Skip to main content
SpringerLink
Log in

Tafuketide, a phylogeny-guided discovery of a new polyketide from Talaromyces funiculosus Salicorn 58

  • Biotechnological products and process engineering
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

A phylogeny-guided approach was applied to screen endophytic fungi containing type I polyketide synthase (PKS I) biosynthetic gene sequences and aimed to correlate genotype to chemotype for the discovery of novel bioactive polyketides. Salicorn 58, which was identified as Talaromyces funiculosus based on its internal transcribed spacer (ITS) and ribosomal large-subunit (LSU) DNA sequences, showed significant target bands. A chemical investigation of the culture of Salicorn 58 was allowed for the isolation of a new polyketide, Talafun (1), and a new natural product, N-(2′-hydroxy-3′-octadecenoyl)-9-methyl-4,8-sphingadienin (2), together with six known compounds, including chrodrimanin A (3), chrodrimanin B (4), N-(4-hydroxy-2-methoxyphenyl) acetamide (5), butyl β-glucose (6), 3β,15β-dihydroxyl-(22E, 24R)-ergosta-5,8(14),22-trien-7-dione (7), and (3β,5a,8a,22E)-5,8-epidioxyergosta-6,22-dien-3-ol (8). Their chemical structures were elucidated by extensive spectroscopic analysis and electro circular dichroism (ECD) spectrum calculations. Antioxidant experiments revealed that compound 5 showed strong ABTS+ radical scavenging activity with an IC50 value of 11.43 ± 1.61 μM and potent ferric reducing activity (FRAP assay) with FRAP value of 187.52 ± 2.97. Antimicrobial assays revealed that compounds 1 and 4 showed high levels of selectivity toward Escherichia coli with MIC values of 18 ± 0.40 and 43 ± 0.52 μM, respectively. Compounds 2 and 3 exhibited broad-spectrum antimicrobial activity against Staphylococcus aureus, Mycobacterium smegmatis, Micrococcus tetragenus, Mycobacterium phlei, and E. coli, respectively. The results from the current research highlight the advantage of phylogeny-guided pipeline for the screening of new polyketides from endophytic fungi containing PKS I genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76. doi:10.1006/abio.1996.0292

    Article  CAS  PubMed  Google Scholar 

  • Dethoup T, Manoch L, Kijjoa A, Pinto M, Gales L, Damas AM, Silva A, Eaton G, Herz W (2007) Merodrimanes and other constituents from Talaromyces thailandiasis. J Nat Prod 70:1200–1202

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Kallifidas D, Brady SF (2011) Functional analysis of environmental DNA-derived type II polyketide synthases reveals structurally diverse secondary metabolites. Pnas 108:12629–12634. doi:10.1073/pnas.1103921108/-/DCSupplemental

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao H, Hong K, Zhang X, Liu H-W, Wang N-L, Zhuang L, Yao X-S (2007) New steryl esters of fatty acids from the mangrove fungus Aspergillus awamori. Helv Chim Acta 90:1165–1178. doi:10.1002/hlca.200790116

    Article  CAS  Google Scholar 

  • Gomez S, Cosson C, Deschamps AM (1997) Evidence for a bacteriocin-like substance produced by a new strain of Streptococcus sp., inhibitory to Gram-positive food-borne pathogens. Res Microbiol 148:757–766. doi:10.1016/s0923-2508(97)82451-5

    Article  CAS  PubMed  Google Scholar 

  • 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 107:680–688. doi:10.1017/s0953756203007834

    Article  CAS  PubMed  Google Scholar 

  • Bingle LEH, Simpson TJ, Lazarus CM (1999) Ketosynthase domain probes identify two subclasses of fungal polyketide synthase genes. Fungal Genet Biol 26:209–223. doi:10.1006/fgbi.1999.1115

    Article  CAS  PubMed  Google Scholar 

  • Hayashi H, Oka Y, Kai K, Akiyama K (2012) New chrodrimanin congeners, chrodrimanins D-H, from YO-2 of Talaromyces sp. Biosci Biotech Bioch 76:1765–1768. doi:10.1271/bbb.120365

    Article  CAS  Google Scholar 

  • Jumpathong J, Seshime Y, Fujii I, Peberdy J, Lumyong S (2011) Genome screening for reducing type I polyketide synthase genes in tropical fungi associated with medicinal plants. World J Microb Biot 27:1989–1995. doi:10.1007/s11274-011-0659-9

    Article  CAS  Google Scholar 

  • Kahlos K, Kangas L, Hiltunen R (1989) Ergosterol peroxide, an active compound from Inonotus radiatus. Planta Med 55:389–390. doi:10.1055/s-2006-962036

    Article  CAS  PubMed  Google Scholar 

  • Kang H-S, Brady FS (2014a) Mining soil metagenomes to better understand the evolution of natural product structural diversity-pentangular polyphenols as a case study. J Am Chem Soc 136:18111–18119. doi:10.1021/ja510606j

  • Kang HS, Brady SF (2014b) Arixanthomycins A-C: phylogeny-guided discovery of biologically active eDNA-derived pentangular polyphenols. ACS Chem Biol 9:1267–1272. doi:10.1021/cb500141b

  • Katalinic V, Modun D, Music I, Boban M (2005) Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp Biochem Phys C: CBP 140:47–52. doi:10.1016/j.cca.2005.01.005

    CAS  Google Scholar 

  • Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. P Natl Acad Sci 100:15670–15675. doi:10.1073/pnas.2532165100

    Article  CAS  Google Scholar 

  • Kroon PA, Williamson G, Fish NM, Archer DB, Belshaw NJ (2000) A modular esterase from Penicillium funiculosum which releases ferulic acid from plant cell walls and binds crystalline cellulose contains a carbohydrate binding module. Eur J Biochem 267:6740–6752. doi:10.1046/j.1432-1033.2000.01742.x

    Article  CAS  PubMed  Google Scholar 

  • Lin CN, Tome WP, Won SJ (1991) Novel cytotoxic principles of Formosan Ganoderma lucidum. J Nat Prod 54(4):998–1002. doi:10.1021/np50076a012

  • Liu K, Ding X, Deng B, Chen W (2009) Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. J Ind Microbiol Biotechnol 36:1171–1177. doi:10.1007/s10295-009-0598-8

    Article  CAS  PubMed  Google Scholar 

  • Meikrantz W, Feldman RP, Sladicka MM, Ho D, Krupnick J, Anderson K, Schlegel RA (1991) Isolation of mitotic p34cdc2 apoenzyme from human cells. Fed Eur Biochem Soc 291:192–194. doi:10.1016/0014-5793(91)81281-C

    Article  CAS  Google Scholar 

  • Metsa-Ketela M, Salo V, Halo L, Hautala A, Hautala A, Mantsala P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6. doi:10.1111/j.1574-6968.1999.tb08770.x

    Article  CAS  PubMed  Google Scholar 

  • Mori K, Uenishi K (1996) Synthesis of (2S,2′ R ,3 R ,3′ E,4E,8E)-1-o-(β-D-Glucopyranosyl)-N-(2′- hydroxy-3′-octadecenoyl)-9-methyl-4,8-sphingadienine (Pen II), the major cerebroside isolated from Penicillium funiculosum as the fruiting-inducer against Schizophyllum commune. Liebigs Ann:1–6

  • Nugroho AE, Morita H (2014) Circular dichroism calculation for natural products. J Nat Med 68:1–10. doi:10.1007/s11418-013-0768-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donnell, K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds)The fun- gal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, UK, pp 225–233

  • Rojas JD, Sette LD, de Araujo WL, Lopes MS, da Silva LF, Furlan RL, Padilla G (2012) The diversity of polyketide synthase genes from sugarcane-derived fungi. Microbial Ecol 63:565–577. doi:10.1007/s00248-011-9938-0

    Article  CAS  Google Scholar 

  • Samson RA, Yilmaz N, Houbraken J, Spierenburg H, Seifert KA, Peterson SW, Varga J, Frisvad JC (2011) Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium. Stud Mycol 70:159–183. doi:10.3114/sim.2011.70.04

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544. doi:10.1016/s1286-4579(03)00073-x

    Article  CAS  PubMed  Google Scholar 

  • 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 28:2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Fang Y, Zhang M, Lin A, Zhu T, Gu Q, Zhu W (2008) Six new ergosterols from the marine-derived fungus Rhizopus sp. Steroids 73:19–26. doi:10.1016/j.steroids.2007.08.008

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Liu T, Xin Z (2014a) A new glucitol from an endophytic fungus Fusarium equiseti Salicorn 8. Eur Food Res Technol 239:365–376. doi:10.1007/s00217-014-2230-z

    Article  CAS  Google Scholar 

  • Wang X, Wang H, Liu T, Xin Z (2014b) A PKS I gene-based screening approach for the discovery of a new polyketide from Penicillium citrinum Salicorn 46. Appl Microbiol Biotechnol 98:4875–4885. doi:10.1007/s00253-014-5572-3

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Zhang M, Zhao Y, Wang H, Liu T, Xin Z (2013) Pentadecyl ferulate, a potent antioxidant and antiproliferative agent from the halophyte Salicornia herbacea. Food Chem 141:2066–2074. doi:10.1016/j.foodchem.2013.05.043

    Article  CAS  PubMed  Google Scholar 

  • Wei M-Y, Chen G-Y, Wang Y, Zhang X-L, Wang C-Y, Shao C-L (2011) Isolation, 1H, 13C NMR assignments, and crystal structure of chrodrimanin B from a marine fungus Aspergillus sp. Chem Nat Compd 47:571–573. doi:10.1007/s10600-011-9997-y

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications, Academic, pp 315–322

  • Wood TM, Mccrae SI, Macfarlane CC (1980) The isolation, purification and properties of the cellobiohydrolase component of Penicillium funiculosum cellulase. Biochem J 189:51–65. doi:10.1042/bj1890051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Furutani S, Ihara M, Ling Y, Yang X, Kai K, Hayashi H, Matsuda K (2015) Meroterpenoid chrodrimanins are selective and potent blockers of insect GABA-gated chloride channels. PLoS One 10:e0122629. doi:10.1371/journal.pone.0122629

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Wang T, Pei Y, Hua H, Feng B (2001) Studies on chemical constituents of the fermentation liquor of soil fungus 07-11. J Pharm Sci 10:190–192

    Google Scholar 

  • Zhao Y, Wang H, Liu T, Xin Z (2013) The individual lipid compositions produced by Cunninghamella sp. Salicorn 5, an endophytic oleaginous fungus from Salicornia bigelovii Torr. Eur Food Res Technol 238:621–633. doi:10.1007/s00217-013-2141-4

    Article  Google Scholar 

  • Zheng C-J, Xu L-L, Li Y-Y, Han T, Zhang Q-Y, Ming Q-L, Rahman K, Qin L-P (2013) Cytotoxic metabolites from the cultures of endophytic fungi from Panax ginseng. Appl Microbiol Biotechnol 97:7617–7625. doi:10.1007/s00253-013-5015-6

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Li L, Wang W, Che Q, Li D, Gu Q, Zhu T (2015) Chrodrimanins I and J from the antarctic moss-derived fungus Penicillium funiculosum GWT2-24. J Nat Prod 78:1442–1445. doi:10.1021/acs.jnatprod.5b00103

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the project funded by special funds of agro-product quality safety risk assessment of the Ministry of Agriculture of the People’s Republic of China (GJFP2015012).

Author information

Authors and Affiliations

  1. Key Laboratory of Food Processing and Quality Control, College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Jia Guo, Huomiao Ran & Zhihong Xin

  2. School of Food Science, Henan Institute of Science and Technology, Xinxiang, 453003, People’s Republic of China

    Jie Zeng

  3. Shenzhen Key Laboratory of Fermentation, Purification and Analysis, Shenzhen Polytechnic, Shenzhen, Guangdong, 518055, People’s Republic of China

    Jia Guo & Dong Liu

Authors
  1. Jia Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huomiao Ran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhihong Xin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhihong Xin.

Ethics declarations

Human and animal rights

This article does not contain any studies with human or animal subjects.

Conflict of interest

The authors declare that they have no competing interests.

Electronic supplementary material

ESM 1

(PDF 733 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, J., Ran, H., Zeng, J. et al. Tafuketide, a phylogeny-guided discovery of a new polyketide from Talaromyces funiculosus Salicorn 58. Appl Microbiol Biotechnol 100, 5323–5338 (2016). https://doi.org/10.1007/s00253-016-7311-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-016-7311-4

Keywords

Search

Navigation