Article pubs.acs.org/JAFC
Cite This: J. Agric. Food Chem. 2019, 67, 8191−8196
Monoacylglycerol of 7,10-Dihydroxy-8(E)‑octadecenoic Acid Enhances Antibacterial Activities against Food-Borne Bacteria Kai Yu Chen,† In Hwan Kim,‡ Ching T. Hou,§ Yomi Watanabe,∥ and Hak-Ryul Kim*,†,⊥
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†
School of Food Science and Biotechnology, and ⊥Institute of Agricultural Science & Technology, Kyungpook National University, Daegu, Korea 41566 ‡ Department of Public Health Sciences, Graduate School, Korea University, Seoul, Korea § Renewable Product Technology Research Unit, National Center for Agricultural Utilization Research, ARS, USDA, Peoria, Illinois 61604, United States ∥ Osaka Research Institute of Industrial Science and Technology, Osaka, Japan S Supporting Information *
ABSTRACT: Conversion of free fatty acids into monoacylglycerol gives rise to new structural properties, particularly amphipathic property. Therefore, monoacylglycerols are widely used in pharmaceutical and food industries and are also reported to facilitate better absorption into the human body. A functional fatty acid when transformed into a monoacylglycerol will possibly conserve both the original functionality and amphipathic property. The compound 7,10-dihydroxy-8(E)octadecenoic acid (DOD) was generated from oleic acid by Pseudomonas aeruginosa PR3 and was known to contain antimicrobial activities against a broad range of food-borne and plant pathogenic bacteria. Here, we attempted to convert DOD into its monoacylglycerol form using lipase for producing an amphipathic antibacterial agent. Consequently, the monoacylglycerol of DOD (DOD-MAG) was successfully produced by coincubating DOD, glycerol, and lipase at 30 °C. The maximum conversion yield reached 70% after 12 h of incubation. Antibacterial activity of DOD-MAG was enhanced by 8 times from the original activity of DOD against food-borne bacteria. KEYWORDS: dihydroxy fatty acid, monoacylglycerol, lipase, antibacterial activity
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INTRODUCTION Hydroxy fatty acids are mainly produced by plants in nature and contain single or multiple hydroxy groups which can be attributed to beneficial industrial properties including higher activity and viscosity as opposed to the normal fatty acids.1 Owing to these features, hydroxy fatty acids can be widely applied as a lubricant, biodegradable plastic materials, paints, cosmetics, and medicine. The compound 7,10-dihydroxy-8(E)octadecenoic acid (DOD) is one such hydroxy fatty acid. DOD was first produced from oleic acid by Pseudomonas aeruginosa PR3 with over 60% production yield.2 Vegetable oils containing oleic acid were also successfully used as substrates by the strain PR3 to produce DOD.3−5 Recently, Sohn et al. reported that DOD was highly active against a broad range of food-borne and plant pathogenic microorganisms.6,7 Antimicrobial activities of DOD were also observed against the common yeast Candida albicans.8 Conversion of some health-beneficial fatty acids into their glyceride forms was considered to be more effective in dietary application. Eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) were reportedly more efficiently absorbed via food in glyceride forms than in free fatty acid forms.9 Glycerides containing n-3 unsaturated fatty acids which have cardioprotective properties, such as EPA and DHA, were synthesized by various lipases.10,11 Production of monoacylglycerols (MAGs) from various fatty acids by lipases has also been reported.11−14 Of those MAGs, MAGs of medium-chain fatty acids reportedly showed highly enhanced antimicrobial © 2019 American Chemical Society
activities as opposed to those of free fatty acids against certain Gram-positive bacteria.15 Thormar et al. reported that free unsaturated fatty acids and their MAGs in milk inactivated enveloped viruses, but not the nonenveloped ones, by disrupting their envelope membrane.16 These reports motivated us to synthesize MAG of DOD (DOD-MAG) using lipase enzyme and to further confirm that the antibacterial activity of DOD can be enhanced in MAG form. Considering the potential of DOD as an antimicrobial agent and the efficient application of MAGs in food and pharmaceutical industries, the feasibility of using DOD-MAG across several industries as a novel antimicrobial agent can be explored.
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MATERIALS AND METHODS
Materials. Olive oil (extra virgin grade) was purchased from a local market (Incheon, South Korea). Heptadecanoic acid (C17:0) was purchased from Nu-Chek Prep (Elysian, MN). A mixture of trimethylsilylimidazole (TMSI) and pyridine (1:4, v/v) was purchased from Supelco Inc. (Bellefonte, PA). Thin-layer precoated Kieselgel 60F254 plates were purchased from EM Science (Cherry Hill, NJ). Lipase Novozyme 435, TLIM, and RMIM were purchased from Novozymes (Bagsvaerd, Denmark). Other lipases were kindly provided to us by Dr. Yomi Watanabe of the Osaka Research Received: Revised: Accepted: Published: 8191
May 16, 2019 July 3, 2019 July 8, 2019 July 8, 2019 DOI: 10.1021/acs.jafc.9b03063 J. Agric. Food Chem. 2019, 67, 8191−8196
Article
Journal of Agricultural and Food Chemistry
held at 270 and 280 °C, respectively. Elaidic acid (C17:0) was added as an internal standard to the sample before derivatization for quantification. For GC/mass spectrometry (GC/MS), electronimpact (EI) mass spectra were obtained using a Hewlett-Packard (Avondale, PA) 5890 GC coupled with a Hewlett-Packard 5972 Series Mass Selective Detector. The column outlet was connected directly to the ion source. Separation was carried out in a methylsilicon column (30 m × 0.25 mm i.d., 0.25 μm film thickness) at a temperature gradient of 20 °C/min ranging from 70 to 170 °C, with a holding time of 1 min at 170 °C and of 5 °C/min at 250 °C followed by holding at this temperature for 15 min (helium flow rate = 0.67 mL/min). Proton and 13C NMR spectra were determined in deuterated chloroform with a Varian-500 spectrometer (Billerica, MA), operated at a frequency of 400 and 100 MHz, respectively. Determination of Antibacterial Activity. The antimicrobial activity of the sample was determined according to the method described in the Manual of Clinical Microbiology.17 For disk diffusion methods, cell suspension of 500 μL (0.3, o.d. at 600 nm) was added and spread uniformly on the surface of nutrient agar plate (15−20 mL nutrient agar medium, 9 cm in diameter). Whatman filter papers (No. 1 discs of 6 mm diameter) were impregnated with 20 μL of DMSO solution containing an appropriate amount of the individual compound and placed on the surface of the seeded agar plates. The plates were incubated at 37 °C for 24 h to form clear zones. Antibacterial activity was evaluated by measuring the distance between the edge of the disc and the edge of the clear zone. Minimum inhibitory concentration (MIC) of the sample was determined following the slightly modified twofold dilution method. A loopful of the bacterial culture from the LB slant was inoculated in the Luria broth and incubated at 37 °C for 24 h. The suspension culture was diluted with LB medium to achieve an inoculum of approximately 105 CFU/mL. A twofold serial dilution of the sample solution was performed to obtain final concentrations of the sample ranging from 500 to 1.95 μg/mL working volume in a 1.5 mL Eppendorf tube. The purified sample was first dissolved in 50% DMSO. The tubes containing 800 μL of LB medium were inoculated with 100 μL of the bacterial suspension and 100 μL of the sample solution and were subsequently incubated under inverted shaking conditions at 100 rpm and 37 °C for 12 h. After incubation, optical density of the tube suspension was measured at 600 nm and compared with that of the negative control. Tube suspension with DMSO alone (5% final concentration) was used as a negative control. The minimum inhibitory concentration (MIC50, μg/mL) was defined as the concentration at which cell growth was inhibited by over 50% in comparison with the negative control. All the experiments were performed in duplicate, and all the average values were within the error range, unless specified otherwise.
Institute of Industrial Science and Technology (Osaka, Japan). All other chemicals were reagent grade and were used without further purification. Other chemicals were purchased from Sigma Chemical Co. (St. Louis, MO), unless mentioned otherwise. Microorganism. Pseudomonas aeruginosa NRRL strain B-18,602 (PR3) was kindly provided by Dr. Hou of the National Center for Agricultural Utilization Research (Peoria, IL). The strain was aerobically grown at 28 °C by incubating under shaking conditions of 200 rpm in a 125 mL Erlenmeyer flask containing 50 mL of SM6 medium. SM6 medium contained (per liter) 4 g of dextrose, 2 g of K2HPO4, 2 g of (NH4)2HPO4, 1 g of NH4NO3, 1 g of yeast extract, 0.056 g of FeSO4·7H2O, 0.1 g of MgSO4, and 0.01 g of MnSO4·7H2O. The medium was adjusted to pH 7.0 by dilution with phosphoric acid. Standard conditions were employed as the incubation condition, unless mentioned otherwise. For determining antibacterial activities, the following six strains of well-known food-borne pathogenic and food-spoilage bacteria were obtained from the Korea Food and Drug Administration (Daegu, Korea): Bacillus subtilis (ATCC 6501), Escherichia coli (ATCC 8739), Listeria monocytogenes (ATCC 19111), Salmonella typhimurium (KCTC 2515), Staphylococcus aureus (ATCC 6538), and S. aureus (ATCC 1621). The stock cultures were maintained on Luria broth (LB) agar medium at 4 °C. Liquid culture of a strain was prepared by transferring a loopful of cells from the stock culture to a flask containing LB medium followed by incubation at 37 °C for 24 h. Production of DOD. DOD was produced according to our previous report.4 In brief, olive oil (1%, v/v) was added to a 24-h-old culture of P. aeruginosa PR3 followed by an additional incubation for 72 h under standard conditions. At the end of cultivation, the culture broth was acidified to pH 2 using 6 N HCl followed by immediate extraction performed twice with an equal volume of ethyl acetate and diethyl ether. The solvent was evaporated from the combined extracts using a rotary evaporator. The crude DOD extract was applied onto the silica gel column (1.5 cm i.d. × 30 cm) for purification. Fractionation was performed using two column volumes of the solvent mixture with a varied ratio of ethyl acetate over hexane. Production of MAG of DOD. Bioconversion was carried out in a 20 mL glass vial by using 100 mg of DOD (95%+ purity by GC), 100 mg of lipase, and 200 μL of glycerol dissolved in 3 mL of tert-butanol. The reaction was carried out in a water bath at 30 °C and was subjected to stirring (300 rpm) with a magnetic bar for 24 h. After incubation, the reaction vials were centrifuged at 4000 rpm for 10 min to obtain the product-containing supernatant. The supernatant was evaporated by nitrogen gas flushing and then fractionated using 2 mL of ethyl acetate and distilled water mixture (1:1, v/v) to remove residual glycerol. The ethyl acetate layer was recovered and used as the crude extract. The degree of esterification was expressed as the ratio (mol %) of the amount of fatty acids esterified to total fatty acids in the reaction mixture.14 Analytical Methods. Reaction products were analyzed using TLC (thin layer chromatography) and quantified via GC (gas chromatography) analysis by employing heptadecanoic acid as an internal standard. TLC analysis was conducted in a solvent system (chloroform:methanol:water:ammonium hydroxide, 47:20:2.5:0.25, v/v/v/v), and the spots were visualized by spraying the plate with 50% sulfuric acid followed by heating at 95 °C for 10 min. For purifying the target product isolated on a TLC plate, silica gels from the target spot were scraped off from the plate, and the product was subsequently extracted from the silica gel using chloroform. For GC analysis, an appropriate amount of sample was first methylated with diazomethane for 5 min at room temperature followed by derivatization with a mixture of TMSI and pyridine (1:4 v/v) for at least 30 min at room temperature. The TMS-derivatized samples were analyzed via gas chromatography (ACME 6100 series, Younglin Co., Korea) equipped with an FID and a capillary column (SPB-1, 15 m × 0.32 mm i.d., 0.25 μm thickness, Supelco Inc., Bellefonte, PA). GC run was carried out at temperature gradients of 20 °C/min ranging from 100 to 150 °C, 5 °C/min from 150 to 200 °C, and 0.5 °C/min from 200 to 210 °C followed by a 10 min hold at 300 °C (nitrogen gas flow rate: 0.67 mL/min). Injector and detector temperatures were
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RESULTS Production and Structure Confirmation of the Target Compound. Several lipases were tested to confirm the production of DOD-MAG. All the lipases presented a new additional spot except DOD at similar locations during TLC analysis of the crude extracts obtained from coincubation of DOD, glycerol, and lipase (data provided in the Supporting Information). This result confirmed that a novel compound was produced owing to the coincubation of DOD, glycerol, and lipase. Among the lipases tested, Novozyme 435 showed a relatively big size of spot. Therefore, Novozyme 435 was selected for further experiments. GC analysis of the crude extract of the reaction product by Novozyme 435 presented an unknown major peak (designated by a question mark) at a retention time of 31.8 min, along with the peaks of the substrate DOD and internal standard (Figure 1). The peaks of DOD and internal standard were confirmed using standard materials (data not shown).
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consistent with the TMS derivative of DOD which was esterified to glycerol with a molecular mass of 676. For the confirmation of structure of the target compound, the purified sample (96%+ purity by GC) was subjected to proton and 13C NMR analysis. Proton NMR of the sample showed the following resonance signals: olefinic protons (−CHCH−) at 5.88 ppm; three tertiary protons (−CH− O−), two of DOD molecule and one of glycerol molecule at 3.9 ppm; methylene groups of DOD moiety covered from 1.29 to 2.25 ppm; two methylene groups of glycerol moiety covered from 3.56 to 4.36 ppm; all hydroxyl protons at 2.0 ppm; and a terminal methyl proton at 0.96 ppm. 13C NMR confirmed the presence of the following carbons: carbonyl carbon at 178.2 ppm; a double bond between at 133.5 and 133.9 ppm; two −CH−OH carbons of DOD moiety at 72.2 and 72.9 ppm; one −CH−OH carbon of glycerol moiety at 70.3 ppm; two −CH2−O− carbons of glycerol moiety at 63.4 and 65.2 ppm; other methylene carbons of DOD moiety covered from 22.7 to 37.3 ppm; and the terminal methyl carbon at 14.1 ppm. Based on the results of a previous as well as of this study, we confirmed that sn-1 MAG of DOD was successfully produced from DOD esterification to glycerol by the lipase Novozyme 435. Production of sn-2 MAG of DOD was excluded because the lipase Novozyme 435 used in this study was specific to sn1,3. The overall pathway of DOD-MAG production from DOD and glycerol by lipase is shown in Figure 3. Time-Coursed Production of DOD-MAG. For the optimum production of DOD-MAG, time-coursed production of DOD-MAG was studied under the standard reaction conditions mentioned in the Materials and Methods section. The ratio of glycerol to DOD was maintained at 6:1 for maximizing the bioconversion process. As shown in Figure 4, DOD-MAG production increased rapidly over 7 h after incubation and was saturated thereafter. The maximum amount of DOD-MAG produced was 91.2 mg (per 100 mg of DOD), suggesting that 70.5% of DOD was converted into DOD-MAG. The degree of esterification was similar to the
Figure 1. GC analysis of the crude extract obtained from the coincubation of DOD, glycerol, and lipase Novozyme 435 for 12 h at 30 °C. IS represents the internal standard, and other analytical conditions are given in the Materials and Methods section.
This new peak was further analyzed via GC/MS for structure determination. The EI GC/MS data of the TMS derivative of the product are provided in Figure 2. There were several major fragments representing DOD moiety in the molecule. The intense fragment arising from alpha cleavage to the derivatized hydroxy group toward the methyl end resulted in the formation of two fragments, one at 215 m/z containing one TMS and the other at 343 m/z containing two TMS and a double bond. The minor fragment arising from alpha cleavage to the derivatized hydroxy groups toward the methyl end was observed at 441 m/z containing two TMS at the 7th and 10th carbon position and a double bond between the 8th and 9th carbon position in the 18-carbon fatty acyl chain. These results were consistent with the previous results corresponding to the description of DOD structure.2,4 Other EI spectra at 103 and 205 m/z indicated fragments of glycerol moiety containing sn1 and sn-1,2 hydroxyl groups, respectively. These results were
Figure 2. Electron-impact mass spectrum of the TMS derivative of the product shown as a question mark in Figure 1. Sample preparation and running conditions are given in the Materials and Methods section. 8193
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Figure 3. Schematic pathway for the production of DOD-MAG by esterifying DOD and glycerol using lipase Novozyme 435.
Figure 4. Time-coursed production of DOD-MAG using lipase Novzyme 435. Open circle and closed square represent the degree of esterification and production of DOD-MAG, respectively.
Figure 5. Effect of DOD and DOD-MAG on the cell growth of Staphylococcus aureus ATCC 6538. Closed circle and open circle represent DOD and DOD-MAG, respectively.
amount of DOD-MAG. The maximum degree of esterification was 71.2%. Antibacterial Activities of DOD-MAG. Antibacterial activity of DOD-MAG was determined and compared with that of DOD against S. aureus ATCC 6538. In the disk diffusion method, both DOD-MAG and DOD presented a dose-dependent increase in size of the clear zone on the same plate at a dosage of 50−400 μg (data provided in the Supporting Information). However, the size of the clear zone of DOD-MAG was substantially larger than that of DOD at each concentration, suggesting that the antibacterial activity of DOD-MAG was considerably stronger than that of DOD against S. aureus ATCC 6538. Because DOD-MAG exerted a stronger antibacterial activity against S. aureus ATCC 6538 than DOD, the minimal inhibitory concentrations (MIC) of DOD-MAG and DOD were also determined and compared against the same strain (Figure 5). As shown in this figure, the MIC value of DOD was 250 ppm. However, the MIC value of DOD-MAG decreased to 31.3 ppm, presenting 8 times lower value than that of DOD. These results confirmed that the transformation of DOD into its MAG form resulted in a remarkable enhancement of the original antibacterial activity of DOD against S. aureus ATCC 6538. Based on these results, the minimal inhibitory concentrations (MIC50) of DOD-MAG and DOD were also determined and compared against other well-known food-
born pathogenic bacteria (Table 1). MIC50 values of DODMAG against all the tested strains were 2−8 times lower than Table 1. Antibacterial Activities of DOD-MAG against Food-Born Pathogenic Bacteria bacteria
DOD(MIC50)a
DODMG(MIC50)a
Staphylococcus aureus ATCC 1621 (+)b Staphylococcus aureus ATCC 6538 (+)b Salmonella typhimurium KCTC 2515 (−)c Listeria monocytogenes ATCC 19111 (+)b Bacillus subtilis ATCC 6051 (+)b Corynebacterium glutamicum KACC 10784 (+)b Escherichia coli ATCC 8739 (−)c
31.3 62.5 125.0
15.6 15.6 31.3
125.0
31.3
62.5 125.0
31.3 31.3
250.0
31.3
a
Unit of MIC50 is μg/mL. bGram-positive. cGram-negative.
those of DOD. MIC50 values of DOD-MAG were in the range of 15.6−31.3 ppm, whereas those of DOD were in the range of 31.3−250 ppm. There was no significant difference in the MIC50 values of DOD-MAG against both Gram-positive and Gram-negative strains. 8194
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fields such as food, pharmaceutical, medicine, and cosmetics. However, for industrial application, further studies should focus upon maximum production under optimal reaction conditions. In conclusion, we were the first to report successful production of the MAG of a novel hydroxy fatty acid, DOD, by subjecting DOD to coincubation with glycerol and lipase. The conversion yield was fairly high, and the antibacterial properties of DOD against food-born pathogenic bacteria were highly enhanced after transformation into its monoacylglycerol form. Our results suggested that DOD-MAG could be used as a dual-functional industrial compound having both efficient antibacterial activity and amphipathic property.
DISCUSSIONS Generally, normal short- or medium-chain fatty acids are known to possess antimicrobial activities against viruses and bacteria.15,18 Some of them have been used as additives to milk formulas for preventing or reducing microbial infections in infants.19 Additionally, natural antimicrobial compounds are considered to be more acceptable as food additives than synthetic compounds. Recently, a hydroxy fatty acid, DOD, was produced in an ecofriendly manner from the natural vegetable oil via microbial bioconversion.5 DOD reportedly exerts strong antimicrobial effects on several plant pathogenic and food-borne pathogenic bacteria.6,7 Normal MAGs (a monoacylglycerol form of fatty acid) are known to have an amphiphilic property, augmenting wide application in hydrophobic food systems, pharmaceuticals, and cosmetics.20,21 Therefore, lipase-catalyzed production of functional fatty acid-containing MAGs, such as fish oils,22 conjugated linoleic acid,14 and medium-chain fatty acid,15,23 under mild conditions had previously been attempted. Some medium-chain fatty acids showed enhancement of their original antimicrobial activities against several bacteria after transformation into MAG form.15 In our system, we used DOD as a functional fatty acid to produce functional fatty acid-containing MAGs and to confirm any possible enhancement of the original antibacterial activities because DOD exerted a strong antibacterial effect against several pathogenic bacteria. Lipase-catalyzed production of DOD-MAG was successful and efficient, presenting over 70% conversion yield. This result was quite promising although the conversion yield should be maximized after further studies on optimization. Several 18-carbon fatty acids with different structural properties, such as oleic acid13 and conjugated linoleic acid,14 were used to produce different MAGs by employing the lipase enzyme. Their maximum conversion yields reached up to 90% under optimized conditions, although they were focused only on production, missing any studies about biological activities. A study conducted on the antimicrobial activity of MAGs mostly involved medium-chain fatty acids. Thormar et al. studied the microbicidal effects of several MAGs of mediumchain fatty acids against food-borne bacteria.23 Free capric acid (C10), out of the six different medium-chain fatty acids tested, was the most active against Campylobacter jejuni, but its MAG form (monocaprin) did not show any activity enhancement. Activities of caprylic acid and lauric acid were reduced after transformation into MAG. However, monocaprin and monolaurin showed enhanced activities mostly against S. aureus.15 In particular, lauric acid showed remarkable reduction in MIC values from 125−500 ppm with free fatty acids to 7.8− 31.3 ppm with MAG form depending upon the strains of S. aureus. However, the activities of those MAGs against Listeria and Bacillus species were relatively low and were not enhanced any further. Meanwhile, in our system, DOD was active against several food-borne bacteria including Gram-positive and Gram-negative strains, and the antibacterial activities of DOD after transformation into MAG form were consequently not limited to S. aureus alone. The enhancement of antibacterial activities of DOD-MAG was remarkable against all the food-borne bacteria tested, including S. aureus, S. typhimurium, L. monocytogenes, B. subtilis, Corynebacterium glutamicum, and E. coli. In this viewpoint, DOD-MAG seemed to have a high potential for application in broad industrial
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ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.9b03063.
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TLC analysis of the crude extracts obtained from coincubation of DOD, glycerol and different lipases; Effect of different lipases on the degree of esterification after coincubation of DOD, glycerol, and lipase; results of proton NMR analysis; results of 13C NMR analysis; Comparison of antibacterial activities of DOD and DOD-MAG against Staphylococcus aureus ATCC 6538(PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Phone and fax: 82-53-950-5754, 82-53-950-6750. ORCID
In Hwan Kim: 0000-0002-4984-3768 Hak-Ryul Kim: 0000-0002-9058-2774 Funding
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2018R1D1A3B07040443). Notes
The authors declare no competing financial interest.
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REFERENCES
(1) Bagby, M. O.; Calson, K. D. Chemical and biological conversion of soybean oil for industrial products. In Fats for the Future; Cambie, R. C., Ed.; Ellis Horwood Limited Press: Chichester, U.K., 1989; pp 301−317. (2) Hou, C. T.; Bagby, M. O.; Plattner, R. D.; Koritala, S. A novel compound, 7,10-dihydroxy-8(E)-octadecenoic acid from oleic acid by bioconversion. J. Am. Oil Chem. Soc. 1991, 68, 99−101. (3) Bae, J. H.; Suh, M. J.; Kim, B. S.; Hou, C. T.; Lee, I. J.; Kim, I. H.; Kim, H. R. Optimal production of 7,10-dihydroxy-8(E)hexadecenoic acid from palmitoleic acid by Pseudomonas aeruginosa PR3. New Biotechnol. 2010, 27, 352−357. (4) Chang, I. A.; Kim, I. H.; Kang, S. C.; Hou, C. T.; Kim, H. R. Production of 7, 10-dihydroxy-8(E)-octadecenoic acid from triolein via lipase induction by Pseudomonas aeruginosa PR3. Appl. Microbiol. Biotechnol. 2007, 74, 301−306. (5) Suh, M. J.; Baek, K. Y.; Kim, B. S.; Hou, C. T.; Kim, H. R. Production of 7,10-dihydroxy-8(E)-octadecenoic acid from olive oil by Pseudomonas aeruginosa PR3. Appl. Microbiol. Biotechnol. 2011, 89, 1721−1727.
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Article
Journal of Agricultural and Food Chemistry (6) Sohn, H. R.; Bae, J. H.; Hou, C. T.; Kim, H. R. Antibacterial activity of a 7,10-dihydroxy-8(E)-octadecenoic acid against plant pathogenic bacteria. Enzyme Microb. Technol. 2013, 53, 152−153. (7) Sohn, H. R.; Baek, K. Y.; Hou, C. T.; Kim, H. R. Antibacterial activity of a 7,10-dihydroxy-8(E)-octadecenoic acid against food-born pathogenic bacteria. Biocatal. Agr. Biotechnol. 2013, 2, 85−87. (8) Hou, C. T. New bioactive fatty acids. Asia Pac. J. Clin. Nutr. 2008, 17, 192−195. (9) Lawson, T. D.; Hughes, B. G. Human absorption of fish oil fatty acid as triacylglycerols, free acids or ethyl esters. Biochem. Biophys. Res. Commun. 1988, 152, 328−335. (10) Li, Z. Y.; Ward, O. P. Lipase-catalyzed esterification of glycerol and n-3 polyunsaturated fatty acid concentrate in organic solvent. J. Am. Oil Chem. Soc. 1993, 70, 745−748. (11) Li, Z. Y.; Ward, O. P. Synthesis of monoglyceride containing omega-3 fatty acids by microbial lipase in organic solvent. J. Ind. Microbiol. 1994, 13, 49−52. (12) Bornscheuer, U. T. Lipase-catalyzed syntheses of monoacylglycerols. Enzyme Microb. Technol. 1995, 17, 578−586. (13) Yesiloglu, Y.; Kilic, I. Lipase-catalyzed esterification of glycerol and oleic acid. J. Am. Oil Chem. Soc. 2004, 81, 281−284. (14) Watanabe, Y.; Yamauchi-Sato, Y.; Nagao, T.; Yamamoto, T.; Ogita, K.; Shimada, Y. Production of monoacylglycerol of conjugated linoleic acid by esterification followed by dehydration at low temperature using Penicillium camembertii lipase. J. Mol. Catal. B: Enzym. 2004, 27, 249−254. (15) Batovska, D. I.; Todorova, I. T.; Tsvetkova, I. V.; Najdenski, H. M. Antibacterial study of the medium chain fatty acids and their 1monoglycerides: Individual effects and synergistic relationships. Polym. J. Microbiol. 2009, 58, 43−47. (16) Thormar, H.; Isaacs, C. E.; Brown, H. R.; Barshatzky, M. R.; Pessolano, T. Inactivation of enveloped viruses and killing of cells by fatty acids and monoglycerides. Antimicrob. Agents Chemother. 1987, 31, 27−31. (17) Murray, P. R.; Baron, E. J.; Pfaller, M. A.; Tenover, F. C.; Yolke, R. H. Manual of Clinical Microbiology, 6th ed.; ASM: Washington, DC, 1995. (18) Hilmarsson, H.; Kristmundsdottir, T.; Thormar, H. Virucidal activities of medium- and long-chain fatty alcohols, fatty acids and monoglycerides against herpes simplex virus types 1 and 2: comparison at different pH levels. APMIS. 2005, 113, 58−65. (19) Isaacs, C. E.; Litov, R. E.; Thormar, H. Antimicrobial activity of lipids added to human milk, infant formula, and bovine milk. J. Nutr. Biochem. 1995, 6, 362−366. (20) Jackson, M. A.; King, J. W. Lipase-catalyzed glycerolysis of soybean oil in super critical carbon dioxide. J. Am. Oil Chem. Soc. 1997, 74, 103−106. (21) Sonntag, N. O. V. Glycerolysis of fats and methyl esters Status, review and critique. J. Am. Oil Chem. Soc. 1982, 59, 795A− 802A. (22) Byun, H. G.; Eom, T. K.; Jung, W. K.; Kim, S. K. Lipase catalyzed production of monoacylglycerols by the esterification of fish oil fatty acids with glycerol. Biotechnol. Bioprocess Eng. 2007, 12, 491− 496. (23) Thormar, H.; Hilmarsson, H.; Bergsson, G. Stable concentration emulsion of the 1-monoglyceride of capric acid(monocaprin) with microbial activities against the food-borne bacteria Campylobacter jejuni, Salmonella spp., and Escherichia coli. Appl. Environ. Microbiol. 2006, 72, 522−526.
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