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BY 4.0 license Open Access Published by De Gruyter Open Access November 30, 2023

Stability kinetics of orevactaene pigments produced by Epicoccum nigrum in solid-state fermentation

  • Sawinder Kaur EMAIL logo , Paramjit S. Panesar , Sushma Gurumayum , Jyoti Singh , Amine Assouguem EMAIL logo , Abderrahim Lazraq , Riaz Ullah , Essam A. Ali , Azra Skender and Prasad Rasane
From the journal Open Chemistry

Abstract

Orevactaene yellow pigment was produced by solid-state fermentation of broken rice using Epicoccum nigrum. The pigment was extracted using water as a solvent and subjected to stability studies at different temperatures (30, 40, 60, and 80°C), pH (4, 6, and 8), sterilization, and sunlight exposure treatment. The observed data were fitted in the first-order kinetic model. Yellow pigment stability was found to vary at different temperatures studied. At 30°C, only a 4% decrease in color intensity was observed after 2 h; at 40°C, an 8% decrease was observed, and at 80°C and pH 6.0, 17% of color intensity was lost. These results showed that the orevactaene pigment produced by E. nigrum is heat-sensitive and changes in color intensity should be expected in heat-processed products. After 180 min at 80°C, yellow pigments maintained 82 and 76% of the initial color at pH 6 and 8, while a 65% decrease in color intensity was observed at 80°C, pH 4. Autoclaving resulted in 69% decay and exposure of pigment to sunlight for 2 h showed 1% decay. The half-life period of the pigment at different temperatures varied from 82.5 to 5.25 h. The decimal reduction time decreased from 275 to 17.5 h with an increase in the temperature. Thermodynamic parameters for pigment decay at pH 6.0 were represented in terms of enthalpy ∆H, activation energy E a, free energy ∆G, and entropy ∆S. The values observed were 44.52–44.93, 48.48, 96.60–105.18 kJ/mol, and −170.50 to −171.85 J/mol/K, respectively. All these parameters help in predicting the quality changes in terms of appearance during thermal processing and optimizing the process.

1 Introduction

The application of food colors in processed food products is a considerable aspect in deciding the acceptability for both manufacturers and consumers. Approximately 39 colorants have been approved by the European Union to be used as food additives, whereas the United States has allowed about 36 [1]. According to global industry analysts, the market of food colors is anticipated to touch USD 2.97 billion by 2025 [2]. Among the different pigments available, carotenoids alone are anticipated to show a growth of 5.7% annually and increase up to $2.0 billion by 2022 [3].

Food colors used in the processed food industry are either produced synthetically or extracted from natural sources. Nevertheless, recently, the use of synthetic colors has steadily declined, owing to the allergic reactions shown by some of them, such as azorubin and tartrazine. The synthetic pigment tartrazine is a yellow color pigment and is highly poisonous to human lymphocyte cells. It is also shown to have toxic, cytotoxic, and mutagenic effects on plants, animals, and human cells [4,5]. Therefore, alternative sources of yellow pigments that are derived from natural or nature identical sources like plants and animals, including micro-organisms, have increased keeping in view the safety concerns about synthetic pigments [6,7]. Finding new sources of natural pigments in order to substitute synthetic pigments is in progress. Microorganisms have been attracting researchers’ attraction as a source of natural pigment in comparison to plant and animal sources [8]. Pigment synthesis using a microbial fermentation process has a number benefits, including relatively simpler extraction, increased product yields, plenty of substrates, no environmental barrier, and short span of time [9,10].

Microorganisms are recognized to secrete diversified forms of pigments as secondary metabolites, such as carotenoids, acyl phenol, naphthaquinones, fenazine, pyrone, anthraquinone, and sclertiorine [11]. Several studies have been reported on the fungus, Monascus purpureus, as it has been traditionally used for centuries as a food colorant in China, Taiwan, and Japan [12]. However, the production of mycotoxin citrinin along with the pigment in Monascus-fermented food has limited the use of these genera for natural colorant production [13]. Some species of Aspergillus sp. produce hydroxyanthraquinoid pigments in combination with various mycotoxins such as cyclochlorotine, citrinin, oxaline, secalonic acid, and rugulosin [14]. Some strains of Talaromyces species and Epicoccum nigrum have been discovered to produce pigment without co-producing mycotoxin [15]. E. nigrum is reported to produce polyketides, carotenoids, and flavanoids in different proportions depending on the strain and culturing conditions [9].

Heat processes are commonly used in the food processing industry for processing and preservation purposes in order to adhere to safety and stability specifications. These processes may result in physico-chemical reactions in foods causing quality degradation in terms of appearance, texture, and flavor [16]. Stability is one of the critical areas to be worked on for real-time food application and distribution [17]. Exhaustive information on the fate of pigments under different processing and storage conditions is required for the optimization of the process conditions for large-scale industrial processes [18]. Kinetic modeling provides useful insights into the mechanism of quality changes. Thermodynamic parameters, such as entropy, enthalpy, and activation energy data, may be used to predict the modifications in quality parameters of foods during different levels of heat treatments, thereby resulting in the designing of the optimized processing conditions. To the best of our knowledge, no work has been published on the stability study of orevactaene pigments produced by E. nigrum, which has the potential to become a natural colorant for the processed food industry.

The present study focuses on the stability studies of orevactaene, a pigment produced by E. nigrum, under different processing conditions using kinetic modeling.

2 Materials and methods

2.1 Solid-state fermentation

E. nigrum was isolated from agricultural fields of Lovely Professional University, Phagwara, Punjab, and identified by the National Fungal Culture Collection of India, Pune, was used for the study. Potato dextrose agar was used to grow the Epicoccum species, and it was sub-cultured for 15 days. For solid-state fermentation, 20 g of broken rice was taken, and the moisture content was maintained at 60% with distilled water. The flasks were stored at room temperature on the laboratory shelf for 1 h for moisture equilibration. The flasks were then autoclaved at 121°C for 20 min. The inoculum was prepared by scrapping the 7-day-old slant with 10 ml of distilled water. About 10% of inoculum was added to the autoclaved substrate and incubated at 25 ± 2°C for 10 days. After fermentation, the substrate was autoclaved and dried at 50°C for 24 h and milled to get the powder [9].

2.2 Extraction of pigments

For the extraction process, 0.8 g of the fermented matter was taken in a flask and distilled water was added to make the final volume of 50 ml. The flask was capped to avoid evaporation during the experiment. The flasks were incubated at 55.7°C for 57 min [9]. After incubation, the contents were filtered using Whatman filter paper number 1, and the filtrate was used for determining the orevactaene pigment spectrophotometrically (Shimadzu UV-1800, Japan) at a wavelength of 426 nm.

2.3 Pigment stability evaluation

To evaluate the stability of the pigment, the pigment solutions were maintained at pH 6.0 and incubated at different temperatures (30–80°C) for 0–240 min. The response of pH on pigment stability was studied at a constant temperature of 80°C and different pH values (4.0–8.0) for 0 to 180 min. Sodium citrate–phosphate and sodium phosphate buffers (0.2 M) were used to maintain the pH. Stability was also checked for the sterilization process (121°C for 15 min) and sunlight exposure for a period of 2 h. In all these treatments, absorbance was determined spectrophotometrically (Shimadzu UV-1800, Japan) at 426 nm [19].

2.4 Pigment degradation kinetics

Pigment degradation during the thermal treatment of pigment extracts follows first-order kinetics [20], demonstrating a logarithmic order of degradation given by

(1) A A 0 = exp ( kt ) .

The decimal reduction time (D value) is the time required for a one-log reduction of the initial absorbance at a given temperature and is related to reaction constant k as per equation (2):

(2) D = ln ( 10 ) k .

The half-life (t 1/2) of pigment degradation is given by equation (3):

(3) t 1 / 2 = ln ( 2 ) k .

2.5 Thermodynamic analysis

The activation energy, E a, was calculated using the Arrhenius equation, which relates the reaction rate constant to absolute temperature. The relation is given by equation (4):

(4) k = k 0 exp E a RT .

For a more precise determination of the activation energy, equations (1) and (4) can be combined to obtain equation (5):

(5) A A 0 = exp k 0 exp E a RT t ,

where A/A 0 indicates the residual absorbance (426 nm) at time interval t (min), k (min−1) is the pigment degradation rate constant at a given temperature, E a is the activation energy, k 0 is the Arrhenius constant, and R is the universal gas constant (8.31 J/mol K).

The Q 10 value is commonly used for illustrating the effect of temperature on biological reactions and is defined as the number of times a reaction rate changes with a 10°C change in the temperature. It is calculated by using equation (6):

(6) Q 10 = exp E a R 10 T 2 T 1

The relation between the temperature and degradation reactions occurring in foods during processing and storage can also be indicated in terms of z values. The relation of the z value and Q 10 is expressed as follows:

(7) z = 10 ln ( 10 ) ln ( Q 10 ) .

Thermodynamic parameters were evaluated using mathematical formulae based on the absolute reaction rate theory [21],

(8) k = K B T h e S * R e H * RT ,

where K B is the Boltzmann’s constant (1.38 × 10−23 J/K), h is the Planck’s constant (6.63 × 10−34 J s), ΔS* is the entropy of activation (J/mol K), and ΔH* is the enthalpy of activation (J/mol).

The enthalpy was calculated from the activation energy (E a) using the following equation:

(9) H * = E a RT .

The free energy of activation (ΔG*, kJ/mol) was calculated using the following equation:

(10) G * = H * T S * .

2.6 Data analysis

The experimental data were statistically evaluated based on the coefficient of determination (R 2), chi-square (χ 2), and standard error of the mean (SEM). These parameters of evaluations have been used successfully to correlate the degradation of bioactive compounds during thermal treatments. The variations in average values between various treatments were expressed as mean ± SE. One-way ANOVA, Duncan’s multiple range test in posthoc tests with probability P < 0.05 was used to test the differences in parameters under consideration using the SPSS statistical software (version 22) [19]:

(10) χ 2 = ( a measured a predicted ) 2 n p ,

(11) S EM = ( a measured a predicted ) 2 n ,

(12) R MSE = ( a measured a predicted ) 2 n ,

where p is the number of parameters and n is the number of observations.

3 Results and discussion

The characterization and evaluation of natural pigments are mainly based on absorption spectra obtained spectrophotometrically. Most of the degradative reactions are temperature-dependent and can result in a change in the intensity of color within due course of time. These changes in the spectral and visual properties are due to the structural changes caused by the thermal treatment [22]. Knowing the thermal stability of a colorant is important to designing productive strategies to prevent changes in visual appearance. The effect of temperature and pH on the stability of the orevactaene pigment was investigated.

3.1 Degradation kinetics

Kinetic models are commonly used to optimize the industrial process, save time, and minimize the effect of treatment on product quality [23]. The kinetic study of color degradation during thermal processing helps to quantify color under varied time–temperature combinations after knowing the order of a reaction.

Thermal degradation of the orevactaene pigment was investigated at 30, 40, 60, and 80°C at pH 6.0. The data were analyzed using the Arrhenius and first-order kinetic model. Figure 1 shows the good curve fitting using the first-order model. The values of the degradation rate constant (k), coefficient of determination (R 2), Chi-square (χ 2), SEM, and root mean square error (RMSE) are calculated and tabulated in Table 1. The extracellular pigment demonstrates good thermal resistance at lower temperatures as indicated by lower k values and highest at 80°C, suggesting higher stability at lower temperatures. The same is observed in the results of half-life (t 1/2) values at different temperatures as shown in Table 2.

Figure 1 
                  Thermal degradation kinetics of the orevactaene pigment exposed to different temperatures at pH 6.0. Error bars represent standard deviations (n  =  3).
Figure 1

Thermal degradation kinetics of the orevactaene pigment exposed to different temperatures at pH 6.0. Error bars represent standard deviations (n  =  3).

Table 1

Performance of the first-order degradation model at various temperatures

Temperature (°C) k (min−1) R 2 χ 2 SEM RMSE
30 0.00014 ± 0.00001 0.98 5.136 × 10−5 0.0001 0.0022
40 0.00024 ± 0.00003 0.93 0.00029 0.0008 0.0053
60 0.00072 ± 0.0001 0.92 0.00324 0.0086 0.0178
80 0.002 ± 0.0005 0.82 0.00228 0.0061 0.0150

K, rate constant; R 2, coefficient of determination; χ 2, chi-square; SEM, standard error mean; RMSE, root mean square error.

Table 2

Kinetic parameters of the thermal degradation of the orevactaene pigment at pH 6.0

Temperature (°C) k (min−1) t 1/2 (h) D value (h) z value (°C)
30 0.00014 ± 0.00001 82.5 ± 1.5 275 ± 13.5 37.42 ± 2.5
40 0.00024 ± 0.00003 41.25 ± 1.2 137.5 ± 16.07
60 0.00072 ± 0.0001 14.26 ± 2.0 47.53 ± 10.05
80 0.002 ± 0.0005 5.25 ± 2.25 17.5 ± 1.5

k, rate constant; t 1/2, half-life; D, decimal reduction time; and z, thermal death temperature. Data are presented as mean ± S.D. (n = 3).

Figure 2 shows the residual absorbance (A/A 0) of the pigment extract against time at different temperatures (30, 40, 60, and 80°C) investigated. It can be noticed that the color degradation rate increased as the temperature increased. Decreased color stability due to high temperatures is expected in most natural colors, but changes in pH can include various effects on natural colors [24,25]. The orevactaene pigment of E. nigrum is a nine-conjugated compound similar to β-carotene which when converted into solutions are more susceptible to isomerization and oxidative degradation reactions. Both light and heat influence the stability through radical-mediated oxidation reactions. The presence of oxygen and lower pH results in enhanced degradation as suggested by Arimboor et al. [26]. The kinetic parameters such as rate constant (k), activation energy values (E a), and half-life period (t 1/2) are important for predicting the fate of pigment during processing and storage. The first-order kinetic model has been frequently used to predict and characterize the thermal deterioration of natural and microbial pigments, such as anthocyanins [27] and Monascus pigment [19]. The fungal pigments obtained from Monascus and Penicillium have also been reported to follow first-order degradation kinetics. Morales-Oyervides et al. [28] reported that the red pigment secreted by P. purpurogenum GH2 is found to be stable at temperatures up to 80°C in the pH range of 4–8, while the red pigment produced by M. ruber is stable at lower temperatures ranging from 30 to 60°C at pH 6.0–8.0 [19].

Figure 2 
                  Effect of temperature and time on the residual absorbance of the orevactaene pigment.
Figure 2

Effect of temperature and time on the residual absorbance of the orevactaene pigment.

Reaction constants help characterize the kinetics of chemical reactions. The D values for thermal degradation of the orevactaene pigment secreted by E. nigrum using broken rice as a substrate ranged from 275 to 17.5 h in the temperature range of 30–80°C and the z value was found to be 37–38°C. The half-life period varied from 82.5 to 5.25 h at 30–80°C (Table 2). The effect of conventional heating on the P. purpurogenum GH2 pigment showed the D value range of 43.54–6.4 h and t 1/2 value range of 13.1–1.94 h in the thermal region of 60–90°C [29]. Silveira et al. [19] reported the D value range of Monascus pigment to be 357–34 h in the temperature range of 30–80°C, while the z value was varied for the same pigment, half-life period from 107.5 to 10 h. Chandran et al. [20] studied the degradation kinetics of beetroot color using different cooking methods; t 1/2 for beetroot puree color degradation ranged from 365 to 21 min for the temperature range of 50–120°C. The z value, 37.42°C, is the temperature required to shift the D value by 1log cycle. The z values of T. purpurogenus [30], P. purpurogenum GH2 [28], and M. purpureus [19] are 40.05, 48.7, and 50°C, respectively.

The degradation rate constants (k) were used to calculate the activation energy using the Arrhenius equation to ascertain the temperature-dependent behavior (equation 4). A plot between Ln k on the log scale and the reciprocal of the absolute temperature is used to find the activation energy. The k-values evaluated showed a good fit to the Arrhenius equation (Figure 3), thus contributing to the calculation of k 0 and E a. The activation energy, E a, represents the energy barrier that molecules need to cover so that one may react and is considered an important criterion for analyzing the thermal stability of the pigment [31].

Figure 3 
                  Arrhenius equation graph of constants of orevactaene degradation.
Figure 3

Arrhenius equation graph of constants of orevactaene degradation.

The E a of the orevactaene pigment obtained from E. nigrum obtained is 47.48 kJ/mol. In the degradation of Monascus pigments, E a was 40.8 kJ/mol [19] and for the water-soluble extracellular pigment produced by T. purpurogenus it was 52.50 kJ/mol [30]. However, for other yellow food colorants like lutein, riboflavin, curcumin, β-carotene, gardenia yellow, and Opuntia betaxanthins, E a values were 3.2, 36.4, 23.7, 6.5, 31.2, and 43.7 kJ/mol, respectively [22]. The E a value for the onion solid waste pigment was 12.11 kJ/mol [32].

The calculated value of k 0 for the orevactaene pigment was 10.40 min−1. The first-order model and Arrhenius equation can be combined as per equation (5) as follows:

(6) A A 0 = exp 10.40 exp 5832 8.314 T t .

These combined equations give an idea of the effect of time and temperature combination on pigment stability in terms of the residual pigment, which is an important parameter in the food industry. Orevactaene discoloration varied at 30, 40, 60, and 80°C. At 30°C, only 12% decrease in the color intensity was observed after 4 h; at 40°C,31% decrease; and at 80°C, 56% of the color was lost (Figure 2). The results showed that the orevactene pigment produced by E. nigrum is heat sensitive and changes in color intensity can be expected in heat-processed products. Similar results are reported for Monascus pigments by Abdollahi et al. [24] and Gjadhar and Mellem [33] for the Serratia marcescens pigment. However, further studies can be conducted to see the interactive effect of different food components on the stability of pigment.

The estimation of thermodynamic parameters may provide information related to the rate of pigment degradation under the influence of temperature and structure modification. Table 3 shows the calculated values of ∆H*, ∆G*, and ∆S*. For the orevactaene pigment, in the thermal region of 303–353 K, the enthalpy of activation (ΔH*) ranged from 44.52 ± 1.55 to 44.93 ± 1.51 kJ/mol, the entropy of activation (∆S*) ranged from −170.5 ± 7.5 to −171.85 ± 8.2 J/mol K, and the free energy of activation (∆G*) ranged from 96.60 ± 3.5 to 105.18 ± 2.2 kJ/mol.

Table 3

Thermodynamic parameter values for the orevactaene pigment decay at pH 6.0

Temperature (K) E a (kJ/mol) H* (kJ/mol) G* (kJ/mol) S* (J/mol K)
303 47.48 ± 1.64 44.93 ± 1.51 96.60 ± 3.5 −170.50 ± 7.5
313 44.85 ± 1.55 98.47 ± 1.5 −171.29 ± 8.1
333 44.69 ± 1.47 101.89 ± 1.9 −171.78 ± 8.5
353 44.52 ± 1.55 105.18 ± 2.2 −171.85 ± 8.2

E a, activation energy; ∆H*, enthalpy of activation; ∆S*, entropy of activation; and ∆G*, free energy of activation. Data are presented as mean ± S.D.

The values of ∆H* for the thermal degradation represent a measure of the amount of non-covalent bonds ruptured and thus the conformational changes in the pigment. The decreasing values of ∆H* with an increase in temperature indicate a change in conformation [18,34] The positive value of ∆H* represents a gain in energy by the system and involves the conversion of reactants to products by bond rupturing. The ∆H* data are in confirmation with the previously reported data for fungal pigments. However, the enthalpy changes observed for the P. purpurogenum pigment was 39.88–39.47 kJ/mol in the temperature range of 303–353 K [28], and 38.29–37.88 kJ/mol for the Monascus pigment at 303–353 K [19], and T. purpurogenus showed an enthalpy change of 49.98–49.48 kJ/mol at 303–363 K [30]. ∆S* measures the degree of disorderliness of the system. From a thermodynamic point of view, ∆G* values indicate that degradation reaction conditions are not supportive at higher temperatures [19], which may be because of the negative entropic contribution in the degradation process. Negative ∆S* values indicate that the system shows a low level of disorder in the system [18,34]. Negative ∆S* values along with positive ∆H* and ∆G* values confirm the endothermic, non-spontaneous nature of the reaction.

The stability of Epicoccum pigments at different pH values was studied at 80°C. Figure 4 shows the % residual absorbance at three different pH values under investigation. The degradation kinetics was found to be influenced by pH as a higher amount of degradation is observed at lower pH. At acidic pH, i.e., pH 4, pigment precipitation was observed which may restrict its use in acidic foods. After 180 min, yellow pigments maintained 82 and 76% of the initial color at pH 6 and 8 (Figure 4). This is further confirmed by the changes in half-life values of the pigment which increases with increase in pH (Table 4). At high temperatures, with increased pH, there is an increase in the stability of pigments. Similar results have been reported for red pigments produced by Monascus, which, at 80°C and pH 4 and 5, showed colloidal instability [19]. Red pigment showed retention of 81, 84, and 85% at pH 6, 7, and 8, respectively, when treated at 80°C for 180 min.

Figure 4 
                  Effect of pH and time on the residual absorbance of the orevactaene pigment at 80°C.
Figure 4

Effect of pH and time on the residual absorbance of the orevactaene pigment at 80°C.

Table 4

Kinetic parameters of the degradation of the orevactaene pigment at pH 4.0, 6.0, and 8.0 and temperature of 80 °C

pH k (min−1) R 2 t 1/2 (h) D value (h)
4.0 0.0105 ± 0.0002 0.85 1.1 ± 0.5 3.65 ± 1.5
6.0 0.0015 ± 0.0001 0.94 7.7 ± 1.1 25.55 ± 2.0
8.0 0.001 ± 0.0005 0.95 11.55 ± 2.5 38.33 ± 1.5

k, rate constant; t 1/2, half-life, and D, decimal reduction time.

Autoclaving treatment was also performed for Epicoccum pigments, which resulted in a 69% degradation color. Natural pigments commonly show such a level of degradation, which can be compensated by proper pigment dosage. The stability of pigments during sunlight exposure was also checked. Pigments were exposed to sunlight for 2 h from 12 to 2 p.m., which resulted in only 1% degradation of the color. The degradation of color observed in the present study is the same as that commonly found in natural pigments [24].

4 Conclusion

The thermal and pH stability of the orevactaene pigment produced by E. nigrum was discussed in this work. The yellow orevactaene pigment produced by E. nigrum was found to be sensitive to temperature and pH changes. At high temperatures and low pH, the pigment was unstable and the stability increased as pH approached neutrality. These results showed that the orevactaene pigment produced by E. nigrum is heat- and pH-sensitive, and changes in color intensity should be expected in heat-processed products. Thermodynamic parameters might help in designing the thermal treatments in order to enhance the thermal stability of the pigment.

Acknowledgement

The authors acknowledge the support and infrastructure facilities provided by Lovely Professional University, Phagwara, Punjab (India), for the research work. Authors Also wish to thanks Researchers Supporting Project Number (RSP2023R110) at King Saud University Riyadh Saudi Arabia for financial Support.

  1. Funding information: This study was funded by researchers supporting project (number RSP2023R110), King Saud University, Riyadh, Saudi Arabia.

  2. Author contributions: Sawinder Kaur: conduct of experimentation, writing original draft, revision; Parmjit S. Panesar: conceptualization and supervision; Prasad Rasane: reviewing and supervision; Jyoti Singh: reviewing; Sushma Gurumayum: conceptualization and supervision; Amine Assouguem; software, reviewing and supervision; Abderrahim Lazraq; reviewing and supervision; Riaz Ullah; writing review and editing; Essam A Ali; reviewing and supervision; Azra Skender, writing review and editing.

  3. Conflict of interest: The authors state no conflicts of interest in this work.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-09-27
Revised: 2023-10-27
Accepted: 2023-11-15
Published Online: 2023-11-30

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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