Article pubs.acs.org/jnp
Antimicrobial Metabolites from Streptomyces sp. SN0280 Hui Tian,† Jamil Shafi,† Mingshan Ji,†,‡ Yuhui Bi,† and Zhiguo Yu*,†,‡ †
College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, People’s Republic of China Engineering & Technological Research Center of Biopesticide for Liaoning Province, Shenyang 110866, People’s Republic of China
‡
S Supporting Information *
ABSTRACT: One new indole derivative, chloroindole (1), one new diketone, streptoone A (2), two new ketonic acids, streptoones B (3) and C (4), and one known macrolide antibiotic, X-14952B (5), were isolated from Streptomyces sp. SN0280. Extensive NMR, HRESIMS, and IR analysis was used to elucidate their structures. Streptoone A (2) displayed antibacterial activity (MIC value of 7.81 μg/mL) against Clavibater michiganensis, comparable with the positive control streptomycin (MIC value of 7.81 μg/mL). Streptoone B (3) showed antifungal activity (MIC value of 15.63 μg/mL) against Phytophthora capsici (positive control carbendazol MIC value of 7.81 μg/mL). These molecules provide new templates for the potential treatment and management of these phytopathogens. ffective and sustained control of phytopathogens is important in agriculture. Increasing incidence of resistance in pathogens (often caused by application of conventional fungicides) and environmental and human health hazards drive the need to search for new safe plant protectants.1,2 It is particularly desirable to evaluate new classes of biologically active natural products that might function by modes of action different from those of existing antimicrobial agents, thus avoiding problems of resistance and residual material.3 Microbes have been very important in the production of natural antimicrobial drugs. They account for more than 10% of reported bioactive metabolites.4,5 About 45% of reported microbial metabolites are products of actinomycetes,with approximately 75% of metabolites being produced by species of the genus Streptomyces.6,7 Streptomyces species provide a rich source of natural products that may have potential agricultural uses.8 These include macrolides, terpenoids, flavonoids, and peptides, several of which are antibiotics.9 Several such antibiotics have been used successfully to control plant diseases. Streptomycin was the first antibiotic used to control plant diseases and has been used to control many bacterial diseases.10 However, tolerance or resistance of plant pathogens to antibiotics has occurred universally after long-term application.11 In order to overcome resistant fungi and bacteria, the development of novel antibiotics for the future has become particularly important. The aim of this study was to isolate and evaluate the antimicrobial activity of Streptomyces metabolites active against phytopathogens, with the goal to develop potential agrochemicals for the control of plant diseases. The extraction, purification, and structural elucidation of five antimicrobial molecules from strain Streptomyces sp. SN0280 are described, including one new indole derivative, chloroindole (1), one new diketone, streptoone A (2), and two new ketonic acids,
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© 2017 American Chemical Society and American Society of Pharmacognosy
streptoones B (3) and C (4), together with one known compound, X-14952B (5). In addition, all the isolated compounds 1−5 were tested for their antimicrobial activities against phytopathogens, including seven fungal and four bacterial strains.
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RESULTS AND DISCUSSION Structure Elucidation. The CH2Cl2 extract of the fermentation broth of Streptomyces sp. SN0280 was subjected to silica gel column chromatography and further fractionated by gel chromatography on Sephadex LH-20 or by HPLC to afford four new compounds (1−4, Figure 1) and one known compound. The known compound was identified as X14952B (5) by comparison to published spectroscopic data.12 Received: November 7, 2016 Published: March 15, 2017 1015
DOI: 10.1021/acs.jnatprod.6b01016 J. Nat. Prod. 2017, 80, 1015−1019
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Information). Therefore, the structure of compound 1 was elucidated as 3-chloro-4-(3-methylbut-2-enyl)-1H-indole and was named as chloroindole. Compound 2 was obtained as a colorless oil . Its molecular formula, C24H40O2, as determined by HRESIMS data, implying the presence of five degrees of unsaturation. The IR spectrum of 2 also displayed absorption bands for the carbonyl group (1713 cm−1). The 1H NMR spectrum of 2 (Table 2) displayed six methyl protons [δH 2.09 (s, H3-1), δH 1.57 (s, H3-24), δH 1.56 (s, H3-23), δH 1.04 (d, J = 6.7 Hz, H3-20 and H3-21), and δH 0.95 (d, J = 6.7 Hz, H3-22)] and four olefinic protons [δH 5.37 (dt, J = 15.3, 6.1 Hz, H-7), δH 5.15 (dd, J = 15.3, 8.5 Hz, H-6), and δH 5.09 (t, J = 6.1 Hz, H-10 and H-14), as well as numerous methylene protons from δH 1.0 to 2.5. Combined 13 C NMR (Table 2) and HSQC spectroscopic data indicated the presence of six methyls, eight methylenes, two saturated methines, four olefinic methines, two fully substituted carbons (δC 135.5 and 133.8), and two ketone carbons (δC 213.1 and 211.6). Further analysis of 2D NMR data allowed for the establishment of the structure of compound 2. An alkanone chain was constructed by the interpretation of 1H−1H COSY and HMBC correlations. The 1H−1H COSY correlations confirmed linkages of H3-21/H-3/H2-4/H-5/H-6/H-7/H2-8/ H2-9/H-10, H2-12/H2-13/H-14, H2-16/H2-17, and H2-19/H320. The correlations of HMBC from H3-21 to C-2, C-3, and C4, H3-22 to C-4, C-5, and C-6, H3-23 to C-10, C-11, and C-12, and H3-24 to C-14, C-15, and C-16 illustrated the positions of the four methyls. In addition, the connections of the alkenyl chains with the C-2 and C-18 ketone carbonyl carbons were secured from HMBC correlations of H3-1 with C-2 and C-3, H2-4 with C-2 and C-6, and H2-16, H2-17, H2-19, and H3-20 with C-18. The relative configuration of 2 was deduced from the data from a NOESY experiment. The α-orientation of H321 and β-orientation of H3-22 were determined by the NOESY correlations from H3-21 to H-5 and H3-22 to H-3. In addition, the NOESY correlations of H-10/H-12 and H-14/H-16 indicated that these protons were oriented on the same side. The geometric isomer of the double bond (between C-6 and C7) was determined as being of E configuration on the basis of the coupling constant (value of 15.3). Consequently, compound 2 was characterized as (6E,10E,14E)-3,5,11,15tetramethyl-6,10,14-icosatriene-2,18-dione. Compound 2 was identified and named as streptoone A. Compound 3 was obtained as a colorless oil and displayed a molecular formula of C17H28O3 as determined by HRESIMS data, with four degrees of unsaturation. The IR spectrum displayed absorption bands for the carbonyl groups (1758 and 1710 cm−1). The 1H and 13C NMR spectroscopic data (Table 2) of 3 showed high resemblance to those of 2, the only difference being that a double bond between C-14 and C-15 was broken and connected with a carboxyl in compound 3. This connection was further confirmed through 2D NMR spectroscopic data (see Supporting Information). The carboxyl was directly linked to methylene at C-13, as determined by HMBC correlation from H2-12 and H2-13 to the carboxyl carbon at δC 178.6. In addition, a combination of the HMBC signals from H3-21 to C-2, C-3, and C-4, H3-22 to C-4, C-5, and C-6, H3-23 to C-10, C-11, and C-12, and H2-12 to C-10 and C-11 illustrated the position of three methyls. The 1H−1H COSY correlations assigned a linkage of H3-21/H-3/H2-4/H5/H-6/H-7/H2-8/H2-9/H-10, H2-12/H2-13. The structure of compound 3 was thus determined as (4E,8E)-4,10,12
Figure 1. Key COSY (bold) and HMBC (arrows) correlations of compounds 1−4.
Compound 1 was obtained as a pale yellow oil. Its molecular formula, C13H14ClN, was established by HRESIMS data, indicating seven degrees of unsaturation. Its IR spectrum displayed absorption bands for a secondary amino group (3426 cm−1). The 1H NMR spectrum of 1 (Table 1) indicated the Table 1. 1H (600 MHz) and 13C (150 MHz) NMR Data of Compound 1 in DMSO-d6 position
δC, type
1 (NH) 2 3 4 5 6 7 8 9 10 11 12 13 14
119.8, CH 130.7, C 124.1, C 127.0, C 112.2, CH 126.5, CH 100.5, CH 135.0, C 32.0, CH2 122.4, CH 132.1, C 25.6, CH3 17.8, CH3
δH (J in Hz) 11.10, s 7.57, s
7.28, brs 7.33, brt (2.8) 6.36, brs 3.44, d (7.3) 5.30, t (7.3) 1.72, s 1.71, s
presence of one olefinic proton [δH 5.30 (t, J = 7.3 Hz, H-11)], one CH2 proton [δH 3.44 (d, J = 7.3 Hz, H2-10)], and two methyl protons [δH 1.72 (s, H3-13) and δH 1.71 (s, H3-14)], suggesting there is a prenyl group in compound 1. Another five proton signals [δH 11.10 (s, 1-NH), δH 7.57 (s, H-2), δH 7.33 (brt, J = 2.8 Hz, H-7), δH 7.28 (brs, H-6), and δH 6.36 (brs, H8)] were assigned to an indole resonance. The corresponding 13 C NMR (Table 1) spectrum displayed 13 carbon signals. Further analysis of HSQC data revealed that these carbon signals included two methyls, one methylene, five methines, and five fully substituted carbons. Detailed analysis of the 1H and 13C NMR spectroscopic data of 1 revealed remarkable similarities with 3-chloro-5-(3-methylbut-2-enyl)-1H-indole, a synthetic compound,13 indicating that 1 also possessed a 3chloroindole skeleton with a substituent prenyl group. However, there are some striking differences in the data for the two compounds. The 13C NMR spectra of 1 showed that three carbon signals (δC 124.1, δC 127.0, and δC 112.2) were moved downfield, indicating the position of the isoprene on the indole ring had changed. The isoprene was located at C-5 of the indole ring based on the HMBC correlations of H2-10 (δH 3.44, d, J = 7.3 Hz) with C-4 (δC 124.1), C-5 (δC 127.0), and C-6 (δC 112.2), as well as H-7 (δH 7.33, brt, J = 2.8 Hz) and H-11 (δH 5.30, t, J = 7.3 Hz) with C-5 (δC 127.0) (Supporting 1016
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Table 2. 1H (600 MHz) and 13C (150 MHz) NMR Data of Compounds 2−4 in CDCl3 2 position
δC, type
1 2 3 4
28.2, CH3 213.1, C 45.3, CH 40.0, CH2
5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
35.2, CH 135.5, CH 129.5, CH 32.8, CH2 28.2, CH2 124.2, CH 135.5, C 39.7, CH2 26.7, CH2 124.9, CH 133.8, C 33.8, CH2 41.3, CH2 211.6, C 36.0, CH2 7.9, CH3 16.1, CH3 21.8, CH3 16.2, CH3 16.2, CH3
3 δH (J in Hz)
2.09, s 2.49, m Ha: 1.60, m Hb: 1.20, m 2.07, m 5.15, dd (15.3, 8.5) 5.37, dt (15.3, 6.1) 2.00, overlap 2.00, overlap 5.09, t (6.1) 1.95, t (7.2) 2.04, m 5.09, t (6.1)
δC, type 28.0, CH3 213.7, C 45.3, CH 40.0, CH2 35.2, CH 135.6, CH 129.3, CH 32.6, CH2 28.1, CH2 125.0, CH 133.5, C 34.5, CH2 33.0, CH2 178.6, C
4 δH (J in Hz)
δC, type
2.11, s
δH (J in Hz)
28.2, CH3 213.3, C 45.3, CH 39.9, CH2
2.50, m Ha: 1.61, m Hb: 1.22, m 2.10, m 5.15, overlap 5.36, dt (15.2, 6.2) 2.00, m 2.03, m 5.15, overlap
2.11, s 2.49, m Ha: 1.60, m Hb: 1.22, m 2.14, overlap 5.21, dd (15.2, 8.3) 5.37, m 2.14, overlap 2.25, brs 6.83, brs
35.2, CH 136.6, CH 128.3, CH 31.4, CH2 29.0, CH2 143.9, CH 128.0, C 173.2, C
2.29, brs 2.43, brs
2.22, t (7.7) 2.47, t (7.7) 2.41, 1.04, 1.04, 0.95, 1.56, 1.57,
q d d d s s
(7.3) (6.7) (6.7) (6.7)
16.1, CH3 21.8, CH3 16.1, CH3
1.04, d (6.7) 0.96, d (6.6) 1.60, s
16.1, CH3 21.8, CH3 12.4, CH3
1.04, d (6.7) 0.97, d (6.6) 1.83, brs
Table 3. Inhibitory Effects of Tested Compounds on Phytopathogenic Fungia MIC, μg/mL compd
Fo
Pc
Et
Ss
Cc
Bc
Pa
1 2 3 4 5 Carbendazol Amphotericin B
125 125 125 125 31.25 15.63 125
31.25 125 15.63 31.25 15.63 7.81 500
125 62.50 31.25 31.25 62.50 125 500
31.25 250 500 250 125 500 500
250 125 >500 >500 62.50 62.50 >500
250 500 >500 >500 15.63 31.25 31.25
250 31.25 250 125 31.25 3.91 62.50
a
Fo = Fusarium oxysporum; Pc = Phytophthora capsici; Et = Exserohilum turcicum; Ss = Stemphylium solani; Cc = Corynespora cassiicola; Bc = Botrytis cinerea; Pa = Pythium aphanidermatum.
NOESY correlations, coupling constants, and biogenetic consideration. Antimicrobial Activity. Compounds 1−5 were evaluated for their antimicrobial activity against 11 phytopathogens, including seven fungi (Fusarium oxysporum, Phytophthora capsici, Exserohilum turcicum, Stemphylium solani, Corynespora cassiicola, Botrytis cinerea, and Pythium aphanidermatum), and four bacteria (Erwinia carotovora, Xanthomonas campestris, Clavibater michiganensis, and Pseudomonas syringae), which commonly infect major food and cash crops. The results of antifungal and antibacterial activities are shown in Table 3 and Table 4, respectively. Carbendazol, amphotericin B, and streptomycin were used as positive controls. Remarkably, streptoone A (2) displayed antibacterial activity (MIC value of 7.81 μg/mL) against Clavibater michiganensis, comparable with the positive control streptomycin (MIC value of 7.81 μg/mL). Streptoone B (3) showed antifungal activity (MIC value of 15.63 μg/mL) against Phytophthora capsici (positive control carbendazol MIC value of 7.81 μg/mL). These molecules
-trimethyl-4,8-diene-13-oxotetradecanoic acid and named streptoone B. Compound 4 was obtained as a colorless oil. Its molecular formula was established as C15H24O3 on the basis of the HRESIMS data, indicating four degrees of unsaturation. The IR spectrum displayed absorption bands for the carbonyl group (1711 cm−1). In a way similar to that used for compound 3, assignments of 1H and 13C NMR resonances of compound 4 were conducted, and all signals could be identified (Table 2), except for two methylenes at C-12 and C-13 that have disappeared from the spectra of compound 3. Further analysis of the HMBC correlation from H3-23 to C-12 revealed that the carboxyl was located at C-11. The 1H−1H COSY correlations assigned a linkage of H3-21/H-3/H2-4/H-5/H-6/H-7/H2-8/ H2-9/H-10. Therefore, compound 4 was elucidated as (2E,6E)2,8,10-trimethyl-2,6-diene-11-oxododecanoic acid and was named as streptoone C. The relative configurations of 3 and 4 were deduced to be the same as that of 2 on the basis of 1017
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extracts were then concentrated under reduced pressure to get the crude extract. Isolation and Purification. The dried extract was dissolved in 50% CH3OH (600 mL). The solution was extracted four times with equal volumes of CH2Cl2. The CH2Cl2 extract was collected and concentrated on a rotary evaporator under vacuum at 28 °C to yield 4.36 g of solid reddish brown residue. The CH2Cl2 extract was subjected to silica gel column (350 mm × 25 mm i.d.) chromatography eluted stepwise with petroleum etherethyl acetate (100:2, 100:6, 100:12, 100:24, 1:1, and 0:100, v/v, each for 2 L) as the mobile phase to afford six fractions, T1 to T6. Fraction T2 was separated by silica gel column chromatography using 100% petroleum ether, then purified by Sephadex LH-20 column (500 mm × 20 mm i.d.) eluted with CH3OH: CH2Cl2 = 1:1 to yield compound 1 (19.5 mg). Fraction T3 was chromatographed on Sephadex LH-20 column eluted with CH3OH and further purified by reverse-phase semipreparative HPLC, eluted with a 92% CH3OH (0.1% HCOOH was added into the solvent) for 30 min at a flow rate of 3 mL/min, with UV detection at 210 nm, to obtain compound 2 (tR = 20.3 min, 24.7 mg). Fraction T4 separated on a Sephadex LH-20 column eluting with CH3OH as eluent to yield compound 3 (21.1 mg) and a mixture. The mixture was then isolated by reverse-phase semipreparative HPLC applying a 75% CH3OH (0.1% HCOOH was added into the solvent) for 40 min at a flow rate of 3 mL/min, UV detection was at 210 nm, to give compound 4 (tR = 31.7 min, 3.7 mg). Fraction T6 was purified on reverse-phase semipreparative HPLC, eluted with a 73% CH3OH (0.1% HCOOH was added into the solvent) for 35 min at a flow rate of 3 mL/min, UV detection was at 220 nm, to give compound 5 (tR = 27.5 min, 53 mg). Chloroindole (1). Faint yellow oil; [α]24 D + 0.32 (c 1.52, MeOH); IR (KBr) vmax: 3426, 2921, 2855, 1451 cm−1; 1H NMR (600 MHz, DMSO-d6) and 13C NMR (150 MHz, DMSO-d6) data, Table 1; HRESIMS m/z 218.0765 [M − H]− (calcd for C13H13ClN, 218.0754). Streptoone A (2). Colorless oil; [α]24 D + 20.9 (c 2.47, MeOH); IR (KBr) vmax: 2965, 2929, 2850,1713 cm−1; 1H NMR (600 MHz, CDCl3) and 13C NMR (150 MHz, CDCl3) data, Table 2; HRESIMS m/z 361.3108 [M + H]+ (calcd for C24H41O2, 361.3106). Streptoone B (3). Colorless oil; [α]24 D −39.0 (c 2.11, MeOH); IR (KBr) vmax: 2968, 2923, 2855, 1758, 1710 cm−1; 1H NMR (600 MHz, CDCl3) and 13C NMR (150 MHz, CDCl3) data, Table 2; HRESIMS m/z 303.1941 [M + Na]+ (calcd for C17H28O3Na, 303.1936). Streptoone C (4). Colorless oil; [α]24 D -37.0 (c 0.27, MeOH); IR (KBr) vmax: 2919, 2850, 1711 cm−1; 1H NMR (600 MHz, CDCl3) and 13 C NMR (150 MHz, CDCl3) data, Table 2; HRESIMS m/z 275.1625 [M + Na]+ (calcd for C15H24O3Na, 275.1623). Antimicrobial Assay. The antimicrobial activities of compounds 1−5 against fungi and bacteria were determined using liquid cultures in 96-well plates using a modification of the broth microdilution method.15−18 Seven fungal (F. oxysporum, Ph. capsici, Ex. turcicum, S. solani, Co. cassiicola, B. cinerea, and Py. Aphanidermatum) and four bacterial strains (Er. carotovora, X. campestris, Cl. michiganensis, and Ps. syringae) were provided by the Laboratory of Microbial Metabolites, College of Plant Protection, at Shenyang Agricultural University. The medium volume per well was 100 μL. These fungi and bacteria were inoculated in RPMI-1640 medium and MHB medium, respectively. All test compounds and positive controls including carbendazol, amphotericin B, and streptomycin were dissolved in DMSO and tested at concentrations between 0.98 and 500 μg/mL of two-fold step dilution. The microorganism suspensions (10 μL) of each pathogenic fungi and bacteria were added to a 96-well microtiter plate. The negative controls were treated with 1% DMSO, which corresponds to the highest concentration. The incubated plates of fungi and bacteria were incubated at 25 °C for 48 h and 30 °C for 24 h, respectively. Then the absorbance was measured at 600 nm (SpectraMax 190). The minimum inhibitory concentration (MIC) was determined as the lowest concentration that inhibited visible growth of phytopathogens. The growth inhibition of each dilution was calculated using the following formula:
Table 4. Inhibitory Effects of Tested Compounds on Phytopathogenic Bacteriaa MIC, μg/mL compd
Ec
Xc
Cm
Ps
1 2 3 4 5 streptomycin
62.50 500 >500 500 31.25 62.50
>500 250 >500 >500 500 31.25
250 7.81 62.50 125 62.50 7.81
250 62.50 62.50 62.50 62.50 3.91
a
Ec = Erwinia carotovora; Xc = Xanthomonas campestris; Cm = Clavibater michiganensis; Ps = Pseudomonas syringa.
provide new templates for the potential treatment and management of these phytopathogens.
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EXPERIMENTAL SECTION
General Experimental Procedures. Optical rotations were measured with an AP-300 automatic polarimeter (Atago, Tokyo, Japan). Infrared (IR) spectra were recorded in potassium bromide disks on a Spectrum 65 spectrophotometer (PerkinElmer, MA). NMR spectra were recorded on an Avance-600 NMR spectrometer (Bruker, Karlsruhe, Germany) at room temperature. Carbon signals and the residual proton signals of DMSO-d6 (δC 39.52 and δH 2.50) and CDCl3 (δC 77.0 and δH 7.26) were used for calibration. Highresolution electrospray ionization mass spectrometry (HRESIMS) spectra were recorded on 6500 series quadrupole-time-of-flight (QTOF) mass spectrometer (Agilent, Santa Clara, CA). High-performance liquid chromatography (HPLC) analysis was performed on a 1260 Infinity LC system (Agilent), and the column used was a 250 mm × 4.6 mm i.d., 5 μm, ZORBAX Eclipse XDB (Agilent). Semipreparative HPLC was performed on a 1260 series system (Agilent), and the column used was a 250 mm × 9.4 mm i.d., 5 μm, ZORBAX Eclipse XDB (Agilent). Column chromatography was performed using silica gel (100−200 mesh) (Qingdao Ocean Chemical Co. Ltd., Qingdao, China) and Sephadex LH-20 (GE Healthcare, Uppsala, Sweden). All chemical reagents were purchased from a chemical reagent company (Sinopharm Chemical Reagent Co., Ltd., Shanghai, China) and used without further purification. Actinomycetes Material. Streptomyces sp. SN0280 was isolated from the soil collected from Xiuyan, Liaoning Province, China (40° 26′ 212.2″ N, 123° 25′ 17.5″ E), at a height of 194 m, in July 2014. The actinomycetes were identified by phylogenetic analysis, comparing to 16S rRNA sequences available on the EzTaxon database. The resulting sequence data were most similar (99.85%) to the sequence of Streptomyces cuspidosporus NBRC 12378 (GenBank accession no. AB184091.1). The strain was subsequently named as Streptomyces sp. SN0280 (GenBank accession no. KX982505) and was deposited in the Laboratory of Microbial Metabolites, College of Plant Protection, at Shenyang Agricultural University, China. Fermentation and Extraction. The Streptomyces sp. SN0280 was preserved as a spore solution at −80 °C. A two-stage fermentation was performed, and in both stages, F medium [i.e., sucrose, 100 g; glucose, 10 g; casamino acids, 0.1 g; yeast extract, 5 g; 3-(N-morpholino) propanesulfonic acid (MOPS), 21 g; trace elements, 1 mL; K2SO4, 0.25 g; MgCl2·6H2O, 10 g, in a final volume of 1 L H2O, pH 7.0] was used.14 In the first stage, a 250 mL Erlenmeyer flask, containing 50 mL of the F medium, was inoculated with 10 μL of Streptomyces sp. SN0280 spore solution and incubated with shaking (180 rpm) at 28 °C for 2 d to prepare the seed culture. In the second stage, 24 2 L Erlenmeyer flasks, each contains 400 mL of F medium, were inoculated with 20 mL of the seed culture and left for fermentation for 7 d under identical conditions. The fermentation cultures were centrifuged at 5000 rpm and 4 °C for 30 min to remove mycelia, and the broth was extracted with 3% Amberlite XAD 16 resin for 4 h at room temperature with agitation. Resin was harvested by centrifugation and extracted four times with methanol. The combined methanol 1018
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(16) Espinel-Ingroff, A.; Chaturvedi, V.; Fothergill, A.; Rinaldi, M. G. J. Clin. Microbiol. 2002, 40, 3776−3781. (17) Castillo, U. F.; Strobel, G. A.; Ford, E. J.; Hess, W. M.; Porter, H.; Jensen, J. B.; Albert, H.; Robison, R.; Condron, M. A. M.; Teplow, D. B.; Stevens, D.; Yaver, D. Microbiology 2002, 148, 2675−2685. (18) Wang, J.; He, W.; Huang, X.; Tian, X.; Liao, S.; Yang, B.; Wang, F.; Zhou, X.; Liu, Y. J. Agric. Food Chem. 2016, 64, 2910−2916.
% inhibition = 100 × [1 − OD of treated well /OD of negative control well] The dilutions of the tested compounds were independently performed at least three times.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jnatprod.6b01016. Microbial taxonomy, NMR and HRMS spectra for 1−4, and NMR and analytical data for 5 (PDF)
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AUTHOR INFORMATION
Corresponding Author
*Tel.: +86 24 88342209. Fax: +86 24 88487038. E-mail: zyu@ syau.edu.cn. ORCID
Zhiguo Yu: 0000-0002-0909-6788 Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was financially supported by Liaoning Pandeng Scholar Program in 2012, China. We are grateful to Prof. Shihong Luo at the College of Bioscience and Biotechnology, Shenyang Agricultural University, for proofreading the manuscript. The authors thank Shenyang Pharmaceutical University and Dalian Institute of Chemical Physics, Chinese Academy of Sciences, for technical assistance with NMR and MS spectra, respectively.
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REFERENCES
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DOI: 10.1021/acs.jnatprod.6b01016 J. Nat. Prod. 2017, 80, 1015−1019
