Potential secondary metabolite biosynthetic gene clusters and antibacterial activity of novel taxa Gandjariella
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Abstract
Abstract. Ningsih F, Sari DCAF, Yabe S, Yokota A, Sjamsuridzal W. 2020. Potential secondary metabolite biosynthetic gene clusters and antibacterial activity of novel taxa Gandjariella. Biodiversitas 21: 5674-5684. Microbial resistance to available antibiotics has gained increasing attention in recent years and led to the urgent search for active secondary metabolites from novel microbial taxa. This study aimed to assess putative secondary metabolite biosynthetic gene clusters (BGCs) in the genome of a novel thermophilic Actinobacteria type strain Gandjariella thermophila SL3-2-4T and screen for its antibacterial activity. Four other related novel candidate Actinobacteria strains, isolated from forest soil in the Cisolok geothermal area (West Java, Indonesia), were also screened for antibacterial activity in various media solidified with gellan gum. The genome of the SL3-2-4T strain contained 21 antiSMASH-identified secondary metabolite regions harboring BGCs. These BGCs were for polyketide synthase, non-ribosomal peptide synthase, and ribosomally synthesized and post-translationally modified peptide family clusters. Three BGC regions displayed 50-100% similarity with known secondary metabolites. Thirteen and five regions displayed low (4-35%) and no similarity with known BGCs for secondary metabolites, respectively. Strains SL3-2-4T and SL3-2-7 on MM 2 medium solidified with gellan gum at 45 °C for 14 days demonstrated inhibitory activity against all Gram-positive, but not Gram-negative bacteria. Strain SL3-2-10 on ISP 3 gellan gum medium incubated for seven days only active against K. rhizophila NBRC 12078. Strains SL3-2-6 and SL3-2-9 did not exhibit any antibacterial activity against the tested bacterial strains on the three tested media. The results indicated that novel taxa have the potential for the discovery of active secondary metabolites.
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Aigle B, Lautru S, Spiteller D, Dickschat JS, Challis GL, Leblond P, Pernodet J-L. 2014. Genome mining of Streptomyces ambofaciens. J Ind Microbiol Biotechnol 41: 251–263. doi:10.1007/s10295-013-1379-y
Awakawa T, Fujita N, Hayakawa M, Ohnishi Y, Horinouchi S. 2011. Characterization of the biosynthesis gene cluster for alkyl-O-dihydrogeranyl-methoxyhydroquinones in Actinoplanes missouriensis. Chembiochem 12 (3): 439–448. doi:10.1002/cbic.201000628
Balouiri M, Sadiki M, Ibnsouda SK. 2016. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 6 (2): 71–79. doi:10.1016/j.jpha.2015.11.005
Baltz RH. 2008. Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8: 557–563. doi:10.1016/j.coph.2008.04.008
Baltz RH. 2017. Gifted microbes for genome mining and natural product discovery. J Ind Microbiol Biotechnol 44: 573–588. doi:10.1007/s10295-016-1815-x
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19 (5): 455–477. doi:10.1089/cmb.2012.0021
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, Clement C, Ouhdouch Y, van Wezel GP. 2016. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80 (1): 1-43. doi:10.1128/MMBR.00019-15
Bassi CA, Benson DR. 2007. Growth characteristics of the slow-growing actinobacterium Frankia sp. strain CcI3 on solid media. Physiol Plant 130 (3): 391–399. doi:10.1111/j.1399-3054.2007.00866.x
Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417 (6885): 141–147. doi:10.1038/417141a
Bérdy, J. 2012. Thoughts and facts about antibiotics: Where we are now and where we are heading. J Antibiot 65: 385–395. doi:10.1038/ja.2012.27
Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, et al. 2017. antiSMASH 4.0 – Improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res 45: W36–W41. doi:10.1093/nar/gkx319
Bode HB, Bethe B, Hofs R, Zeeck A. 2002. Big effects from small changes: possible ways to explore nature’s chemical diversity. Chembiochemistry 3: 619–627. doi:10.1002/1439-7633(20020703)3:7<619:AID-CBIC619>3.0.CO;2-9
Chen LY, Lai YM, Yang YL, Zhao XQ. 2016. Genome mining reveals the biosynthetic potential of the marine derived strain Streptomyces marokkonensis M10. Synth Syst Biotechnol 1: 56–65. doi:10.1016/j.synbio.2016.02.005
Dai H-Q, Wang J, Xin Y-H, Pei G, Tang S-K, Ren B, Ward A, Ruan J-S, Li W-J, Zhang L-X. 2010. Verrucosispora sediminis sp. nov., a cyclodipeptide-producing actinomycete from deep-sea sediment. Int J Syst Evol Microbiol 60 (8): 1807–1812. doi:10.1099/ijs.0.017053-0
Das N, Tripathi N, Basu S, Bose C, Maitra S, Khurana S. 2015. Progress in the development of gelling agents for improved culturability of microorganisms. Front Microbiol 6: 698. doi: 10.3389/fmicb.2015.00698
Donadio S, Monciardinia P, Sosio M. 2007. Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24: 1073–1109. doi:10.1039/B514050C
El-Naggar N, El-Ewasy S. 2017. Bioproduction, characterization, anticancer and antioxidant activities of extracellular melanin pigment produced by newly isolated microbial cell factories Streptomyces glaucescens NEAE-H. Sci Rep 7: 42129. doi:10.1038/srep42129
Eustáquio A, Ziemert N. 2018. Identification of natural product biosynthetic gene clusters from bacterial genomic data. Methods Pharmacol Toxicol: 1–21. doi:10.1007/7653_2018_32
Fischbach MA, Walsh CT. 2006. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics:? Logic, machinery, and mechanisms. Chem Rev 106 (8): 3468–3496. doi:10.1021/cr0503097
Funabashi M, Nonaka K, Yada C, Hosobuchi M, Masuda N, Shibata T, van Lanen SG. 2009. Identification of the biosynthetic gene cluster of A-500359s in Streptomyces griseus SANK60196. J Antibiot (Tokyo) 62 (6): 325–332. doi:10.1038/ja.2009.38
Gao G, Liu X, Xu M, Wang Y, Zhang F, et al. 2017. Formation of an angular aromatic polyketide from a linear anthrene precursor via oxidative rearrangement. Cell Chem Biol 24 (7): 881–891.e4. doi:10.1016/jchembiol.2017.06.008
Genilloud O. 2017. Actinomycetes: still a source of novel antibiotics. Natural Product Reports 34 (10): 1203–1232. doi:10.1039/c7np00026j
Gonzalez-Burgos E, Gomez-Serranillos MP. 2012. Terpene compounds in nature: A review of their potential antioxidant activity. Curr Med Chem 19 (3): 5319-5341. doi:10.2174/092986712803833335
Grant JR, Stothard P. 2008. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36: W181–W184. doi:10.1093/nar/gkn179
Hamedi J, Wink J. 2017. Introduction. In Wink, J., F. Mohammadipanah & J. Hamedi (eds.). Biology and biotechnology of Actinobacteria. Springer International Publishing AG, Switzerland: 5–28.
Hamedi J, Poorinmohammad N, Wink J. 2017. The Role of Actinobacteria in Biotechnology. In Wink J, Mohammadipanah F, Hamedi J (eds.). Biology and Biotechnology of Actinobacteria. Springer International Publishing AG, Switzerland: 269–328.
Hatsu M, Sasaki T, Gomi S, Kodama Y, Sezaki M, Inouye S, Kondo S. 1992. A new tetracycline antibiotic with antitumor activity. I. Taxonomy and fermentation of the producing strain, isolation and characterization of SF2575. J Antibiot (Tokyo) 45 (3): 320–324. doi:10.7164/antibiotics.45.320
Hopwood DA. 1967. Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol Rev 31 (4): 373–403.
Hopwood DA, Sermonti, G. 1963. The genetics of Streptomyces coelicolor. Adv Genet: 273–342. doi:10.1016/s0065-2660(08)60289-8
Hu Y, Phelan V, Ntai I, Farnet CM, Zazopoulos E, Bachmann BO. 2007. Benzodiazepine biosynthesis in Streptomyces refuineus. Chem Biol 14: 691–701. doi:10.1016/j.chembiol.2007.05.009
Huang H, Yao Y, He Z, Yang T, Ma J, Tian X, Li Y, Huang C, Chen X, Li W, Zhang S, Zhang C, Ju J. 2011. Antimalarial ?-carboline and indolactam alkaloids from Marinactinospora thermotolerans, a deep sea isolate. J Nat Prod 74: 2122–2127. doi:10.1021/np200399t
Igarashi Y, Trujillo M, Martínez-Molina E, Yanase S, Miyanaga S, Obata T, Sakurai H, Saiki I, Fujita T, Furumai T. 2007. Antitumor anthraquinones from an endophytic actinomycete Micromonospora lupini sp. nov. Bioorg Med Che. Lett 17: 3702?3705. doi:10.1016/j.bmcl.2007.04.039
Iorio M, Cruz J, Simone M, Bernasconi A, Brunati C, Sosio M, Donadio S, Maffioli SI. 2017. Antibacterial paramagnetic quinones from Actinoallomurus. J Nat Prod 80 (4): 819–827. doi:10.1021/acsjnatprod.6b00654
Ivanova V, Laatsch H, Kolarova M, Aleksieva K. 2013. Structure elucidation of a new natural diketopiperazine from a Microbispora aerata strain isolated from Livingston Island, Antarctica. Nat Prod Lett 27: 164–170. doi:10.1080/14786419.2012.665911
Kersten RD, Lane AL, Nett M, Richter TKS, Duggan BM, Dorrestein PC, Moore BS. 2013. Bioactivity-guided genome mining reveals the lomaiviticin biosynthetic gene cluster in Salinispora tropica. Chembiochem 14 (8): 955–962. doi:10.1002/cbic.201300147
Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, UK.
Kurtböke DI. 2012. Biodiscovery from rare actinomycetes: an eco-taxonomical perspective. Appl Microbiol Biotechnol 93 (5): 1843–1852. doi:10.1007/s00253-012-3898-2
Lackner G, Schenk A, Xu Z, Reinhardt K, Yunt ZS, Piel J, Hertweck C. 2007. Biosynthesis of pentangular polyphenols: deductions from the benastatin and griseorhodin pathways. J Am Chem Soc 129 (30): 9306–9312. doi:10.1021/ja0718624
Li A, Piel J. 2002. A gene cluster from a marine Streptomyces encoding the biosynthesis of the aromatic spiroketal polyketide griseorhodin A. Chem Biol 9 (9): 1017–1026. doi:10.1016/s1074-5521(02)00223-5
Li L, Wang P, Tang Y. 2014. C-glycosylation of anhydrotetracycline scaffold with SsfS6 from the SF2575 biosynthetic pathway. J Antibiot (Tokyo) 67 (1): 65-70. doi:10.1038/ja.2013.88
Liu Y, Li M, Mu H, Song S, Zhang Y, Chen K, He X, Wang H, Dai Y, Lu F, Yan Z, Zhang H. 2017. Identification and characterization of the ficellomycin biosynthesis gene cluster from Streptomyces ficellus. Appl Microbiol Biotechnol 101 (20): 7589-7602. doi:10.1007/s00253-017-8465-4
Liu WT, Lamsa A, Wong WR, Boudreau PD, Kersten R, Peng Y, Moree WJ, Duggan BM, Moore BS, Gerwick WH, Linington RG, Pogliano K, Dorrestein PC. 2014. MS/MS-based networking and peptidogenomics guided genome mining revealed the stenothricin gene cluster in Streptomyces roseosporus. J Antibiot (Tokyo) 67 (1): 99–104. doi:10.1038/ja.2013.99
Lopez P, Hornung A, Welzel K, Unsin C, Wohlleben W, Weber T, Pelzer S. 2010. Isolation of the lysolipin gene cluster of Streptomyces tendae Tü 4042. Gene 461 (1–2): 5–14. doi:10.1016/jgene.2010.03.016
Matsuda K, Hasebe F, Shiwa Y, Kanesaki Y, Tomita T, Yoshikawa H, Shin-ya K, Kuzuyama T, Nishiyama M. 2017. Genome mining of amino group carrier protein-mediated machinery: Discovery and biosynthetic characterization of a natural product with unique hydrazone unit. ACS Chem Biol 12 (1): 124–131. doi:10.1021/acschembio.6b00818
Mohammadipanah F, Dehhaghi M. 2017. Classification and taxonomy of Actinobacteria. In Wink J, Mohammadipanah F, Hamedi J (eds.). Biology and Biotechnology of Actinobacteria. Springer International Publishing AG, Switzerland: 51–77.
Ningsih F, Yokota A, Sakai Y, Nanatani K, Yabe S, Oetari A, Sjamsuridzal W. 2019. Gandjariella thermophila gen. nov., sp. nov., a new member of the family Pseudonocardiaceae, isolated from forest soil in a geothermal area. Int J Syst Evol Microbiol 69 (10): 3080–3086. doi.org/10.1099/ijsem.0.003594
Niu G. 2018. Genomics-driven natural product discovery in actinomycetes. Trends Biotechnol 36 (3): 238–241. doi:10.1016/j.tibtech.2017.10.009
?mura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, et al. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: Deducing the ability of producing secondary metabolites. Proc Natl Acad Sci U S A 98 (21): 12215–12220. doi:10.1073/pnas.211433198
Onaka H, Nakaho M, Hayashi K, Igarashi Y, Furumai T. 2005. Cloning and characterization of the goadsporin biosynthetic gene cluster from Streptomyces sp. TP-A0584. Microbiology (Reading) 151 (Pt 12): 3923–3933. doi:10.1099/mic.0.28420-0
Pan R, Bai X, Chen J, Zhang H and Wang H. 2019. Exploring structural diversity of microbe secondary metabolites using OSMAC strategy: A literature review. Front Microbiol 10: 294. doi:10.3389/fmicb.2019.00294
Pickens LB, Kim W, Wang P, Zhou H, Watanabe K, Gomi S, Tang Y. 2009. Biochemical analysis of the biosynthetic pathway of an anticancer tetracycline SF2575. J Am Chem Soc 131 (48): 17677–17689. doi:10.1021/ja907852c
Pickens LB, Sawaya MR, Rasool H, Pashkov I, Yeates TO, Tang Y. 2011. Structural and biochemical characterization of the salicylyl-acyltranferase SsfX3 from a tetracycline biosynthetic pathway. J Biol Chem 286 (48): 41539–41551. doi:10.1074/jbc.M111.299859
Prabhu J, Schauwecker F, Grammel N, Keller U, Bernhard M. 2004. Functional expression of the ectoine hydroxylase gene (thpD) from Streptomyces chrysomallus in Halomonas elongata. Appl Environ Microbiol 70 (5): 3130–3132. doi:10.1128/aem.70.5.3130-3132.2004
Rabe P, Citron CA, Dickschat JS. 2013, Volatile terpenes from actinomycetes: A biosynthetic study correlating chemical analyses to genome data. ChemBioChem, 14: 2345-2354. doi:10.1002/cbic.201300329
Redenbach M, Kieser HM, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood DA. 1996. A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21 (1): 77–96. doi:10.1046/j.1365-2958.1996.6191336x
Rutledge PJ, Challis GL. 2015. Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nat Rev Microbiol 13: 509–523. doi: 10.1038/nrmicro3496
Sari DCAF, Ningsih F, Yokota A, Yabe S, Sjamsuridzal W, Oetari A. 2020. IOP Conf Ser: Earth Environ Sci 483: 012017. doi:10.1088/1755-1315/483/1/012017
Shirling ET, Gottlieb D. 1966. Methods for characterization of Streptomyces species. Intl J Syst Bacteriol 16 (3): 313–340.
Solecka J, Zajko J, Postek M, Rajnisz A. 2012. Biologically active secondary metabolites from actinomycetes. Cent Eur J Biol 7 (3): 373–390. doi:10.2478/s11535-012-0036-1
Strobel T, Al-Dilaimi A, Blom J. Gessner A, Kalinowski J, Luzhetska M, Pühler A, Szczepanowski R, Bechthold A, Rückert C. 2012. Complete genome sequence of Saccharothrix espanaensis DSM 44229T and comparison to the other completely sequenced Pseudonocardiaceae. BMC Genomics 13: 465. doi:10.1186/1471-2164-13-465
Sun L, Wang S, Zhang S, Shao L, Zhang Q, Skidmore C, Chang C-WT, Yu D, Zhan J. 2016. Characterization of three tailoring enzymes in dutomycin biosynthesis and generation of a potent antibacterial analogue. ACS Chem Biol 11 (7): 1992–2001. doi:10.1021/acschembio.6b00245
Suzuki S. 2001. Establishment and use of gellan gum media for selective isolation and distribution survey of specific rare actinomycetes. Actinomycetologica 15 (2): 55–60. doi:10.3209/saj.15_55
Tanizawa Y, Fujisawa T, Nakamura Y. 2018. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34: 1037–1039. doi: 10.1093/bioinformatics/btx713
Tian X-P, Long L-J, Li S-M, Zhang J, Xu Y, He J, Li J, Wang F-Z, Li W-J, Zhang C-S, Zhang S. 2013. Pseudonocardia antitumoralis sp. nov., a deoxynyboquinone-producing actinomycete isolated from a deep-sea sediment. Int J Syst Evol Microbiol 63: 893–899. doi:10.1099/ijs.0.037135-0
Tiwari K, Gupta RK. 2012. Rare actinomycetes: a potential storehouse for novel antibiotics. Crit Rev Biotechnol 32 (2): 108–132. doi:10.3109/07388551.2011.562482
Yabe S, Aiba Y, Sakai Y, Hazaka M, Yokota A. 2010. Thermosporothrix hazakensis gen. nov., sp. nov., isolated from compost, description of Thermosporotrichaceae fam. nov. within the class Ktedonobacteria Cavaletti et al. 2007 and emended description of the class Ktedonobacteria. Int J Syst Evol Microbiol 60: 1794–1801. doi: 10.1099/ijs.0.018069-0
Yokota A, Ningsih F, Nurlaili DG, Sakai Y, Yabe S, Oetari A, Santoso I, Sjamsuridzal W. 2016. Paenibacillus cisolokensis sp. nov., isolated from litter of a geyser. Int J Syst Evol Microbiol 66: 3088–3094. doi:10.1099/ijsem.0.001151
Yunt Z, Reinhardt K, Li A, Engeser M, Dahse H-M, Gütschow M, Bruhn T, Bringmann G, Piel J. 2009. Cleavage of four carbon-carbon bonds during biosynthesis of the griseorhodin a spiroketal pharmacophore. J Am Chem Soc 131 (6): 2297–2305. doi:10.1021/ja807827k
Zhang X, Parry RJ. 2007. Cloning and characterization of the pyrrolomycin biosynthetic gene clusters from Actinosporangium vitaminophilum ATCC 31673 and Streptomyces sp. strain UC 11065. Antimicrob Agents Chemother 51 (3): 946–957. doi:10.1128/AAC.01214-06
Zhang Q, Doroghazi JR, Zhao X, Walker MC, van der Donk WA. 2015. Expanded natural product diversity revealed by analysis of lanthipeptide-like gene clusters in Actinobacteria. Appl Environ Microbiol 81 (13): 4339–4350. doi:10.1128/AEM.00635-15
Zheng Y, Saitou A, Wang C-M, Toyoda A, Minakuchi Y, Sekiguchi Y, Ueda K, Takano H, Sakai Y, Abe K, Yokota A, Yabe S. 2019. Genome Features and Secondary Metabolites Biosynthetic Potential of the Class Ktedonobacteria. Front Microbiol 10: 893. doi: 10.3389/fmicb.2019.00893
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