of the Streptomyces produced compounds containing CHON elements with molecular weight approximately 100-400 Da. The active extract of GMY01 bacterium had five major detected compounds, namely kuraramine (C12H18N2O2), laminine (C9H20N2O2) 2-ethylacetanilide (C10H13NO), propoxur (C11H15NO3), and 3-methyl-1,2-diphenylbutan-1-one (C17H18O). This Indonesian marine bacterium is potential for bioassay guided isolation of antiplasmodial compounds in the future studies.
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References
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Komaki, H., Sakurai, K., Hosoyama, A., Kimura, A., Igarashi, Y., Tamura, T., 2018. Diversity of nonribosomal peptide synthetase and polyketide synthase gene clusters among taxonomically close Streptomyces strains. Sci. Rep. https://doi.org/10.1038/s41598-018-24921-y
Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msy096
Kumar, V., Bharti, A., Gusain, O., Bisht, G.S., 2011. Scanning electron microscopy of Streptomyces without use of any chemical fixatives. Scanning 33, 446–449. https://doi.org/10.1002/sca.20261
Low, Z.J., Pang, L.M., Ding, Y., Cheang, Q.W., Hoang, K.L.M., Tran, H.T., Li, J., Liu, X.W., Kanagasundaram, Y., Yang, L., Liang, Z.X., 2018. Identification of a biosynthetic gene cluster for the polyene macrolactam sceliphrolactam in a Streptomyces strain isolated from mangrove sediment. Sci. Rep. https://doi.org/10.1038/s41598-018-20018-8
Mbaba, M., de la Mare, J.A., Sterrenberg, J.N., Kajewole, D., Maharaj, S., Edkins, A.L., Isaacs, M., Hoppe, H.C., Khanye, S.D., 2019. Novobiocin–ferrocene conjugates possessing anticancer and antiplasmodial activity independent of HSP90 inhibition. J. Biol. Inorg. Chem. https://doi.org/10.1007/s00775-018-1634-9
Nurjasmi, R., Widada, J., 2009. Diversity of Actinomycetes at Several Forest Types in Wanagama I Yogyakarta and Their Potency as a Producer of Antifungal Compound. Indones. J. Biotechnol. 14, 1196–1205. https://doi.org/10.22146/ijbiotech.7813
Pereira, P.H.F., Macrae, A., Reinert, F., De Souza, R.F., Coelho, R.R.R., Pötter, G., Klenk, H.P., Labeda, D.P., 2017. Streptomyces odonnellii sp. Nov., a proteolytic streptomycete isolated from soil under cerrado (savanna) vegetation cover. Int. J. Syst. Evol. Microbiol. https://doi.org/10.1099/ijsem.0.002446
Sanz, L.M., Crespo, B., De-Cózar, C., Ding, X.C., Llergo, J.L., Burrows, J.N., García-Bustos, J.F., Gamo, F.J., 2012. P. falciparum in vitro killing rates allow to discriminate between different antimalarial mode-of-action. PLoS One 7. https://doi.org/10.1371/journal.pone.0030949
Seipke, R.F., 2015. Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS One. https://doi.org/10.1371/journal.pone.0116457
Sottorff, I., Wiese, J., Lipfert, M., Preußke, N., Sönnichsen, F.D., Imhoff, J.F., 2019. Different secondary metabolite profiles of phylogenetically almost identical streptomyces griseus strains originating from geographically remote locations. Microorganisms. https://doi.org/10.3390/microorganisms7060166
Sumanadasa, S.D.M., Goodman, C.D., Lucke, A.J., Skinner-Adams, T., Saham, I., Haque, A., Do, T.A., McFadden, G.I., Fairlie, D.P., Andrews, K.T., 2012. Antimalarial activity of the anticancer histone deacetylase inhibitor SB939. Antimicrob. Agents Chemother. 56, 3849–3856. https://doi.org/10.1128/AAC.00030-12
Tajuddeen, N., Van Heerden, F.R., 2019. Antiplasmodial natural products: An update. Malar. J. 18, 1–62. https://doi.org/10.1186/s12936-019-3026-1
Také, A., Matsumoto, A., Omura, S., Takahashi, Y., 2015. Streptomyces lactacystinicus sp. nov. and Streptomyces cyslabdanicus sp. nov., producing lactacystin and cyslabdan, respectively. J. Antibiot. (Tokyo). https://doi.org/10.1038/ja.2014.162
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. https://doi.org/10.1093/nar/25.24.4876
Trager, W., Jensen, J.B., 2005. Human malaria parasites in continuous culture. J. Parasitol. https://doi.org/10.1645/0022-3395(2005)091[0484:HMPICC]2.0.CO;2
Undabarrena, A., Ugalde, J.A., Seeger, M., Cámara, B., 2017. Genomic data mining of the marine actinobacteria Streptomyces sp. H-KF8 unveils insights into multi-stress related genes and metabolic pathways involved in antimicrobial synthesis. PeerJ 2017. https://doi.org/10.7717/peerj.2912
Werdyani, S., Wijayanti, N., Fitria, A., Rahmawati, S., 2017. Cytotoxic effects of ethyl acetate fractions from secondary metabolites of Streptomyces Sp. GMY01 on human breast cancer MCF7 cell lines. Asian J. Pharm. Clin. Res. 10, 9–11. https://doi.org/10.22159/ajpcr.2017v10s3.21351
Xu, H., Chater, K.F., Deng, Z., Tao, M., 2008. A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in streptomyces. J. Bacteriol. https://doi.org/10.1128/JB.01849-07
Xu, L., Ye, K.X., Dai, W.H., Sun, C., Xu, L.H., Han, B.N., 2019. Comparative genomic insights into secondary metabolism biosynthetic gene cluster distributions of marine Streptomyces. Mar. Drugs. https://doi.org/10.3390/md17090498
Zhang, L., Wang, J., Li, T., Li, P., Wang, Y., Yang, M., Liu, Jin?Ping, Liu, Ji?Hua, 2019. Determination of the chemical components and phospholipids of velvet antler using UPLC/QTOF?MS coupled with UNIFI software. Exp. Ther. Med. 3789–3799. https://doi.org/10.3892/etm.2019.7372
Ziemert, N., Alanjary, M., Weber, T., 2016. The evolution of genome mining in microbes-a review. Nat. Prod. Rep. https://doi.org/10.1039/c6np00025h
Antony, H.A., Parija, S.C., 2016. Antimalarial drug resistance: An overview. Trop. Parasitol. https://doi.org/10.4103/2229-5070.175081
Arakawa, K., Sugino, F., Kodama, K., Ishii, T., Kinashi, H., 2005. Cyclization mechanism for the synthesis of macrocyclic antibiotic lankacidin in Streptomyces rochei. Chem. Biol. https://doi.org/10.1016/j.chembiol.2005.01.009
Beck, C., Garzón, J.F.G., Weber, T., 2020. Recent Advances in Re-engineering Modular PKS and NRPS Assembly Lines. Biotechnol. Bioprocess Eng. https://doi.org/10.1007/s12257-020-0265-5
Bloland, P.B., 2001. Drug resistance in malaria (WHO/CDS/CSR/DRS/2001.4). http//whqlibdoc.who.int/hq/2001/WHO_CDS_CSR_DRS_2001.4.pdf, World Heal. Organ.
Braña, A.F., Sarmiento-Vizcaíno, A., Pérez-Victoria, I., Martín, J., Otero, L., Palacios-Gutiérrez, J.J., Fernández, J., Mohamedi, Y., Fontanil, T., Salmón, M., Cal, S., Reyes, F., García, L.A., Blanco, G., 2019. Desertomycin G, a new antibiotic with activity against mycobacterium tuberculosis and human breast tumor cell lines produced by streptomyces althioticus MSM3, isolated from the cantabrian sea intertidal macroalgae ulva sp. Mar. Drugs. https://doi.org/10.3390/md17020114
Chaudhary, S., Kanwar, R.K., Sehgal, A., Cahill, D.M., Barrow, C.J., Sehgal, R., Kanwar, J.R., 2017. Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Front. Plant Sci. https://doi.org/10.3389/fpls.2017.00610
Chianese, G., Yerbanga, S.R., Lucantoni, L., Habluetzel, A., Basilico, N., Taramelli, D., Fattorusso, E., Taglialatela-Scafati, O., 2010. Antiplasmodial triterpenoids from the fruits of neem, Azadirachta indica. J. Nat. Prod. https://doi.org/10.1021/np100325q
Choi, S.S., Kim, H.J., Lee, H.S., Kim, P., Kim, E.S., 2015. Genome mining of rare actinomycetes and cryptic pathway awakening. Process Biochem. https://doi.org/10.1016/j.procbio.2015.04.008
Das, A., 2015. Anticancer effect of antimalarial artemisinin compounds. Ann. Med. Health Sci. Res. https://doi.org/10.4103/2141-9248.153609
Dobson, L.F., O’Cleirigh, C.C., O’Shea, D.G., 2008. The influence of morphology on geldanamycin production in submerged fermentations of Streptomyces hygroscopicus var. geldanus. Appl. Microbiol. Biotechnol. https://doi.org/10.1007/s00253-008-1493-3
Duru, V., Witkowski, B., Ménard, D., 2016. Review article plasmodium falciparum resistance to artemisinin derivatives and piperaquine: A major challenge for malaria elimination in Cambodia. Am. J. Trop. Med. Hyg. https://doi.org/10.4269/ajtmh.16-0234
Farida, Y., Widada, J., Meiyanto, E., 2007. Combination Methods for Screening Marine Actinomycetes Producing Potential Compounds as Anticancer. Indones. J. Biotechnol. 12, 988–997. https://doi.org/10.22146/ijbiotech.7772
Haldar, K., Bhattacharjee, S., Safeukui, I., 2018. Drug resistance in Plasmodium. Nat. Rev. Microbiol. 16, 156–170. https://doi.org/10.1038/nrmicro.2017.161
Hall, T., 2013. BioEdit version 7.2. 5. Ibis Biosci. Carlsbad, CA, USA.
Handayani, I., Ratnakomala, S., Lisdiyanti, P., Alanjary, M., Wohlleben, W., Mast, Y., 2018a. Complete Genome Sequence of Streptomyces sp. Strain BSE7F, a Bali Mangrove Sediment Actinobacterium with Antimicrobial Activities. https://doi.org/10.1128/genomeA.00618-18
Handayani, I., Ratnakomala, S., Lisdiyanti, P., Fahrurrozi, Kusharyoto, W., Alanjary, M., Ort-Winklbauer, R., Kulik, A., Wohlleben, W., Mast, Y., 2018b. Complete Genome Sequence of Streptomyces sp. Strain SHP22-7, a New Species Isolated from Mangrove of Enggano Island, Indonesia. Microbiol. Resour. Announc. https://doi.org/10.1128/mra.01317-18
Herdini, C., Hartanto, S., Mubarika, S., Hariwiyanto, B., Wijayanti, N., Hosoyama, A., Yamazoe, A., Nojiri, H., Widada, J., 2015. Diversity of Nonribosomal Peptide Synthetase Genes in the AnticancerProducing Actinomycetes Isolated from Marine Sediment in Indonesia. Indones. J. Biotechnol. 20, 34. https://doi.org/10.22146/ijbiotech.15266
Herdini, C., Mubarika, S., Hariwiyanto, B., Wijayanti, N., Hosoyama, A., Yamazoe, A., Nojiri, H., Widada, J., 2017. Secondary bioactive metabolite gene clusters identification of anticandida-producing streptomyces Sp. GMR22 isolated from Wanagama forest as revealed by Genome mining approach. Indones. J. Pharm. 28, 26–33. https://doi.org/10.14499/indonesianjpharm28iss1pp26
Intaraudom, C., Bunbamrung, N., Dramae, A., Danwisetkanjana, K., Rachtawee, P., Pittayakhajonwut, P., 2015. Antimalarial and antimycobacterial agents from Streptomyces sp. BCC27095. Tetrahedron Lett. 56, 6875–6877. https://doi.org/10.1016/j.tetlet.2015.10.098
Kautsar, S.A., Blin, K., Shaw, S., Weber, T., Medema, M.H., 2020. BiG-FAM: the biosynthetic gene cluster families database. Nucleic Acids Res. https://doi.org/10.1093/nar/gkaa812
Komaki, H., Sakurai, K., Hosoyama, A., Kimura, A., Igarashi, Y., Tamura, T., 2018. Diversity of nonribosomal peptide synthetase and polyketide synthase gene clusters among taxonomically close Streptomyces strains. Sci. Rep. https://doi.org/10.1038/s41598-018-24921-y
Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. https://doi.org/10.1093/molbev/msy096
Kumar, V., Bharti, A., Gusain, O., Bisht, G.S., 2011. Scanning electron microscopy of Streptomyces without use of any chemical fixatives. Scanning 33, 446–449. https://doi.org/10.1002/sca.20261
Low, Z.J., Pang, L.M., Ding, Y., Cheang, Q.W., Hoang, K.L.M., Tran, H.T., Li, J., Liu, X.W., Kanagasundaram, Y., Yang, L., Liang, Z.X., 2018. Identification of a biosynthetic gene cluster for the polyene macrolactam sceliphrolactam in a Streptomyces strain isolated from mangrove sediment. Sci. Rep. https://doi.org/10.1038/s41598-018-20018-8
Mbaba, M., de la Mare, J.A., Sterrenberg, J.N., Kajewole, D., Maharaj, S., Edkins, A.L., Isaacs, M., Hoppe, H.C., Khanye, S.D., 2019. Novobiocin–ferrocene conjugates possessing anticancer and antiplasmodial activity independent of HSP90 inhibition. J. Biol. Inorg. Chem. https://doi.org/10.1007/s00775-018-1634-9
Nurjasmi, R., Widada, J., 2009. Diversity of Actinomycetes at Several Forest Types in Wanagama I Yogyakarta and Their Potency as a Producer of Antifungal Compound. Indones. J. Biotechnol. 14, 1196–1205. https://doi.org/10.22146/ijbiotech.7813
Pereira, P.H.F., Macrae, A., Reinert, F., De Souza, R.F., Coelho, R.R.R., Pötter, G., Klenk, H.P., Labeda, D.P., 2017. Streptomyces odonnellii sp. Nov., a proteolytic streptomycete isolated from soil under cerrado (savanna) vegetation cover. Int. J. Syst. Evol. Microbiol. https://doi.org/10.1099/ijsem.0.002446
Sanz, L.M., Crespo, B., De-Cózar, C., Ding, X.C., Llergo, J.L., Burrows, J.N., García-Bustos, J.F., Gamo, F.J., 2012. P. falciparum in vitro killing rates allow to discriminate between different antimalarial mode-of-action. PLoS One 7. https://doi.org/10.1371/journal.pone.0030949
Seipke, R.F., 2015. Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS One. https://doi.org/10.1371/journal.pone.0116457
Sottorff, I., Wiese, J., Lipfert, M., Preußke, N., Sönnichsen, F.D., Imhoff, J.F., 2019. Different secondary metabolite profiles of phylogenetically almost identical streptomyces griseus strains originating from geographically remote locations. Microorganisms. https://doi.org/10.3390/microorganisms7060166
Sumanadasa, S.D.M., Goodman, C.D., Lucke, A.J., Skinner-Adams, T., Saham, I., Haque, A., Do, T.A., McFadden, G.I., Fairlie, D.P., Andrews, K.T., 2012. Antimalarial activity of the anticancer histone deacetylase inhibitor SB939. Antimicrob. Agents Chemother. 56, 3849–3856. https://doi.org/10.1128/AAC.00030-12
Tajuddeen, N., Van Heerden, F.R., 2019. Antiplasmodial natural products: An update. Malar. J. 18, 1–62. https://doi.org/10.1186/s12936-019-3026-1
Také, A., Matsumoto, A., Omura, S., Takahashi, Y., 2015. Streptomyces lactacystinicus sp. nov. and Streptomyces cyslabdanicus sp. nov., producing lactacystin and cyslabdan, respectively. J. Antibiot. (Tokyo). https://doi.org/10.1038/ja.2014.162
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. https://doi.org/10.1093/nar/25.24.4876
Trager, W., Jensen, J.B., 2005. Human malaria parasites in continuous culture. J. Parasitol. https://doi.org/10.1645/0022-3395(2005)091[0484:HMPICC]2.0.CO;2
Undabarrena, A., Ugalde, J.A., Seeger, M., Cámara, B., 2017. Genomic data mining of the marine actinobacteria Streptomyces sp. H-KF8 unveils insights into multi-stress related genes and metabolic pathways involved in antimicrobial synthesis. PeerJ 2017. https://doi.org/10.7717/peerj.2912
Werdyani, S., Wijayanti, N., Fitria, A., Rahmawati, S., 2017. Cytotoxic effects of ethyl acetate fractions from secondary metabolites of Streptomyces Sp. GMY01 on human breast cancer MCF7 cell lines. Asian J. Pharm. Clin. Res. 10, 9–11. https://doi.org/10.22159/ajpcr.2017v10s3.21351
Xu, H., Chater, K.F., Deng, Z., Tao, M., 2008. A cellulose synthase-like protein involved in hyphal tip growth and morphological differentiation in streptomyces. J. Bacteriol. https://doi.org/10.1128/JB.01849-07
Xu, L., Ye, K.X., Dai, W.H., Sun, C., Xu, L.H., Han, B.N., 2019. Comparative genomic insights into secondary metabolism biosynthetic gene cluster distributions of marine Streptomyces. Mar. Drugs. https://doi.org/10.3390/md17090498
Zhang, L., Wang, J., Li, T., Li, P., Wang, Y., Yang, M., Liu, Jin?Ping, Liu, Ji?Hua, 2019. Determination of the chemical components and phospholipids of velvet antler using UPLC/QTOF?MS coupled with UNIFI software. Exp. Ther. Med. 3789–3799. https://doi.org/10.3892/etm.2019.7372
Ziemert, N., Alanjary, M., Weber, T., 2016. The evolution of genome mining in microbes-a review. Nat. Prod. Rep. https://doi.org/10.1039/c6np00025h
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