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Identification and Antifungal Activity of Compounds from the Mangrove

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Identification and Antifungal Activity of Compounds from the Mangrove marine drugs Article Identification and Antifungal Activity of Compounds from the Mangrove Endophytic Fungus Aspergillus clavatus R7 Wensheng Li 1, Ping Xiong 1, Wenxu Zheng 1, Xinwei Zhu 1, Zhigang She 2, Weijia Ding 1,* and Chunyuan Li 1,* 1 College of Materials and Energy, South China Agricultural University, Guangzhou 510642, China; [email protected] (W.L.); [email protected] (P.X.); [email protected] (W.Z.); [email protected] (X.Z.) 2 School of Chemistry and Chemical Engineering, Sun Yat-Sen University, Guangzhou 510275, China; [email protected] * Correspondence: [email protected] (W.D.); [email protected] (C.L.); Tel.: +86-20-85280319 (C.L.) Received: 17 July 2017; Accepted: 17 August 2017; Published: 19 August 2017 Abstract: Two new coumarin derivatives, 4,40-dimethoxy-5,50-dimethyl-7,70-oxydicoumarin (1), 7-(γ,γ-dimethylallyloxy)-5-methoxy-4-methylcoumarin (2), a new chromone derivative, (S)-5-hydroxy-2,6-dimethyl-4H-furo[3,4-g]benzopyran-4,8(6H)-dione (5), and a new sterone derivative, 24-hydroxylergosta-4,6,8(14),22-tetraen-3-one (6), along with two known bicoumarins, kotanin (3) and orlandin (4), were isolated from an endophytic fungus Aspergillus clavatus (collection No. R7), isolated from the root of Myoporum bontioides collected from Leizhou Peninsula, China. Their structures were elucidated using 1D- and 2D- NMR spectroscopy, and HRESIMS. The absolute configuration of compound 5 was determined by comparison of the experimental and calculated electronic circular dichroism (ECD) spectra. Compound 6 significantly inhibited the plant pathogenic fungi Fusarium oxysporum, Colletotrichum musae and Penicillium italicum, compound 5 significantly inhibited Colletotrichum musae, and compounds 1, 3 and 4 greatly inhibited Fusarium oxysporum, showing the antifungal activities higher than those of the positive control, triadimefon. Keywords: mangrove endophytic fungus; coumarin; chromone; sterone; antifungal activity; Aspergillus clavatus 1. Introduction Marine mangrove endophytic fungi are among the most productive sources of structurally unusual and biologically active natural products [1–3]. Aspergillus clavatus, belonging to Ascomycetes (Eurotiales, Trichocomaceae), is usually found as a saprophytic fungus, which is widespread in nature, producing mycotoxins and other metabolites with activities [4–9]. In our continuous search for new bioactive natural products from mangrove endophytes, the methanol extract from the endophytic fungus, A. clavatus (collection No. R7) isolated from the root of Myoporum bontioides A. Gray collected from Leizhou Peninsula, China, had been screened to show antifungal activities against several plant pathogenic fungi [10]. This prompted us to investigate the corresponding metabolites. As a result, two new coumarin derivatives, 4,40-dimethoxy-5,50-dimethyl-7,70-oxydicoumarin (1), 7-(γ,γ-dimethylallyloxy)-5-methoxy-4-methylcoumarin (2), a new chromone derivative, (S)-5-hydroxy-2,6-dimethyl-4H-furo[3,4-g]benzopyran-4,8(6H)-dione (5), and a new sterone derivative, 24-hydroxylergosta-4,6,8(14),22-tetraen-3-one (6), along with two known bicoumarins, kotanin (3) and orlandin (4)[11], were isolated (Figure1). Herein, we report their isolation, structural elucidation and bioactivity. Mar. Drugs 2017, 15, 259; doi:10.3390/md15080259 www.mdpi.com/journal/marinedrugs Mar. Drugs 2017, 15, 259 2 of 10 Figure 1. The chemical structures of compounds 1–6. Figure 1. The chemical structures of compounds 1–6. 2. Results and Discussion Compound 1 was obtained as a white, amorphous powder. It showed a molecular ion peak at m/z 395.1129 in the positive HR-ESI-MS spectrum, corresponding to molecular formula C H O m/z 395.1129 in the positive HR‐ESI‐MS spectrum, corresponding to molecular formula C2222H1818O77 + 1 (fourteen degrees of unsaturation) ([M + H] +,, calcd. calcd. 395.1125). 395.1125). The The 1HH NMR NMR spectrum spectrum of of 11 (Table(Table 11)) exhibited signals of two meta-coupling aromatic protons at δ 6.92 (d, 1H, 2.4 Hz) and 7.05 (d, 1H, exhibited signals of two meta‐coupling aromatic protons at δH 6.92H (d, 1H, 2.4 Hz) and 7.05 (d, 1H, 2.4 Hz), 2.4 Hz), an olefinic proton at δ 5.70 (s, 1H), an aromatic methyl group at δ 2.56 (s, 3H) and a an olefinic proton at δH 5.70 (s, 1H),H an aromatic methyl group at δH 2.56 (s, 3H) and a methoxylH group at δH δ 13 3.94methoxyl (s, 3H). group The 13 atC NMRH 3.94 and (s, 3H). HSQC The spectraC NMR of 1 and revealed HSQC 11 spectra carbon of signals,1 revealed including 11 carbon one methyl, signals, oneincluding methoxyl, one methyl,one ester one carbonyl methoxyl, and oneeight ester olefinic carbonyl carbons. and These eight NMR olefinic and carbons. MS data These suggested NMR that and compoundMS data suggested 1 was most that likely compound a symmetrical1 was most coumarin likely a dimer symmetrical derivative coumarin [12,13], dimer wherein derivative each subunit [12,13], whereinwas substituted each subunit by one was methoxyl substituted and byone one methyl, methoxyl and connected and one methyl, together and by connected one oxygen together atom. Comparisonby one oxygen of the atom. NMR Comparison spectral data of of compound the NMR spectral 1 with those data of of the compound known 7‐hydroxy1 with those‐4‐methoxy of the‐ 5known‐methylcoumarin 7-hydroxy-4-methoxy-5-methylcoumarin [11] showed great similarity in [that11] showed they both great use similarity deuterated in dimethyl that they sulfoxide both use asdeuterated solvent. However, dimethyl sulfoxidethe chemical as solvent. shifts of However, compound the 1 chemicalare obviously shifts shifted of compound downfield1 are by obviously 3.3/0.28, 6.0/0.37shifted downfieldppm at C‐6/H by‐ 3.3/0.28,6, C‐8/H‐8, 6.0/0.37 and upfield ppm by at C-6/H-6,5.7 ppm at C-8/H-8, C‐7, compared and upfield with those by 5.7 of ppm 7‐hydroxy at C-7,‐ 4compared‐methoxy with‐5‐methylcoumarin, those of 7-hydroxy-4-methoxy-5-methylcoumarin, suggesting that the two coumarin suggesting subunits that were the two presumably coumarin 0 connectedsubunits were together presumably through connected an oxygen together atom from through C‐7 and an oxygen C‐7′ in atom 1. This from presumption C-7 and C-7 wasin further1. This presumption was further confirmed by HMBC experiment (Figure2). HMBC correlations from δ 6.92 confirmed by HMBC experiment (Figure 2). HMBC correlations from δH 6.92 (H‐6/H‐6′) to δCH 109.4 (H-6/H-60) to δ 109.4 (C-4a/C-40a), 155.5 (C-7/C-70), 105.4 (C-8/C-80) and 23.5 (C-10/C-100), from δ (C‐4a/C‐4′a), 155.5C (C‐7/C‐7′), 105.4 (C‐8/C‐8′) and 23.5 (C‐10/C‐10′), from δH 2.56 (H‐10/H‐10′) to δHC 2.56 (H-10/H-100) to δ 109.4 (C-4a/C-40a), 137.9 (C-5/C-50) and 119.6 (C-6/C-60), and from δ 7.05 109.4 (C‐4a/C‐4′a), 137.9C (C‐5/C‐5′) and 119.6 (C‐6/C‐6′), and from δH 7.05 (H‐8/H‐8′) to δC H109.4 0 δ 0 0 0 (H-8/H-8(C‐4a/C‐4′a)) to andC 156.4109.4 (C (C-4a/C-4‐8a/C‐8′a),a) suggested and 156.4 that (C-8a/C-8 the methyla), suggested (C‐10/C‐10 that′) and the the methyl oxygen (C-10/C-10 atom were) and the oxygen atom were attached on C-5/C-50 and C-7/C-70, respectively. Simultaneously, HMBC attached on C‐5/C‐5′ and C‐7/C‐7′, respectively. Simultaneously, HMBC correlations from δH 5.70 correlations from δ 5.70 (H-3/H-30) to δ 162.1 (C-2/C-20), 169.5 (C-4/C-40), and 109.4 (C-4a/C-40a), (H‐3/H‐3′) to δC 162.1H (C‐2/C‐2′), 169.5 (C‐C4/C‐4′), and 109.4 (C‐4a/C‐4′a), and from δH 3.94 (H‐9/H‐9′) and from δ 3.94 (H-9/H-90) to 169.5 (C-4/C-40), along with a four-bond HMBC correlation from δ 2.56 to 169.5 (CH‐4/C‐4′), along with a four‐bond HMBC correlation from δH 2.56 (H‐10/H‐10′) to δC H169.5 0 δ 0 0 (H-10/H-10(C‐4/C‐4′), indicated) to C 169.5 that (C-4/C-4 the methoxyl), indicated was thatconnected the methoxyl to C‐4/C was‐4 connected′. Therefore, to C-4/C-4 compound. Therefore, 1 was 0 0 0 unambiguouslycompound 1 was elucidated unambiguously as 4,4′‐ elucidateddimethoxy‐ as5,5 4,4′‐dimethyl-dimethoxy-5,5‐7,7′‐oxydicoumarin.-dimethyl-7,7 -oxydicoumarin. Mar. Drugs 2017, 15, 259 3 of 10 Table 1. 1H and 13C NMR data for compounds 1 and 2. 1 a 2 b No. δC δH, Mult. (J in Hz) δC δH, Mult. (J in Hz) 1 2 162.1, C 7.61, s 163.2, C 2-OH 3 88.6, CH 5.7, s 87.5, CH 5.54, s 4 169.5, C 169.8, C 5 137.9, C 138.4, C 6 119.6, CH 6.92, d (2.4) 116.3, CH 6.64, d (2.4) 7 155.5, C 161.2, C 8 105.4, CH 7.05, d (2.4) 99.4, CH 6.68, d (2.4) 9 57.2, CH3 3.94, s 55.9, CH3 3.94, s 10 23.5, CH3 2.56, s 23.4, CH3 2.62, s 4a 109.4, C 107.8, C 8a 156.4, C 156.6, C 0 1 65.1, CH2 4.55, d (7.2) 20 162.1, C 7.61, s 118.8, CH 5.47, t (7.2) 30 88.6, CH 5.7, s 139.1, C 0 4 169.5, C 25.8, CH3 1.82, s 0 5 137.9, C 18.2, CH3 1.77, s 60 119.6, CH 6.92, d (2.4) 70 155.5, C 80 105.4, CH 7.05, d (2.4) 0 9 57.2, CH3 3.94, s 0 10 23.5, CH3 2.56, s 40a 109.4, C 80a 156.4, C a b Measured in CD3COCD3; Measured in CDCl3.
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