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New Antibacterial Phenone Derivatives Asperphenone A–C from Mangrove-Derived Fungus Aspergillus Sp

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New Antibacterial Phenone Derivatives Asperphenone A–C from Mangrove-Derived Fungus Aspergillus Sp marine drugs Article New Antibacterial Phenone Derivatives Asperphenone A–C from Mangrove-Derived Fungus Aspergillus sp. YHZ-1 Zhi-Kai Guo 1,2,†, Yi-Qin Zhou 1,†, Hao Han 1, Wen Wang 1, Lang Xiang 1, Xin-Zhao Deng 1, Hui-Ming Ge 1,* and Rui-Hua Jiao 1,* 1 State Key Laboratory of Pharmaceutical Biotechnology, Institute of Functional Biomolecules, School of Life Sciences, Nanjing University, Nanjing 210023, China; [email protected] (Y.-Q.Z.); [email protected] (H.H.); [email protected] (W.W.); [email protected] (L.X.); [email protected] (X.-Z.D.) 2 Key Laboratory of Biology and Genetic Resources of Tropical Crops, Ministry of Agriculture, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; [email protected] * Correspondence: [email protected] (H.-M.G.); [email protected] (R.-H.J.) † These authors contributed equally to this work. Received: 29 December 2017; Accepted: 25 January 2018; Published: 30 January 2018 Abstract: Marine fungi are a promising source of novel bioactive natural products with diverse structure. In our search for new bioactive natural products from marine fungi, three new phenone derivatives, asperphenone A–C (1–3), have been isolated from the ethyl acetate extract of the fermentation broth of the mangrove-derived fungus, Aspergillus sp. YHZ-1. The chemical structures of these natural products were elucidated on the basis of mass spectrometry, one- and two-dimensional NMR spectroscopic analysis and asperphenone A and B were confirmed by single-crystal X-ray crystallography. Compounds 1 and 2 exhibited weak antibacterial activity against four Gram-positive bacteria, Staphylococcus aureus CMCC(B) 26003, Streptococcus pyogenes ATCC19615, Bacillus subtilis CICC 10283 and Micrococcus luteus, with the MIC values higher than 32.0 µM. Keywords: mangrove endophyte; Aspergillus sp.; marine natural product; asperphenone; antibacterial activity 1. Introduction Marine filamentous fungi are a rich source of antimicrobial compounds, anti-inflammatory, anticancer and antiviral agents [1–5]. Among all the marine-sourced fungi, the species in the genus Aspergillus (Trichocomaceae) are an important source for novel pharmacological metabolites such as polyketides, alkaloids and terpenoids [6–9]. The mangrove plants inhabit the intertidal zones in the tropics and subtropics, providing a very unique habitat for animals and microbes. Thus, the mangrove-associated fungi, with the majority coming from endophytic species, have attracted much attention to discover structurally diverse and bioactive secondary metabolites. In the past several years, our research group has explored many novel secondary metabolites from mangrove-derived endophytic fungi, such as sesquiterpenoids diaporols A-I, diaporine with regulation activity of macrophage differentiation and other polyketides [10–12]. As part of our ongoing search for novel biologically active natural products from microbe from special environment [13,14], we chemically investigated an endophytic fungus, Aspergillus sp. YHZ-1, from mangrove plant from Hainan Island, China. Fractionation of the ethyl acetate extract of its liquid fermentation broth led to the discovery of three new phenone derivatives, which we have named asperphenone A–C (1–3). Mar. Drugs 2018, 16, 45; doi:10.3390/md16020045 www.mdpi.com/journal/marinedrugs Mar.Mar. Drugs Drugs2018 2018, 16, 16, 45, x FOR PEER REVIEW 2 of2 7 of 7 of three new phenone derivatives, which we have named asperphenone A–C (1–3). Compounds 1 Compoundsand 2 were1 testedand 2 wereand displayed tested and weak displayed antibacterial weak antibacterial activity against activity fouragainst Gram-positive four Gram-positive bacteria. bacteria.Herein, Herein,we report we reportthe isolation the isolation and structure and structure elucidation elucidation of these of these new new compounds compounds and and their their antibacterialantibacterial activity. activity. 2.2. Results Results AA large-scale large-scale fermentation fermentation broth broth (50(50 L) of Aspergillus sp.sp. YHZ-1 YHZ-1 was was collected collected and and extracted extracted with with ethylethyl acetate acetate three three times times to to produce produce aa crude extract. The The subsequent subsequent fractionation fractionation by by repeated repeated column column chromatographychromatography over over silica silica gel, gel, octadecylsilyloctadecylsilyl silic silicaa gel gel (ODS), (ODS), Sephadex Sephadex LH-20 LH-20 and and semi-preparative semi-preparative reversed-phasereversed-phase highhigh performanceperformance liquidliquid chroma chromatographytography (HPLC) (HPLC) yielded yielded three three new new phenone phenone derivatives,derivatives, asperphenone asperphenone A–C A–C ((11––33)) (Figure(Figure1 1).). FigureFigure 1. 1.The The structures structures ofof asperphenoneasperphenone A–C A–C ( (11––33) )isolated isolated from from AspergillusAspergillus sp.sp. YHZ-1. YHZ-1. AsperphenoneAsperphenone AA ((11)) waswas isolated as as a areddish-brown reddish-brown needle needle crystal. crystal. The Themolecular molecular formula formula of 1 was determined to be C17H16O7 on the basis of the high-resolution (HR) ESI-MS (m/z 355.2716 [M + of 1 was determined to be C17H16O7 on the basis of the high-resolution (HR) ESI-MS (m/z 355.2716 + 1 13 [MNa] + Na, calcd.]+, calcd. 355.2706) 355.2706) along along with with the theH and1H andC 13NMRC NMR data data (Table (Table 1), 1indicating), indicating ten ten degrees degrees of of unsaturation. The1 1H,13 13C and HSQC NMR spectra (in supplementary materials) in DMSO-d6 revealed unsaturation. The H, C and HSQC NMR spectra (in supplementary materials) in DMSO-d6 revealed signals of two methyls (δC/δH 11.6/1.73, C-14/H3-14; δC/δH 26.6/2.52, C-16/H3-16), one oxygenated signals of two methyls (dC/dH 11.6/1.73, C-14/H3-14; dC/dH 26.6/2.52, C-16/H3-16), one oxygenated methyl (δC/δH 60.3/3.78, 10-OMe), one methylene (δC/δH 19.4/3.70, C-7/H2-7), one ketone carbon (δC methyl (dC/dH 60.3/3.78, 10-OMe), one methylene (dC/dH 19.4/3.70, C-7/H2-7), one ketone carbon 203.8, C-15), two α,β-unsaturated carbonyl carbons (δC 182.7, C-9; δC 185.1, C-12), three phenolic (dC 203.8, C-15), two a,b-unsaturated carbonyl carbons (dC 182.7, C-9; dC 185.1, C-12), three phenolic hydroxyl protons (δH 10.25, 1-OH; δH 13.21, 5-OH; δH 10.85, 11-OH) and ten aromatic/olefinic carbons, hydroxyl protons (dH 10.25, 1-OH; dH 13.21, 5-OH; dH 10.85, 11-OH) and ten aromatic/olefinic whose chemical shift values indicated the presence of one 1,2,3,4-tetrasubstituted benzene ring (δC carbons, whose chemical shift values indicated the presence of one 1,2,3,4-tetrasubstituted benzene 162.7, C-1; δC/δH 107.8/6.42 (d, J = 8.8 Hz), C-2/H-2; δC/δH 131.8/7.67 (d, J = 8.8 Hz), C-3/H-3; δC 112.8, ring (d 162.7, C-1; d /d 107.8/6.42 (d, J = 8.8 Hz), C-2/H-2; d /d 131.8/7.67 (d, J = 8.8 Hz), C-4; δCC 162.4, C-5; δC C112.0,H C-6) and four quaternary carbons (δC 136.0,C C-8;H δC 138.8, C-10; δC 143.3, C-3/H-3;C-11; δC d144.5,C 112.8, C-13). C-4; ThedC 162.4,tetrasubstituted C-5; dC 112.0, benzene C-6) ring and was four determined quaternary as carbons a 1,3-dihydroxy-4- (dC 136.0, C-8; dCacetophenone138.8, C-10; d moiety,C 143.3, which C-11; dwasC 144.5, deduced C-13). by Theanalysis tetrasubstituted of the 1H-1H COSY benzene correlation ring was from determined H-2 to H- as a 1 1 1,3-dihydroxy-4-acetophenone3 and the HMBC correlations from moiety, H-2 which to C-4 was and deduced C-6, from by H-3 analysis to C-1, of C-5 the andH- C-15,H COSY from correlationH3-16 to fromC-4 H-2and C-15 to H-3 and and from the 5-OH HMBC to C-4, correlations C-5 and C-6 from (Figure H-2 2). to HMBC C-4 and correlations C-6, from from H-3 H to2-7 C-1, to C-1, C-5 C- and C-15,5 and from C-6 H permitted3-16 to C-4 the and linkage C-15 andof C-7 from to 5-OHC-6 of to the C-4, acetophenone C-5 and C-6 moiety. (Figure 2The). HMBCpresence correlations of a p- frombenzoquinone H2-7 to C-1, moiety C-5 could and C-6be deduced permitted from the the linkage chemical of shifts C-7 toof C8-C13 C-6 of in the 1, acetophenonewhich was partially moiety. Theconfirmed presence by of the a p observation-benzoquinone of HMBC moiety correlations could be deducedfrom H3-14 from to C-8, the C-12 chemical and C-13 shifts and of from C8-C13 H2-7 in 1, whichto C-8, was C-9 partially and C13. confirmed Meanwhile, by the the connectivity observation of of the HMBC p-benzoquinone correlations and from acetophenone H3-14 to C-8, moietiesC-12 and C-13via andthe methylene from H2-7 C-7 to was C-8, established C-9 and C13. by the Meanwhile, relevant HMBC the connectivity correlations. ofHowever, the p-benzoquinone the positions of and acetophenonethe hydroxyl moietiesgroup and via methoxyl the methylene group on C-7 the was p-benzoquinone established by moiety the relevant cannot HMBCbe determined correlations. as However,their 2D correlations the positions cannot of the be hydroxyl observed.
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