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New Butenolides and Cyclopentenones from Saline Soil-Derived Fungus Aspergillus Sclerotiorum

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New Butenolides and Cyclopentenones from Saline Soil-Derived Fungus Aspergillus Sclerotiorum molecules Article New Butenolides and Cyclopentenones from Saline Soil-Derived Fungus Aspergillus Sclerotiorum Li-Ying Ma 1, Huai-Bin Zhang 1, Hui-Hui Kang 1, Mei-Jia Zhong 1, De-Sheng Liu 1,*, Hong Ren 2 and Wei-Zhong Liu 1,* 1 College of Pharmacy, Binzhou Medical University, Yantai 264003, China 2 Beijing Higher Institution Engineering Research Center of Food Additives and Ingredients, Beijing Key Laboratory of Flavor Chemistry, Beijing Laboratory for Food Quality and Safety, Beijing Technology and Business University, Beijing 100048, China * Correspondence: [email protected] (D.-S.L.); [email protected] (W.-Z.L.); Tel.: +86-535-691-3205 (W.-Z.L.) Received: 3 July 2019; Accepted: 20 July 2019; Published: 21 July 2019 Abstract: Three new γ-hydroxyl butenolides (1–3), a pair of new enantiomeric spiro-butenolides (4a and 4b), a pair of enantiomeric cyclopentenones (5a new and 5b new natural), and six known compounds (6–11), were isolated from Aspergillus sclerotiorum. Their structures were established by spectroscopic data and electronic circular dichroism (ECD) spectra. Two pairs of enantiomers [(+)/(–)-6c and (+)/(–)-6d] obtained from the reaction of 6 with acetyl chloride (AcCl) confirmed that 6 was a mixture of two pairs of enantiomers. In addition, the X-ray data confirmed that 7 was also a racemate. The new metabolites (1 5) were evaluated for their inhibitory activity against cancer − and non-cancer cell lines. As a result, compound 1 exhibited moderate cytotoxicity to HL60 and A549 with IC50 values of 6.5 and 8.9 µM, respectively, and weak potency to HL-7702 with IC50 values of 17.6 µM. Furthermore, compounds 1 9 were screened for their antimicrobial activity using the − micro-broth dilution method. MIC values of 200 µg/mL were obtained for compounds 2 and 3 towards Staphylococcus aureus and Escherichia coli, while compound 8 exhibited a MIC of 50 µ/mL towards Candida albicans. Keywords: Aspergillus sclerotiorum; γ-hydroxyl butenolides; cyclopentenones; enantiomer; cytotoxicity; antimicrobial activity 1. Introduction Aspergillus sclerotiorum widely distributes in various environments such as marine samples, soil, sea-salt field, and rotting apples, and produces a series of bioactive metabolites. Representatives include asterriquinones [1], aspochracin derivative [2], lovastatin analogues [3], butenolides [4], cyclopeptides [5–7], sclerotiamide [8], hydroxamic acids [9], and ochratoxin [10]. In addition, co-incubation of this strain with Penicillium citrinum resulted in the production of furanone derivatives and alkaloids [11]. The Yellow River Delta is formed mainly by the deposition of sand and mud carried by the Yellow River, which is the world’s youngest wetland ecosystem [12]. High evaporation and tidal intrusion heavily salinizes and alkalizes the soil, half of which is barren and not suitable for the growth of crops [13,14]. The saline soil is typically characterized by poor nutrient and high salinity, which endows the microorganism special biosynthetic pathways during the evolutionary process to produce structurally novel and biologically active secondary metabolites. Up to now, only a few research papers have been carried out on the fungi from this unique environment [15]. In our continuation of investigation on the saline soil-derived fungi from the Yellow River Delta, dozens of natural products (NPs) with multifarious structural features and a wide range of biological activities Molecules 2019, 24, 2642; doi:10.3390/molecules24142642 www.mdpi.com/journal/molecules Molecules 2019, 24, 2642 2 of 13 Molecules 2019, 24, x FOR PEER REVIEW 2 of 13 werewere obtained obtained [16 [16,17].,17]. As As part part of our of ongoingour ongoing efforts efforts in seeking in seeking for new bioactivefor new NPs,bioactiveA. sclerotiorum NPs, A. JH42sclerotiorum with antimicrobial JH42 with antimicrobial activity was isolatedactivity was from isolated saline soil,from and saline subjected soil, and to subjected chemical to exploration, chemical whichexploration, led to the which achievement led to the ofachievement six new (1– 3of, 4asix, 4b,newand (1–5a3, 4a), a, 4b, new and natural 5a), a ( 5bnew), andnatural six known(5b), and (6 –six11 ) compoundsknown (6– (Figure11) compounds1). Additionally, (Figure the 1). isolated Additionally,γ-hydroxyl the isolated butenolides γ-hydroxyl in the current butenolides work werein the all provedcurrent to undergowork were tautomerism all proved at C-4to basedundergo on the tautomerism analyses of physicochemicalat C-4 based on properties, the analyses calculated of ECDphysicochemical data, and X-ray properties, diffraction. calculated Herein, ECD details data, of theand isolation, X-ray diffraction. structure elucidation,Herein, details acetylation, of the cytotoxic,isolation,and structure antimicrobial elucidation, activities acetylation, of these compounds cytotoxic, areand reported. antimicrobial activities of these compounds are reported. FigureFigure 1. 1.Structures Structures of of Compounds Compounds1 1−33, ,4a 4a, ,4b 4b, ,5a 5a,,5b 5b,,6 6−1111,(, (+)/(−)-+)/( )-6c6c andand (+)/(−)- (+)/( )-6d6d. − − − − 2. Results 2. Results Compound 1 was obtained as an optically inactive colorless oil with the molecular formula of Compound 1 was obtained as an optically inactive colorless oil with the molecular formula of C7H8O4 as determined by the deprotonated-ion HRESIMS at m/z 155.0339 [M H]− (calcd for C7H7O4, C7H8O4 as determined by the deprotonated-ion HRESIMS at m/z 155.0339 [M− − H]− (calcd for C7H7O4, 155.0344). Its IR spectrum indicated the presence of hydroxyl (3374 cm 1), keto carbonyl (1755 cm 1), 155.0344). Its IR spectrum indicated the presence of hydroxyl (3374 cm−–1), keto carbonyl (1755 cm–1−), α,β-unsaturated lactone groups (1731, 1652 cm 1)[18]. The 1H NMR spectrum (Table1) in DMSO- d α,β-unsaturated lactone groups (1731, 1652 cm−–1) [18]. The 1H NMR spectrum (Table 1) in DMSO-d66 showed two singlet methyls at δ 2.25 and 1.96, a singlet olefinic proton at δ 6.18, and a hydroxyl showed two singlet methyls at δHH 2.25 and 1.96, a singlet olefinic proton at δH 6.18, and a hydroxyl group at δ 8.50. Its 13C NMR spectrum revealed seven carbon resonances, corresponding to a keto group at HδH 8.50. Its 13C NMR spectrum revealed seven carbon resonances, corresponding to a keto carbonyl ( 201.5), four diagnostic carbon signals ( 170.2, 165.7, 118.9 and 105.7) for a -hydroxyl carbonyl δ(CδC 201.5), four diagnostic carbon signals (δC 170.2, 165.7, 118.9 and 105.7) for a γγ-hydroxyl butenolidebutenolide moiety moiety [4 [4],], and and two two methyl methyl groups groups (δ C(δ24.7C 24.7 and and 12.7) 12.7) (Table (Table1). The1). The gross gross structure structure of 1 ofwas 1 unambiguouslywas unambiguously established established by the by HMBC the HMBC correlations correlations from H-2from to H-2 C-1, to C-3 C-1, and C-3 C-4, and from C-4, H-6from to H-6 C-4 andto C-4 C-5, and and C-5, from and H-7 from to C-1, H-7 C-3 to and C-1, C-4 C-3 (Figure and C-42). It(Figure was a mixture2). It was of a inseparable mixture of enantiomers, inseparable whichenantiomers, mutually which transformed mutually through transformed the γ-keto-acid through formthe γ-keto-acid as existence form in penicillic as existence acid in [19 penicillic]. acidCompound [19]. 2 was also isolated as an optically inactive colorless oil with the molecular formula of C8H12CompoundO5 as elucidated 2 was by also the isolated HRESIMS as anm /zoptically187.0610 inactive [M H] colorless− (calcd oil for with C8H 11theO 5molecular, 187.0601). formula The IR 1 − absorptionof C8H12O5 bands as elucidated at 3373, by 1739 the and HRESIMS 1652 cm m/z− suggested 187.0610 [M the − presence H]− (calcd of for hydroxyl, C8H11O5α, ,187.0601).β-unsaturated The 1 lactoneIR absorption groups. ThebandsH NMRat 3373, spectrum 1739 inand MeOH- 1652d4 displayedcm–1 suggested signals forthe apresence singlet olefinic of hydroxyl, proton at δHα,β5.86,-unsaturated an oxymethine lactone at groups.δH 3.56 The (dd, 1HJ = NMR7.0, 3.2 spectrum Hz), a diastereotopic in MeOH-d4 displayed methylene signals at δH for3.90 a (m)singlet and olefinic proton at δH 5.86, an oxymethine at δH 3.56 (dd, J = 7.0, 3.2 Hz), a diastereotopic methylene Molecules 2019,, 24,, 2642x FOR PEER REVIEW 33 of of 13 at δH 3.90 (m) and 3.66 (dd, J = 11.7, 7.0 Hz), a methoxyl at δH 3.50 (s) and a methyl at δH 2.09 (Table 3.66 (dd, J = 11.7, 7.0 Hz), a methoxyl at δ 3.50 (s) and a methyl at δ 2.09 (Table1). The 13C NMR 1). The 13C NMR spectrum (Table 1), withH the help of DEPT and HSQCH data, showed the presence spectrum (Table1), with the help of DEPT and HSQC data, showed the presence of two methyls (one of two methyls (one oxygenated), an oxymethylene, an olefinic and an oxymethine, a hemiketal oxygenated), an oxymethylene, an olefinic and an oxymethine, a hemiketal carbon (δC 110.1), and two carbon (δC 110.1), and two quaternary carbons (δC 172.9 and 168.7). The above data indicated 2 was quaternary carbons (δ 172.9 and 168.7). The above data indicated 2 was also a γ-hydroxyl butenolide also a γ-hydroxyl butenolideC as 1. The main differences were the appearances of an oxygenated as 1. The main differences were the appearances of an oxygenated methyl, an oxymethylene and an methyl, an oxymethylene and an oxymethine, together with the disappearances of a carbonyl and a oxymethine, together with the disappearances of a carbonyl and a methyl. The planar structure and the methyl. The planar structure and the assignments of the NMR data were completed by the HMBC assignments of the NMR data were completed by the HMBC correlations (Figure2).
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