Culturable endophytes diversity isolated from Paeonia ostii and the genetic basis for their bioactivity

• Autorzy: Yang R.-H. , Zhang S.-W. , Xue D. , Xuan J.-H. , Zhang Y.-B. , Peng B.-B.
• Języki publikacji: EN

Abstrakty

EN

Paeonia ostii is known for its excellent medicinal values as Chinese traditional plant. To date, the diversity of culturable endophytes associated with P. ostii is in its initial phase of exploration. In this study, 56 endophytic bacteria and 51 endophytic fungi were isolated from P. ostii roots in China. Subsequent characterization of 56 bacterial strains by 16S rDNA gene sequence analysis revealed that nine families and 13 different genera were represented. All the fungal strains were classed into six families and 12 genera based on ITS gene sequence. The biosynthetic potential of all the endophytes was further investigated by the detection of putative polyketide synthase (PKS) and nonribosomal peptide synthetase (NRPS) genes. The PCR screens were successful in targeting thirteen bacterial PKS, five bacterial NRPS, ten fungal PKS and nine fungal NRPS gene fragments. Bioinformatic analysis of these detected endophyte gene fragments facilitated inference of the potential bioactivity of endophyte bioactive products, suggesting that the isolated endophytes are capable of producing a plethora of secondary metabolites. These results suggest that endophytes isolated from P. ostii had abundant population diversity and biosynthetic potential, which further proved that endophytes are valuable reservoirs of novel bioactive compounds.

Słowa kluczowe

EN

endophyte; diversity; Paeonia ostii; medicinal property; China; medicinal plant; bioactivity

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2018
• Tom: 67
• Numer: 4
• Opis fizyczny: p.441-453,fig.,ref.

Twórcy

autor

Yang R.-H.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

autor

Zhang S.-W.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

autor

Xue D.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

autor

Xuan J.-H.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

autor

Zhang Y.-B.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

autor

Peng B.-B.

• Department of Environmental Engineering and Chemistry, Luoyang Institute of Science and Technology, Luoyang, P.R.China

Bibliografia

• Akinsanya MA, Goh JK, Lim SP, Ting ASY. 2015. Diversity, antimicrobial and antioxidant activities of culturable bacterial endophyte communities in Aloe vera. FEMS Microbiol Lett. 362(23):fnv184.
• Aleti G, Sessitsch A, Brader G. 2015. Genome mining: Prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Comput Struct Biotechnol J. 13:192–203.
• Aly AH, Debbab A, Proksch P. 2011. Fifty years of drug discovery from fungi. Fungal Divers. 50(1):3–19.
• Amnuaykanjanasin A, Punya J, Paungmoung P, Rungrod A, Tachaleat A, Pongpattanakitshote S, Cheevadhanarak S, Tanticharoen M. 2005. Diversity of type I polyketide synthase genes in the wood-decay fungus Xylaria sp. BCC 1067. FEMS Microbiol Lett. 251(1):125–136.
• Amoutzias G, Chaliotis A, Mossialos D. 2016. Discovery strategies of bioactive compounds synthesized by nonribosomal peptide synthetases and type-I polyketide synthases derived from marine microbiomes. Mar Drugs. 14(4):80.
• Ayuso-Sacido A, Genilloud O. 2005. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol. 49(1):10–24.
• Bais HP, Fall R, Vivanco JM. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134(1):307–319.
• Banerjee D. 2011. Endophytic fungal diversity in tropical and subtropical plants. Res J Microbiol. 6(1):54–62.
• Brady SF, Clardy J. 2000. CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J Nat Prod. 63(10):1447–1448.
• Brown DW, Butchko RAE, Busman M, Proctor RH. 2012. Identification of gene clusters associated with fusaric acid, fusarin, and perithecial pigment production in Fusarium verticillioides. Fungal Genet Biol. 49(7):521–532.
• Burja AM, Banaigs B, Abou-Mansour E, Grant Burgess J, Wright PC. 2001. Marine cyanobacteria – a prolific source of natural products. Tetrahedron. 57(46):9347–9377.
• Bushley KE, Turgeon BG. 2010. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol. 10(1):26.
• Butcher RA, Schroeder FC, Fischbach MA, Straight PD, Kolter R, Walsh CT, Clardy J. 2007. The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. Proc Natl Acad Sci USA. 104(5):1506–1509.
• Chen G, Zhang L, Zhu Y. Determination of glycosides and sugars in Moutan Cortex by capillary electrophoresis with electrochemical detection. J Pharm Biomed Anal. 2006a 41(1):129–134.
• Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, et al. 2006b. Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol. 188(11):4024–4036.
• Cohen SD. 2006. Host selectivity and genetic variation of Discula umbrinella isolates from two oak species: analyses of intergenic spacer region sequences of ribosomal DNA. Microb Ecol. 52(3):463–469.
• Crawford JM, Korman TP, Labonte JW, Vagstad AL, Hill EA, Kamari-Bidkorpeh O, Tsai SC, Townsend CA. 2009. Structural basis for biosynthetic programming of fungal aromatic polyketide cyclization. Nature. 461(7267):1139–1143.
• Cui JL, Guo TT, Ren ZX, Zhang NS, Wang ML. 2015. Diversity and antioxidant activity of culturable endophytic fungi from alpine plants of Rhodiola crenulata, R. angusta, and R. sachalinensis. PLoS One. 10(3):e0118204.
• Deshmukh SK, Verekar SA, Bhave SV. 2015. Endophytic fungi: a reservoir of antibacterials. Front Microbiol. 5:715.
• Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G. 2017. Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol. 8:199.
• El-Deeb B, Fayez K, Gherbawy Y. 2013. Isolation and characterization of endophytic bacteria from Plectranthus tenuiflorus medicinal plant in Saudi Arabia desert and their antimicrobial activities. J Plant Interact. 8(1):56–64.
• Evans BS, Robinson SJ, Kelleher NL. 2011. Surveys of non-ribosomal peptide and polyketide assembly lines in fungi and prospects for their analysis in vitro and in vivo. Fungal Genet Biol. 48(1):49–61.
• Fewer DP, Österholm J, Rouhiainen L, Jokela J, Wahlsten M, Sivonen K. 2011. Nostophycin biosynthesis is directed by a hybrid polyketide synthase-nonribosomal peptide synthetase in the toxic cyanobacterium Nostoc sp. strain 152. Appl Environ Microbiol. 77(22):8034–8040.
• Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. 2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31(13):3784–3788.
• Gond SK, Mishra A, Sharma VK, Verma SK, Kumar J, Kharwar RN, Kumar A. 2012. Diversity and antimicrobial activity of endophytic fungi isolated from Nyctanthes arbor-tristis, a well-known medicinal plant of India. Mycoscience. 53(2):113–121.
• Gong B, Yao XH, Zhang YQ, Fang HY, Pang TC, Dong QL. 2015. A cultured endophyte community is associated with the plant Clerodendrum inerme and antifungal activity. Genet Mol Res. 14(2):6084–6093.
• Guo LD, Huang GR, Wang Y, He WH, Zheng WH, Hyde KD. 2003. Molecular identification of white morphotype strains of endophytic fungi from Pinus tabulaeformis. Mycol Res. 107(6):680–688.
• Hajjaj H, Niederberger P, Duboc P. 2001. Lovastatin biosynthesis by Aspergillus terreus in a chemically defined medium. Appl Environ Microbiol. 67(6):2596–2602.
• Heuer H, Krsek M, Baker P, Smalla K, Wellington EM. 1997. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 63(8):3233–3241.
• Huang Y, Cai Y, Hyde K, Corke H, Sun M. 2008. Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Divers. 33:61.
• Kasahara K, Fujii I, Oikawa H, Ebizuka Y. 2006. Expression of Alternaria solani PKSF generates a set of complex reduced-type polyketides with different carbon-lengths and cyclization. Chem-BioChem. 7(6):920–924.
• Lam KS. 2006. Discovery of novel metabolites from marine actinomycetes. Curr Opin Microbiol. 9(3):245–251.
• Lau CH, Chan CM, Chan YW, Lau KM, Lau TW, Lam FC, Law WT, Che CT, Leung PC, Fung KP, et al. 2007. Pharmacological investigations of the anti-diabetic effect of Cortex Moutan and its active component paeonol. Phytomedicine. 14(11):778–784.
• Liao HL, Chung KR. 2008. Genetic dissection defines the roles of elsinochrome Phytotoxin for fungal pathogenesis and conidiation of the citrus pathogen Elsinoë fawcettii. Mol Plant Microbe Interact. 21(4):469–479.
• Liu H., J. Guo, N. Salam, L. Li, Y. Zhang, J. Han, O. Mohamad and W. Li. 2016. Culturable endophytic bacteria associated with medicinal plant Ferula songorica: molecular phylogeny, distribution and screening for industrially important traits. 3 Biotech. 6:209.
• Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K. 1999. An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett. 180(1):1–6.
• Moffitt MC, Neilan BA. 2001. On the presence of peptide synthetase and polyketide synthase genes in the cyanobacterial genus Nodularia. FEMS Microbiol Lett. 196(2):207–214.
• Mongkolthanaruk W. 2012. Classification of Bacillus beneficial substances related to plants, humans and animals. J Microbiol Biotechnol. 22(12):1597–1604.
• Nair DN, Padmavathy S. 2014. Impact of endophytic microorganisms on plants, environment and humans. Sci World J. 2014:1–11.
• Nikolouli K, Mossialos D. 2012. Bioactive compounds synthesized by non-ribosomal peptide synthetases and type-I polyketide synthases discovered through genome-mining and metagenomics. Biotechnol Lett. 34(8):1393–1403.
• Nimnoi P, Pongsilp N, Lumyong S. 2010. Endophytic actinomycetes isolated from Aquilaria crassna Pierre ex Lec and screening of plant growth promoters production. World J Microbiol Biotechnol. 26(2):193–203.
• Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA. 2015. Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: A review. Microb Pathog. 82: 50–59.
• Ongena M, Jacques P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16(3):115–125.
• Passari AK, Mishra VK, Gupta VK, Saikia R, Singh BP. 2016. Distribution and identification of endophytic Streptomyces species from Schima wallichii as potential biocontrol agents against fungal plant pathogens. Pol J Microbiol. 65(3):319–329.
• Potshangbam M, Devi SI, Sahoo D, Strobel GA. 2017. Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Front Microbiol. 8:325.
• Qiu F, Huang Y, Sun L, Zhang X, Liu Z, Song W. 2007. Leifsonia ginsengi sp. nov., isolated from ginseng root. Int J Syst Evol Microbiol. 57(2):405–408.
• Raviraja NS. 2005. Fungal endophytes in five medicinal plant species from Kudremukh Range, Western Ghats of India. J Basic Microbiol. 45(3):230–235.
• Raviraja NS, Maria GL, Sridhar KR. 2006. Antimicrobial evaluation of endophytic fungi inhabiting medicinal plants of the western ghats of India. Eng Life Sci. 6(5):515–520.
• Röttig M, Medema MH, Blin K, Weber T, Rausch C, Kohlbacher O. 2011. NRPSpredictor2--a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 39(Web Server issue): W362-7.
• Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. 2016. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int. 23(5):3984–3999.
• Sauer M, Lu P, Sangari R, Kennedy S, Polishook J, Bills G, An Z. 2002. Estimating polyketide metabolic potential among nonsporulating fungal endophytes of Vaccinium macrocarpon. Mycol Res. 106(4):460–470.
• Silva-Hughes AF, Wedge DE, Cantrell CL, Carvalho CR, Pan Z, Moraes RM, Madoxx VL, Rosa LH. 2015. Diversity and antifungal activity of the endophytic fungi associated with the native medicinal cactus Opuntia humifusa (Cactaceae) from the United States. Microbiol Res. 175:67–77.
• Slightom JL, Metzger BP, Luu HT, Elhammer AP. 2009. Cloning and molecular characterization of the gene encoding the Aureobasidin A biosynthesis complex in Aureobasidium pullulans BP-1938. Gene. 431(1–2):67–79.
• Starai VJ, Escalante-Semerena JC. 2004. Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci. 61(16):2020–2030.
• Strieker M, Tanović A, Marahiel MA. 2010. Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol. 20(2):234–240.
• Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28(10):2731–2739.
• Tobiasen C, Aahman J, Ravnholt KS, Bjerrum MJ, Grell MN, Giese H. 2006. Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet. 51(1):43–58.
• Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H. 2013. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev. 37(1):44–66.
• Venugopalan A, Srivastava S. 2015. Endophytes as in vitro production platforms of high value plant secondary metabolites. Biotechnol Adv. 33(6):873–887.
• Wang X, Wang H, Liu T, Xin Z. 2014. A PKS I gene-based screening approach for the discovery of a new polyketide from Penicillium citrinum Salicorn 46. Appl Microbiol Biotechnol. 98(11):4875–4885.
• Wang Y, Dai CC. 2011. Endophytes: a potential resource for biosynthesis, biotransformation, and biodegradation. Ann Microbiol. 61(2):207–215.
• Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S. 2015. Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol. 99(7):2955–2965.
• White J, Bruns T, Lee S, Taylor J. 1990. Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. PCR protocols: a guide to methods and applications. New York (USA): Academic Press. p. 315–322.
• Wu X, Monchy S, Taghavi S, Zhu W, Ramos J, van der Lelie D. 2011. Comparative genomics and functional analysis of nichespecific adaptation in Pseudomonas putida. FEMS Microbiol Rev. 35(2):299–323.
• Zhou K, Zhang X, Zhang F, Li Z. 2011. Phylogenetically diverse cultivable fungal community and polyketide synthase (PKS), nonribosomal peptide synthase (NRPS) genes associated with the South China Sea sponges. Microb Ecol. 62(3):644–654.

Identyfikatory

DOI

10.21307/pjm-2018-052