Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin.

Jahn L, Schafhauser T, Wibberg D, Rückert C, Winkler A, Kulik A, Weber T, Flor L, van Pée K-H, Kalinowski J, Ludwig-Müller J, et al. (2017)
Journal of Biotechnology 257: 233-239.

Zeitschriftenaufsatz | Veröffentlicht| Englisch
 
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Autor*in
Jahn, Linda; Schafhauser, Thomas; Wibberg, DanielUniBi; Rückert, ChristianUniBi ; Winkler, AnikaUniBi; Kulik, Andrea; Weber, Tilman; Flor, Liane; van Pée, Karl-Heinz; Kalinowski, JörnUniBi; Ludwig-Müller, Jutta; Wohlleben, Wolfgang
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Abstract / Bemerkung
Fungal aromatic polyketides display a very diverse and widespread group of natural products. Due to their excellent light absorption properties and widely studied biological activities, they offer numerous application for food, textile and pharmaceutical industry. The biosynthetic pathways of fungal aromatic polyketides usually involve a set of successive enzymes, in which a non-reductive polyketide synthase iteratively catalyzes the essential assembly of simple building blocks into (often polycyclic) aromatic compounds. However, only a limited number of such pathways have been described so far and further elucidation of the individual biosynthetic steps is needed to fully exploit the biotechnological and medicinal potential of these compounds. Here, we identified the bisanthraquinone skyrin as the main pigment of the fungus Cyanodermella asteris, an endophyte that has recently been isolated from the traditional Chinese medicinal plant Aster tataricus. The genome of C. asteris was sequenced, assembled and annotated, which enables first insights into a genome from a non-lichenized member of the class Lecanoromycetes. Genetic and in silico analyses led to the identification of a gene cluster of five genes suggested to encode the enzymatic pathway for skyrin. Our study is a starting point for rational pathway engineering in order to drive the production towards higher yields or more active derivatives. Moreover, our investigations revealed a large potential of secondary metabolite production in C. asteris as well as in all Lecanoromycetes of which genomes were available. These findings convincingly emphasize that Lecanoromycetes are prolific producers of secondary metabolites.
Erscheinungsjahr
2017
Zeitschriftentitel
Journal of Biotechnology
Band
257
Seite(n)
233-239
ISSN
0168-1656
eISSN
1873-4863
Page URI
https://pub.uni-bielefeld.de/record/2913403

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Jahn L, Schafhauser T, Wibberg D, et al. Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. Journal of Biotechnology. 2017;257:233-239.
Jahn, L., Schafhauser, T., Wibberg, D., Rückert, C., Winkler, A., Kulik, A., Weber, T., et al. (2017). Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. Journal of Biotechnology, 257, 233-239. doi:10.1016/j.jbiotec.2017.06.410
Jahn, L., Schafhauser, T., Wibberg, D., Rückert, C., Winkler, A., Kulik, A., Weber, T., Flor, L., van Pée, K. - H., Kalinowski, J., et al. (2017). Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. Journal of Biotechnology 257, 233-239.
Jahn, L., et al., 2017. Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. Journal of Biotechnology, 257, p 233-239.
L. Jahn, et al., “Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin.”, Journal of Biotechnology, vol. 257, 2017, pp. 233-239.
Jahn, L., Schafhauser, T., Wibberg, D., Rückert, C., Winkler, A., Kulik, A., Weber, T., Flor, L., van Pée, K.-H., Kalinowski, J., Ludwig-Müller, J., Wohlleben, W.: Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin. Journal of Biotechnology. 257, 233-239 (2017).
Jahn, Linda, Schafhauser, Thomas, Wibberg, Daniel, Rückert, Christian, Winkler, Anika, Kulik, Andrea, Weber, Tilman, Flor, Liane, van Pée, Karl-Heinz, Kalinowski, Jörn, Ludwig-Müller, Jutta, and Wohlleben, Wolfgang. “Linking secondary metabolites to biosynthesis genes in the fungal endophyte Cyanodermella asteris: The anti-cancer bisanthraquinone skyrin.”. Journal of Biotechnology 257 (2017): 233-239.

3 Zitationen in Europe PMC

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Date Palm Trees Root-Derived Endophytes as Fungal Cell Factories for Diverse Bioactive Metabolites.
Ben Mefteh F, Daoud A, Chenari Bouket A, Thissera B, Kadri Y, Cherif-Silini H, Eshelli M, Alenezi FN, Vallat A, Oszako T, Kadri A, Ros-García JM, Rateb ME, Gharsallah N, Belbahri L., Int J Mol Sci 19(7), 2018
PMID: 29986518
Phenotyping the genus Hypericum by secondary metabolite profiling: emodin vs. skyrin, two possible key intermediates in hypericin biosynthesis.
Kimáková K, Kimáková A, Idkowiak J, Stobiecki M, Rodziewicz P, Marczak Ł, Čellárová E., Anal Bioanal Chem 410(29), 2018
PMID: 30291388

51 References

Daten bereitgestellt von Europe PubMed Central.

Exploration of industrially important pigments from soil fungi.
Akilandeswari P, Pradeep BV., Appl. Microbiol. Biotechnol. 100(4), 2015
PMID: 26701360
Sorokiniol: a new enzymes inhibitory metabolite from fungal endophyte Bipolaris sorokiniana LK12.
Ali L, Khan AL, Hussain J, Al-Harrasi A, Waqas M, Kang SM, Al-Rawahi A, Lee IJ., BMC Microbiol. 16(), 2016
PMID: 27277006
Antimicrobial Potential of Thiodiketopiperazine Derivatives Produced by Phoma sp., an Endophyte of Glycyrrhiza glabra Linn.
Arora P, Wani ZA, Nalli Y, Ali A, Riyaz-Ul-Hassan S., Microb. Ecol. 72(4), 2016
PMID: 27357141
Physically discrete beta-lactamase-type thioesterase catalyzes product release in atrochrysone synthesis by iterative type I polyketide synthase.
Awakawa T, Yokota K, Funa N, Doi F, Mori N, Watanabe H, Horinouchi S., Chem. Biol. 16(6), 2009
PMID: 19549600
Biologically active secondary metabolites from the fungi
Bills, Microbiol. Spectr. 4(), 2016
Cytoskyrins A and B, new BIA active bisanthraquinones isolated from an endophytic fungus.
Brady SF, Singh MP, Janso JE, Clardy J., Org. Lett. 2(25), 2000
PMID: 11112640
Characterization of the Aspergillus nidulans monodictyphenone gene cluster.
Chiang YM, Szewczyk E, Davidson AD, Entwistle R, Keller NP, Wang CC, Oakley BR., Appl. Environ. Microbiol. 76(7), 2010
PMID: 20139316
Secondary metabolism and biotrophic lifestyle in the tomato pathogen Cladosporium fulvum.
Collemare J, Griffiths S, Iida Y, Karimi Jashni M, Battaglia E, Cox RJ, de Wit PJ., PLoS ONE 9(1), 2014
PMID: 24465762
New insights into the formation of fungal aromatic polyketides.
Crawford JM, Townsend CA., Nat. Rev. Microbiol. 8(12), 2010
PMID: 21079635
Identification of a starter unit acyl-carrier protein transacylase domain in an iterative type I polyketide synthase.
Crawford JM, Dancy BC, Hill EA, Udwary DW, Townsend CA., Proc. Natl. Acad. Sci. U.S.A. 103(45), 2006
PMID: 17071746
Structural basis for biosynthetic programming of fungal aromatic polyketide cyclization.
Crawford JM, Korman TP, Labonte JW, Vagstad AL, Hill EA, Kamari-Bidkorpeh O, Tsai SC, Townsend CA., Nature 461(7267), 2009
PMID: 19847268
Emodin: A Review of its Pharmacology, Toxicity and Pharmacokinetics.
Dong X, Fu J, Yin X, Cao S, Li X, Lin L; Huyiligeqi, Ni J., Phytother Res 30(8), 2016
PMID: 27188216
Filamentous fungi are large-scale producers of pigments and colorants for the food industry.
Dufosse L, Fouillaud M, Caro Y, Mapari SA, Sutthiwong N., Curr. Opin. Biotechnol. 26(), 2013
PMID: 24679259
Anthraquinones and Derivatives from Marine-Derived Fungi: Structural Diversity and Selected Biological Activities.
Fouillaud M, Venkatachalam M, Girard-Valenciennes E, Caro Y, Dufosse L., Mar Drugs 14(4), 2016
PMID: 27023571
Pilzinhaltstoffe, 32. Nachweis einer bicyclischen Zwischenstufe der Anthrachinon-Biosynthese
Franck, Liebigs Ann. Chem. 1981(), 1981
Fungal anthraquinones
Gessler, Appl. Biochem. Microbiol. 49(), 2013
Elucidation of cladofulvin biosynthesis reveals a cytochrome P450 monooxygenase required for anthraquinone dimerization.
Griffiths S, Mesarich CH, Saccomanno B, Vaisberg A, De Wit PJ, Cox R, Collemare J., Proc. Natl. Acad. Sci. U.S.A. 113(25), 2016
PMID: 27274078
The biosynthetic logic of polyketide diversity.
Hertweck C., Angew. Chem. Int. Ed. Engl. 48(26), 2009
PMID: 19514004
Cyanodermella asteris sp. nov. (Ostropales) from the inflorescence axis of Aster tataricus
Jahn, Mycotaxon 132(), 2017
InterProScan 5: genome-scale protein function classification.
Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S., Bioinformatics 30(9), 2014
PMID: 24451626
Secondary Metabolites from Endophytic Fungus Penicillium pinophilum Induce ROS-Mediated Apoptosis through Mitochondrial Pathway in Pancreatic Cancer Cells.
Koul M, Meena S, Kumar A, Sharma PR, Singamaneni V, Riyaz-Ul-Hassan S, Hamid A, Chaubey A, Prabhakar A, Gupta P, Singh S., Planta Med. 82(4), 2016
PMID: 26848704
Xanthones of Lichen Source: A 2016 Update.
Le Pogam P, Boustie J., Molecules 21(3), 2016
PMID: 26950106
Classification, prediction, and verification of the regioselectivity of fungal polyketide synthase product template domains
Li, J. Biol. Chem. 285(), 2010
Comprehensive curation and analysis of fungal biosynthetic gene clusters of published natural products.
Li YF, Tsai KJS, Harvey CJB, Li JJ, Ary BE, Berlew EE, Boehman BL, Findley DM, Friant AG, Gardner CA, Gould MP, Ha JH, Lilley BK, McKinstry EL, Nawal S, Parry RC, Rothchild KW, Silbert SD, Tentilucci MD, Thurston AM, Wai RB, Yoon Y, Aiyar RS, Medema MH, Hillenmeyer ME, Charkoudian LK., Fungal Genet. Biol. 89(), 2016
PMID: 26808821
Genome-based cluster deletion reveals an endocrocin biosynthetic pathway in Aspergillus fumigatus.
Lim FY, Hou Y, Chen Y, Oh JH, Lee I, Bugni TS, Keller NP., Appl. Environ. Microbiol. 78(12), 2012
PMID: 22492455
Anthraquinones As Pharmacological Tools and Drugs.
Malik EM, Muller CE., Med Res Rev 36(4), 2016
PMID: 27111664
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Antioxidant activity of compounds from the medicinal herb Aster tataricus.
Ng TB, Liu F, Lu Y, Cheng CH, Wang Z., Comp. Biochem. Physiol. C Toxicol. Pharmacol. 136(2), 2003
PMID: 14559292
Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: A review.
Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA., Microb. Pathog. 82(), 2015
PMID: 25865953
Construction of a public CHO cell line transcript database using versatile bioinformatics analysis pipelines.
Rupp O, Becker J, Brinkrolf K, Timmermann C, Borth N, Puhler A, Noll T, Goesmann A., PLoS ONE 9(1), 2014
PMID: 24427317
Biosynthetic incorporation of emodin and emodinanthrone into anthraquinonoids of Penicillium brunneum and Penicillium islandicum
Sankawa, Tetrahedron Lett. 14(), 1973
Metabolic products of fungi. XIII. The structure of oxyskyrin.
SHIBATA S, TAKIDO M, OHTA A, KUROSU T., Pharm Bull 5(6), 1957
PMID: 13527143
Type III polyketide synthases: functional classification and phylogenomics
Shimizu, Chem. Biochem. 18(1), 2016
Genetic and biosynthetic studies of the fungal prenylated xanthone shamixanthone and related metabolites in Aspergillus spp revisited
Simpson, Chem. BioChem 13(), 2012
Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources.
Stanke M, Schoffmann O, Morgenstern B, Waack S., BMC Bioinformatics 7(), 2006
PMID: 16469098
Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans.
Szewczyk E, Chiang YM, Oakley CE, Davidson AD, Wang CC, Oakley BR., Appl. Environ. Microbiol. 74(24), 2008
PMID: 18978088
Molecular Approaches to Screen Bioactive Compounds from Endophytic Fungi.
Vasundhara M, Kumar A, Reddy MS., Front Microbiol 7(), 2016
PMID: 27895623
Synthesis and Evaluation of 131I-Skyrin as a Necrosis Avid Agent for Potential Targeted Radionuclide Therapy of Solid Tumors.
Wang C, Jin Q, Yang S, Zhang D, Wang Q, Li J, Song S, Sun Z, Ni Y, Zhang J, Yin Z., Mol. Pharm. 13(1), 2015
PMID: 26647005
antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters.
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Muller R, Wohlleben W, Breitling R, Takano E, Medema MH., Nucleic Acids Res. 43(W1), 2015
PMID: 25948579
Genome analysis of the sugar beet pathogen Rhizoctonia solani AG2-2IIIB revealed high numbers in secreted proteins and cell wall degrading enzymes.
Wibberg D, Andersson L, Tzelepis G, Rupp O, Blom J, Jelonek L, Puhler A, Fogelqvist J, Varrelmann M, Schluter A, Dixelius C., BMC Genomics 17(), 2016
PMID: 26988094
A new dimeric anthraquinone from endophytic Talaromyces sp. YE3016.
Xie XS, Fang XW, Huang R, Zhang SP, Wei HX, Wu SH., Nat. Prod. Res. 30(15), 2016
PMID: 26815015
Secondary metabolites from cetrarioid lichens: Chemotaxonomy, biological activities and pharmaceutical potential.
Xu M, Heidmarsson S, Olafsdottir ES, Buonfiglio R, Kogej T, Omarsdottir S., Phytomedicine 23(5), 2016
PMID: 27064003
Polyphasic taxonomy of the genus Talaromyces.
Yilmaz N, Visagie CM, Houbraken J, Frisvad JC, Samson RA., Stud. Mycol. 78(), 2014
PMID: 25492983
Clustered pathway genes in aflatoxin biosynthesis.
Yu J, Chang PK, Ehrlich KC, Cary JW, Bhatnagar D, Cleveland TE, Payne GA, Linz JE, Woloshuk CP, Bennett JW., Appl. Environ. Microbiol. 70(3), 2004
PMID: 15006741
Expectorant, antitussive, anti-inflammatory activities and compositional analysis of Aster tataricus.
Yu P, Cheng S, Xiang J, Yu B, Zhang M, Zhang C, Xu X., J Ethnopharmacol 164(), 2015
PMID: 25701752
New cytotoxic compounds of endophytic fungus Alternaria sp. isolated from Broussonetia papyrifera (L.) Vent.
Zhang N, Zhang C, Xiao X, Zhang Q, Huang B., Fitoterapia 110(), 2016
PMID: 27001249
Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica.
Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH., PLoS Pathog. 7(10), 2011
PMID: 22022265

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