Secondary Metabolites from the Culture of the Marine Sponge-Associated Fungi Talaromyces tratensis and Sporidesmium circinophorum

Abstract

Wortmin (1), meso-1,4-bis(4-methoxybenzyl)-2,3-butanediol (2), and a new isocoumarin derivative tratenopyrone (3) were isolated from the marine sponge-associated fungus Talaromyces tratensis KUFA 0091. A new diphenyl ether derivative, circinophoric acid (4), was isolated, together with the previously reported anthraquinones catenarin and physcion, the benzophenone monomethylsoluchrin, and β-ergosterol-5,8-endoperoxide, from the marine sponge-associated fungus Sporidesmium circinophorum KUFA 0043. The structures of the new compounds were established based on an extensive analysis of 1D and 2D NMR spectra, and, in the case of compounds 2–4, also by X-ray analysis. All of the isolated compounds were tested for their antibacterial activity against Gram-positive and Gram-negative bacteria, and multidrug-resistant isolates from the environment, as well as for their anti-quorum sensing based on the pigment production of Chromobacterium violaceum ATCC 31523. None of the compounds exhibited either antibacterial (MIC > 256 µg/mL) or anti-quorum sensing activities. The compounds were also inactive in the antifungal (MIC > 512 µg/mL) and cancer cell line (GI₅₀ > 150 µM) assays.

Key words

Talaromyces tratensis - Trichocomaceae - Sporidesmium circinophorum - Dothideomycetes - marine sponge-associated fungi - azaphilone - isocoumarin - diphenyl ether - wortmin

• References

• 1 Manoch L, Dethoup T, Yilmaz N, Houbraken J, Samson RA. Two new Talaromyces species from soil in Thailand. Mycoscience 2013; 54: 335-342
• 2 Nozawa K, Saito R, Udagawa SI, Nakajima S, Kawai KI. An azaphilone from Talaromyces tardifaciens . Phytochemistry 1995; 39: 719-721
• 3 Kimura T, Nishida M, Kuramochi K, Sugawara F, Yoshida H, Mizushina Y. Novel azaphilones, kasanosins A and B, which are specific inhibitors of eukaryotic DNA polymerases b and y from Talaromyces sp. Bioorg Med Chem 2008; 16: 4594-4599
• 4 Li LQ, Yang YG, Zeng Y, Zou C, Zhao PJ. A new azaphilone, kasanosin C, from an endophytic Talaromyces sp. T1BF. Molecules 2010; 15: 3993-3997
• 5 Dethoup T, Manoch L, Kijjoa A, Nascimento MSJ, Puapairoj P, Silva AMS, Eaton G, Herz W. Bacillisporins D and E, new oxyphenalenones from Talalomyces bacillisporus . Planta Med 2006; 72: 957-960
• 6 Koolen HHF, Menezes LS, Souza MP, Silva FMA, Almeida FGO, de Souza AQL, Nepel A, Barison A, da Silva FH, Evangelista DE, de Souza ADL. Talaroxanthone, a novel xanthone dímer from the endophytic fungus Talaromyces sp. Associated with Duguetia stelechantha (Diels) R.E. Fries. J Braz Chem Soc 2013; 24: 880-883
• 7 Dethoup T, Manoch L, Kijjoa A, Pinto M, Gales L, Damas AM, Silva AMS, Eaton G, Herz W. Merodrimanes and other constituents from Talaromyces thailandiasis . J Nat Prod 2007; 70: 1200-1202
• 8 Guo JP, Tan JL, Wang YL, Wu HY, Zhang CP, Niu XM, Pan WZ, Huang XW, Zhang KQ. Isolation of talathermophilins from thermophilic fungus Talaromyces thermophilus YM3–4. J Nat Prod 2011; 74: 2278-2281
• 9 Chu YS, Niu XM, Wang YL, Guo JP, Pan WZ, Huang XW, Zhang KQ. Isolation of putative biosynthetic intermediates of prenylated indole alkaloids from a thermophilic fungus Talaromyces thermophilus . Org Lett 2010; 12: 4356-4359
• 10 Li H, Huang H, Shao C, Huang H, Jiang J, Zhu X, Liu Y, Liu L, Lu Y, Li M, Lin Y, She Z. Cytotoxic norsesquiterpene peroxides from the endophytic fungus Talaromyces flavus isolated from the mangrove plant Someratia apelata . J Nat Prod 2011; 74: 1230-1235
• 11 Dong Y, Yang J, Zhang H, Lin J, Ran X, Liu M, Lu X, He J. Wortmannilactones A–D, 22-membered triene macrolides from Talaromyces wortmannii . J Nat Prod 2006; 69: 128-130
• 12 Guo JP, Zhu CY, Zhang CP, Chu YS, Wang YL, Zhang JX, Wu DK, Zhang KQ, Niu XM. Thermolides, potent nematocidal PKS-NRPS hybrid metabolites from thermophilic fungus Talaromyces thermophilus . J Am Chem Soc 2012; 34: 20306-20309
• 13 Bara R, Aly AH, Wray V, Lin WH, Proksch P, Debbab A. Talaromins A and B, new cyclic peptides from the endophytic fungus Talaromyces wortmannii . Tetrahedron Lett 2013; 54: 1686-1689
• 14 Chen M, Han L, Shao CL, She ZG, Wang CY. Bioactive diphenyl ether derivatives from a gorgonian-derived fungus Talaromyces sp. Chem Biodivers 2015; 12: 443-450
• 15 Russell DW. Sporidesmolide I, a metabolic product of Sporidesmium bakeri . Biochim Biophys Acta 1960; 45: 411-412
• 16 Russell DW, Brown ME. Sporidesmolic acid B, a hydroxyacyldipeptide from Sporidesmium bakeri . Biochim Biophys Acta 1960; 38: 382-383
• 17 Crotti P, Ferretti M, Macchia F, Stoppioni A. Ring-opening reactions of cis-and trans-2, 3-bis (4-methoxybenzyl)oxirane: competition between assistance by and migration of an acyl group. J Org Chem 1986; 51: 2759-2766
• 18 Anke H, Kolthoum I, Zähner H, Laatsch H. Metabolic products of microorganisms. 185. The anthraquinones of the Aspergillus glaucus group. I. Occurrence, isolation, identification and antimicrobial activity. Arch Microbiol 1980; 126: 223-230
• 19 Ma YM, Li Y, Liu JY, Song YC, Tan RX. Anti-Helicobacter pyroli metabolites from Rhizoctonia sp. Cy064, an endophytic fungus in Cynodon dactylon . Fitoterapia 2004; 75: 451-456
• 20 Kim DS, Baek NI, Oh SR, Jung KY, Lee IS, Kim JH, Lee HK. Anticomplementary activity of ergosterol peroxide from Naematoloma fasciculare and reassignment of NMR data. Arch Pharm Res 1997; 20: 201-205
• 21 Merlini L, Mondelli R, Nasini G, Hesse M. Structure of wortmin, a new metabolite from Penicillium wortmannii . Helv Chim Acta 1973; 561: 232-239
• 22 CAS No. 63035–47-2. 1, 4-bis-(4-methoxyphenyl)-2, 3-butanediol. Available at. http://www.molbase.com/en/cas-63035-47-2.html Accessed August 25, 2015
• 23 Gomes NM, Bessa LJ, Buttachon S, Costa PM, Buaruang J, Dethoup T, Silva AMS, Kijjoa A. Antibacterial and antibiofilm activities of tryptoquivalines and meroditerpenes isolated from the marine-derived fungi Neosartorya paulistensis, N. laciniosa, N. tsunodae, and the soil fungi N. fischeri and N. siamensis . Mar Drugs 2014; 12: 822-839
• 24 McLean RJC, Pearson 3rd LS, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 2004; 58: 351-360
• 25 Wattanadilok R, Sawangwong P, Rodrigues C, Cidade H, Pinto M, Pinto E, Silva A, Kijjoa A. Antifungal activity evaluation of the consitrituents of Haliclona baeri and H. cymaeformis, collected from the Gulf of Thailand. Mar Drugs 2007; 5: 40-51
• 26 Cidade HM, Nascimento MSJ, Pinto MMM, Kijjoa A, Silva AMS, Herz W. Artelastocarpin and carpelastofuran, two new flavones, and cytotoxicities of prenyl flavonoids from Artocarpus elasticus against three cancer cell lines. Planta Med 2001; 67: 867-870
• 27 Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 1980; 8: 4321-4325
• 28 Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 1997; 72: 5463-5467
• 29 Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25: 389-402
• 30 Sheldrick GM. SHELXS-97, Program for Crystal Structure Solution. Göttingen: University of Göttingen; 1997
• 31 Sheldrick GM. A short history of SHELX. Acta Crystallogr A 2008; 64: 112-122
• 32 Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement (CLSI document M100-S21). Wayne, PA: Clinical and Laboratory Standards Institute (CLSI); 2011
• 33 National Committee for Clinical Laboratory Standards. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard (NCCLS document M27-A2). Wayne, PA: National Committee for Clinical Laboratory Standards; 2002
• 34 National Committee for Clinical Laboratory Standards. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi: approved standard (NCCLS Document M38-A). Wayne, PA: National Committee for Clinical Laboratory Standards; 2002
• 35 Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenny S, Boyd MR. New colorimetric cytotoxic assay for anticancer drug screening. J Natl Cancer Inst 1990; 82: 1107-1112
• 36 Monks A, Scudiero D, Skehan P, Shoemaker R, Paul K, Vistica D, Hose C, Langley J, Cronise P, Vaigro-Wolff A, Gray-Goodrich M, Campbell H, Mayo J, Boyd M. Feasibility of a high-flux anticancer drugs screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst 1991; 83: 757-776