Formation of Melatonin and Its Isomer during Bread Dough

Article pubs.acs.org/JAFC

Formation of Melatonin and Its Isomer during Bread Dough Fermentation and Effect of Baking Cemile Yılmaz, Tolgahan Kocadağlı, and Vural Gökmen* Department of Food Engineering, Hacettepe University, 06800 Beytepe, Ankara, Turkey S Supporting Information *

ABSTRACT: Melatonin is produced mainly by the pineal gland in vertebrates. Also, melatonin and its isomer are found in foods. Investigating the formation of melatonin and its isomer is of importance during bread dough fermentation and its degradation during baking since bread is widely consumed in high amounts. Formation of melatonin was not significant during dough fermentation. The melatonin isomer content of nonfermented dough was found to be 4.02 ng/g and increased up to 16.71 ng/g during fermentation. Lower amounts of isomer in crumb and crust than dough showed that the thermal process caused a remarkable degree of degradation in melatonin isomer. At the end of the 180 min fermentation Trp decreased by 58%. The results revealed for the first time the formation of a melatonin isomer in bread dough during yeast fermentation. KEYWORDS: melatonin, melatonin isomer, bread dough fermentation, Saccharomyces cerevisiae, tryptophan

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INTRODUCTION Melatonin (N-acetyl-3-(2-aminoethyl)-5-methoxyindole) is an indoleamine synthesized from L-tryptophan metabolism via serotonin.1 Melatonin has a significant role in regulation of the circadian rhythm and mitigation of sleeping disorders and has many more physiological functions.2 Melatonin can directly scavenge free radical species and stimulate the activity of antioxidant enzymes.3 Although melatonin is produced mainly by the pineal gland in vertebrates1 it might be synthesized in different sites of an organism such as retina, pancreas, skin, bone marrow, and gut.4 Whether melatonin in the gastrointestinal tract is produced by gut tissue or gut symbiotic microorganisms is still unknown.5 Beside vertebrates, melatonin is also found in bacteria, algae, fungi, insects, and plants.6 Tryptophan, an essential amino acid, is the precursor of melatonin in vertebrate pineal gland. Four enzymes including tryptophan hydroxylase (TPH), aromatic amino acid decarboxylase (AAAD), arylalkylamine N-acetyltransferase (AANAT), and N-acetylserotonin methyltransferase (ASMT) are involved for the biosynthesis of melatonin from tryptophan.1 However, the biosynthetic pathway of melatonin can be different in plants as compared to vertebrates. In the first reaction of melatonin synthesis in a plant, as shown in rice, tryptophan decarboxylation occurs rather than hydroxylation.7 Moreover AANAT has not yet been found in higher plants to date.8 Saccharomyces cerevisiae species are widely used in the food industry such as in bread making and beer and wine production. Recent studies have indicated that melatonin is produced by the alcoholic fermentation of yeasts in red wine and beer samples.9,10 Moreover, yeasts are able to synthesize melatonin isomer in red wine samples.5,11,12 The molecular structure of melatonin, 1, and the hypothetical structure of the isomer, 2, identified in foods are shown in Figure 1. It was reported that melatonin and melatonin isomer synthesis largely depended on the growth phase of the yeasts and the concentration of tryptophan, reducing sugars, and the growth © 2014 American Chemical Society

Figure 1. Molecular structures of melatonin, 1, and melatonin isomer, 2, identified in foods.

medium.12,13 It was also reported that yeast fermented foods contain severalfold higher melatonin isomer levels than those fermented by bacteria.14 However, the biosynthetic pathway of melatonin isomer formation is still unknown. Melatonin isomer shows antioxidant and cytoprotective activity, depending on a change in the position of the two substituents on the indole ring.15 Therefore, formation of melatonin isomer in bread during fermentation might contribute to nutritional value. However, there is no information on the bioavailability and biological consequences of melatonin isomer. Since bread is widely consumed in high amounts, investigating the formation of melatonin isomer is of importance during fermentation and its degradation during baking. The goal of this study was to investigate the formation of melatonin and its isomer during bread dough fermentation Received: Revised: Accepted: Published: 2900

January 17, 2014 March 10, 2014 March 11, 2014 March 11, 2014 dx.doi.org/10.1021/jf500294b | J. Agric. Food Chem. 2014, 62, 2900−2905

Journal of Agricultural and Food Chemistry

Article

L. Working solutions of melatonin were prepared in ethanol−water (50:50, v/v). Determination of the melatonin isomer was semiquantitative, and its content was calculated from total ion chromatogram (sum of the area of the MRM transitions (233.2 → 174.2 and 233.2 → 216.2) of melatonin). The linearity was evaluated by plotting the peak area against the concentrations of melatonin standards. Limit of detection (LOD) and limit of quantitation (LOQ) were determined at a signal-to-noise ratio of 3 and 10, respectively. Analysis of Free Amino Acids. Extraction. One gram of sample (dough, ground crumb, and ground crust) was extracted with water in three stages (10, 5, and 5 mL) by vortexing (3 min). After centrifugation (7500g for 5 min) in each stage, supernatants were collected in a test tube. Combined extract was diluted subsequent to centrifugation with a mixture of acetonitrile−water (50:50, v/v), and a part of the diluted extract was filtered through a 0.45 μm syringe filter into an autosampler vial prior to LC−MS/MS analysis. LC−ESI-MS/MS Analysis. The analysis of free amino acids was carried out according to the method described previously.17 An Agilent 1200 series HPLC system coupled to an Agilent 6460 triple quadrupole mass spectrometer (Waldbronn, Germany) was used. The chromatographic separations were performed on a SeQuant ZICHILIC column (150 mm × 4.6 mm i.d., 3.5 μm) using a gradient mixture of 0.1% formic acid in water (A) and 0.1% formic acid in acetonitrile (B) at flow rate of 0.75 mL/min at 40 °C. The eluent composition starting with 25% of A was linearly increased to 60% in 5 min and was held for 5 min. Then, it was linearly decreased to its initial conditions (25% of A) in 5 min. Electrospray ionization was operated in positive mode. The electrospray source had the following settings: drying gas (N2) flow of 10 L/min at 325 °C, nebulizer pressure of 30 psi, sheath gas (N2) flow of 10 L/min at 375 °C, nozzle voltage of 1000 V, and capillary voltage positive of 4000 V. Amino acids were identified by their specific MRM transitions, and the dwell time was 0.1 s for all. Concentration of amino acids was calculated by means of external calibration curves built for individual amino acids in a range between 0.1 and 5.0 mg/L. Statistical Analysis. The results were reported as mean ± standard deviations. Significant differences (p < 0.05) were evaluated by Duncan test after the analysis of variance (ANOVA), by using SPSS 17.0 statistical package.

and baking. Additionally, changes in free amino acids were also determined during fermentation, especially to evaluate tryptophan consumption by yeasts.

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MATERIALS AND METHODS

Chemicals and Consumables. Acetonitrile (HPLC grade), ethanol (HPLC grade), and melatonin (N-acetyl-5-methoxytryptamine) (>98%) were obtained from Sigma-Aldrich (Steinheim, Germany). Formic acid (98%) and high-purity (>98%) alanine (Ala), arginine (Arg), asparagine (Asn), aspartic acid (Asp), glutamic acid (Glu), glutamine (Gln), glycine (Gly), histidine (His), isoleucine (Ile), leucine (Leu), lysine (Lys), methionine (Met), phenylalanine (Phe), proline (Pro), serine (Ser), tryptophan (Trp), tyrosine (Tyr), valine (Val), and γ-aminobutyric acid (GABA) were purchased from Merck Co. (Darmstadt, Germany). Ultrapure water was used throughout the experiments (Milli Q-System, Millipore, Milford, MA, USA). Syringe filters (nylon, 0.45 μm) were purchased from Waters (Milford, MA). ZORBAX Rapid Resolution SB-C18 column (50 mm × 4.6 mm i.d., 3.5 μm) and SeQuant ZIC-HILIC column (150 mm × 4.6 mm i.d., 3.5 μm) were supplied by Agilent Technologies (Waldbronn, Germany) and Merck Co. (Darmstadt, Germany), respectively. Preparation of Dough and Breads. All-purpose wheat flour (Söke Un, Turkey), sugar (Bal Küpü, Turkey), salt (Billur Tuz, Turkey), and instant baker’s yeast (Saccharomyces cerevisiae) (Yuva, Turkey) for preparing breads were purchased from a local market. Breads were prepared using the AACC (American Association of Cereal Chemists) Method 10-10.03 (1983) with some modification.16 100 g of wheat flour, 38 mL of water, and 20 mL of yeast suspension composed of 5.3 g of instant yeast and 11 mL of sugar−salt solution containing 6 g of sugar and 1.5 g of salt were mixed with a mixer until dough development. After the dough was divided into equal pieces, the pieces were fermented at 30 °C for 0 (control), 30, 60, 90, 120, and 180 min. During fermentation, punching was carried out every 30 min. Before baking, a small piece of fermented dough was set apart and stored at −20 °C for melatonin and amino acid analysis. Following fermentation, the dough was baked in a temperature-controlled oven (Memmert Une 400, Germany) at 215 °C for 17 min. Analysis of Melatonin and Melatonin Isomer. Extraction. Crumb and crust samples were ground with a grinder prior to analysis. Two grams of sample (dough, ground crumb, and ground crust) was extracted with ethanol in three stages (5−2.5−2.5 mL) by vortexing (3 min). After centrifugation (7500g for 5 min) in each stage, supernatants were collected in a test tube and evaporated to dryness under a gentle stream of nitrogen. The final residue was redissolved in 1 mL of ethanol−water (50:50, v/v). After centrifugation (13000g) supernatant was passed through a 0.45 μm syringe filter into an autosampler vial prior to LC−MS/MS analysis. LC−ESI-MS/MS analysis. The analysis of melatonin and its isomer was carried out according to the method described previously.14 Melatonin was determined by using an Agilent 1200 series HPLC system coupled to an Agilent 6460 triple quadrupole mass spectrometer (Waldbronn, Germany). The chromatographic separations were performed on a ZORBAX Rapid Resolution SB-C18 column (50 mm × 4.6 mm i.d., 3.5 μm) using a mixture of 0.1% formic acid in water and 0.1% formic acid in acetonitrile (65:35, v/v) at a flow rate of 0.5 mL/min at 40 °C. The injection volume was 5 μL. The electrospray source had the following settings: drying gas (N2) flow of 10 L/min at 325 °C, nebulizer pressure of 30 psi, sheath gas (N2) flow of 10 L/min at 375 °C, nozzle voltage of 1000 V, and positive capillary voltage of 4000 V. MS data were acquired in the positive mode, and melatonin was identified by multiple reaction monitoring (MRM). Fragmentor voltage of precursor ion was 80 V. The ion transitions for melatonin were determined as 233.2 → 174.2 (collision energy of 10 V) and 233.2 → 216.2 (collision energy of 4 V). A dwell time was set at 250 ms for each. The 233.2 → 174.2 MRM transition was selected to quantitate melatonin. Concentration of melatonin was calculated by means of external calibration curves covering the range between 0.05 and 20 μg/

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RESULTS AND DISCUSSION Evaluation of Analytical Method. The chromatographic separation and ion transitions of melatonin and its isomer are given in Figure 2. Retention time, specific MRMs (233.2 → 174.2 and 233.2 → 216.2), and fragment ion ratios acquired from the standard compound were used to confirm the presence of melatonin in the samples. Figure 2A illustrates the chromatogram of 1 ng/mL melatonin standard for the MRM transitions of 233.2 → 174.2 (upper panel) and 233.2 → 216.2 (bottom panel). Since relative abundance of the fragment ion of 174.2 was higher than that of 216.2 for melatonin, the fragment ion of 174.2 was used for the quantitation of melatonin. The ratio of 174.2/216.2 for melatonin was found to be 14.2 ± 2.0. The fragment ion 174.2 originates from the cleavage of amide substituent (−NH2COCH3) from main ion and 216.2 by OH removal. Although the melatonin isomer has the same fragment ions, their ratios were found to be quite different. The abundance of fragment ion 216.2 was much higher than that of 174.2 in the fragmentation pattern of the isomer. Diamantini et al.18 indicated that 174.2 is the base peak for all isomers except where the substituent is bound to nitrogen of the pyrole ring. Therefore, the possible molecular structure of the melatonin isomer, 2, was proposed as shown in Figure 1. However, the position of the methoxy group on the indole ring could not be determined by tandem mass spectrometry. The purification of the isomer is needed for the identification of exact molecular structure by using either NMR spectroscopy or X-ray 2901

dx.doi.org/10.1021/jf500294b | J. Agric. Food Chem. 2014, 62, 2900−2905


Article

curve of melatonin was used. Although the abundant ion of 216.2 is suitable for the quantitation of the isomer, its abundance in fragmentation of melatonin itself was very low, i.e., the transition ratio of 233.2/216.2 is quite different as mentioned. Thus, sum of the ions of 174.2 and 216.2 was used for calibration and quantitation of the isomer in the samples as reported previously.14 An external calibration was built for 0.05−20 ng/mL with melatonin standard, and a good linearity was obtained for the fragment ion 174.2 and for the sum of both fragments. Linearity equations of y = 595.1x + 68.3 and y = 629.5x + 54.1 and good correlation coefficients (R2 = 0.9998 and 0.9997, respectively) were obtained in both quantitations. LOD values of melatonin were 0.03, 0.05, and 0.03 ng/g and LOQ values of melatonin were 0.10, 0.18, and 0.09 ng/g for dough, bread crumb, and bread crust samples respectively. Formation of Melatonin. Figure 3A illustrates the effect of fermentation time on melatonin in bread dough. According to

Figure 2. LC−MS/MS chromatograms for (A) 1.0 ng/mL melatonin standard, (B) bread crumb (nonfermented). Upper panel illustrates the MRM of 233.2 → 174.2, and lower panel illustrates the MRM of 233.2 → 216.2 (1, melatonin; 2, melatonin isomer). Figure 3. Change of the concentrations of (A) melatonin and (B) melatonin isomer in bread dough during fermentation (on dry matter basis).

diffraction spectroscopy. Other investigators have also observed similar fragmentation patterns.12,19 Vitalini et al.11 used MS/MS and Orbitrap MS with a collision cell, but they did not mention the 233.2 → 216.2 transition for the detection of melatonin and its isomer. Figure 2B illustrates the chromatogram of bread crumb prepared from nonfermented dough for the MRM transitions of 233.2 → 174.2 (upper panel) and 233.2 → 216.2 (bottom panel). As shown in Figure 2B, bread crumb contained melatonin isomer having relatively shorter retention time (2.1 min) than melatonin (2.8 min). Differently from melatonin, relative abundance of the fragment ion of 216.2 was higher than that of 174.2 and the ratio of 216.2/174.2 for melatonin isomer was found to be 2.9 ± 0.2. Since there was no standard compound found for the melatonin isomer, it was specifically distinguished from melatonin by retention time and fragment ion ratio. For quantitation of melatonin isomer, calibration

results, nonfermented dough was found to contain 0.07 ng/g melatonin. At the end of the 30, 60, 90, 120, and 180 min of fermentation, 0.05 ( 0.05). 2903



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Table 1. Concentration of Free Amino Acids (μg/g) in Dough during Fermentationa fermentation time, min 0 Ala Arg Asn Asp Glu Gln Gly His Ile Leu Lys Met Phe Pro Ser Trp Tyr Val GABA total a

395.0 250.9 169.1 232.9 1142.8 272.4 76.8 26.0 129.4 180.8 133.7 75.6 198.5 126.5 118.8 597.3 24.9 157.9 163.5 4472.0

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

30 32.9 a 14.6 a 12.1 a 2.6 a 3.9 a 26.0 a 6.2 a 2.7 a 28.3 a 4.7 a 25.5 a 15.9 a 38.8 a 5.9 a 9.7 a 27.2 a 4.3 a 25.9 a 25.2 a 293.8 a

369.5 244.5 149.4 226.3 791.7 260.7 83.8 24.2 124.6 171.9 140.4 67.3 190.3 126.3 112.9 526.1 23.6 145.9 239.1 4018.6

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

60 0.5 a 13.8 ab 0.1 a 0.0 a 41.4 b 19.4 ab 0.5 a 1.9 a 18.4 ab 9.2 a 21.2 a 13.9 ab 36.2 ab 1.4 a 7.5 ab 23.4 b 2.3 a 19.5 a 13.3 b 93.7 ab

90

354.8 ± 12.7 ab 231.5 ± 7.14 ab 119 ± 4.6 b 220.7 ± 1.3 ab 693.9 ± 0.1 c 232.4 ± 16.2 abc 79.3 ± 9.3 a 19.5 ± 0.8 ab 103.2 ± 13.3 ab 139.1 ± 4.9 b 129.9 ± 26.3 a 45.0 ± 7.3 ab 168.2 ± 25.2 ab 131.1 ± 1.8 a 104.5 ± 6.6 ab 480.0 ± 17.8 b 23.1 ± 2.3 a 137.3 ± 14.1 a 269.9 ± 11.3 bc 3682.8 ± 112.2 bc

303.7 221.2 73.0 195.6 545.5 192.4 86.6 15.4 82.7 109.5 109.6 40.9 141.6 130.3 83.9 426.8 22.3 122.1 292.9 3196.3

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

120

19.0 bc 9.7 bc 2.7 c 12.9 bc 11.0 d 25.7 bcd 14.1 a 4.3 b 25.1 ab 4.2 c 34.6 a 13.4 ab 29.5 ab 0.3 a 12.9 abc 26.9 c 2.9 ab 14.3 ab 17.0 c 196.3 cd

277.0 201.5 42.9 184.3 493.8 170.0 93.5 15.3 79.3 102.1 120.7 41.7 130.0 135.9 75.0 372.6 21.7 104.5 307.6 2969.7

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

25.8 c 12.0 c 13.9 d 21.4 c 26.5 e 40.3 cd 12.6 a 5.4 b 29.0 ab 5.2 cd 35.8 a 16.7 ab 46.6 ab 7.8 a 27.0 bc 7.7 d 4.5 ab 31.0 ab 18.7 c 377.7 d

180 161.8 138.2 30.6 76.2 272.5 157.3 87.6 14.0 62.8 92.0 136.9 37.1 97.7 133.5 65.3 251.9 14.2 73.1 298.1 2200.8

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

18.3 d 1.8 d 10.4 d 10.8 d 9.8 f 29.9 d 11.3 a 3.0 b 25.3 ab 4.7 d 28.0 a 14.5 b 37.8 b 2.8 a 15.7 c 1.8 e 3.7 b 23.9 b 11.4 c 261.4 e

Values followed by different spaced letters are significantly different within each row (p < 0.05). Concentrations were given on dry matter basis.

which higher temperatures were attained during the process. It is a fact that the degradation products of melatonin and its isomer are unknown, but this needs further clarification. Primarily, the precise structure of the melatonin isomer needs to be revealed. Since bread as a yeast leavened staple food appears as the major source of melatonin isomer, its biological consequences should be investigated in depth.

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ASSOCIATED CONTENT

S Supporting Information *

Figure depicting degradation kinetics of total amino acids and tryptophan in bread dough during fermentation. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel: +90-312-2977108. Fax: +90-312-2992123. E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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REFERENCES

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Figure 5. Baking effect on (A) tryptophan and (B) total free amino acid content of breads fermented for 120 min (on dry matter basis).

This indicated a potential role of Trp in the formation mechanism during yeast fermentation. At extreme conditions applied during baking, concentration of melatonin isomer significantly decreased in bread. Comparing to crumb, this effect was more pronounced in the crust part expectedly, in 2904



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Formation of Melatonin and Its Isomer during Bread Dough

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