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. 2023 Feb 20;17:100606. doi: 10.1016/j.fochx.2023.100606

Effects of cooling rates during depuration on the quality of Pacific oysters (Crassostrea gigas) at anhydrous preservation stage

Shijie Bi a,b, Changhu Xue c, Yunqi Wen c, Xin Du c, Qianqian Xue c, Zhaojie Li c, Hongying Liu b,d,⁎
PMCID: PMC10039261  PMID: 36974177

Highlights

  • •

    The slow gradient cooling rate was beneficial to ensure the survival rate of oysters.

  • •

    Oysters had well quality in the slow gradient cooling rate.

  • •

    The slow gradient cooling rate was beneficial to reduce the stress of oysters.

  • •

    Oysters had higher quality in the slow gradient cooling rate process.

Keywords: Depuration, Anhydrous preservation, Cooling rate, Quality, Oyster

Abstract

The Pacific oyster could be affected by several pressure sources during cold chain logistics, which reduce the quality of oyster, and even improve its mortality. For improving the quality of oyster, the effects of depuration process at different cooling rates (1, 3, 7, 11 and 16 °C/h) on selected Pacific oyster were studied. The results indicated that extreme fluctuations in the depuration temperatures could affect the survival rates and qualities of oysters. The oysters exhibited low survival rates, glycogen contents and pH values at an increased cooling rate. Their contents in the 1 °C/h group after 3 d preservation were 100 %, 16.30 ± 1.64 mg/100 g and 6.72 ± 0.01, respectively, while there were 71 %, 7.72 ± 0.88 mg/100 g and 6.53 ± 0.01 in the 16 °C/h group after 3 d preservation, respectively. Furthermore, the ATP-related compounds were affected by the different cooling rates. AMP and IMP were the main ATP-related compounds, and their contents in the 1 °C/h group after 3 d preservation were 37.21 ± 1.10 mg/100 g and 29.47 ± 1.10 mg/100 g, respectively, while there were 32.07 ± 1.10 mg/100 g and 13.16 ± 1.60 mg/100 g in the 16 °C/h group after 3 d preservation, respectively. The proportions of the total umami, as well as the sweet amino acids also decreased, the proportions of the umami amino acids and sweet amino acids in the total amino acids, were 31.37%–38.80%, and their proportions in 1 °C/h group were higher than that in 16 °C/h group. Conversely, the fatty acid content of each group exhibited significant differences. Combined with the above results, the oyster maintained a high survival rate and higher quality at a cooling rate of 1 °C/h during depuration.

1. Introduction

The aquaculture of bivalve mollusks plays an essential role in marine fishery resources worldwide (Sun, Liu, Lin, Zhang, & Guo, 2018). Particularly, the Pacific oyster (Crassostrea gigas) accounts for the most popular shellfish globally (Pauly & Zeller, 2017). Owing to their abundant nutritional values and tender meat, oysters enjoyed a reputation as “Undersea Milk” and became a major maricultural species in the past few decades (Gao et al., 2021), with a total aquaculture production of 5,450.3 thousand tons in the whole world (FAO, 2022).

The demand for aquatic products quantity is increasing with the increasing understanding of their nutritional values, especially fresh ones (Barrento, Lupatsch, Keay, & Christophersen, 2013). However, the circulation of aquatic products restricts their survival rates and freshness because aquatic products are subjected to different pressure conditions, including prolonged exposure to the air and temperature fluctuations during their capture, depuration and preservation/transportation (Lee, Mattheis, & Rudell, 2012). These stressors severely reduce the qualities of aquatic products, even accounting for their deaths, and cause significant economic losses in the supply chain (Anacleto et al., 2013). Therefore, it is essential to establish scientific and effective depuration and transportation methods to decrease the loss of nutrition values of aquatic animals. The depuration and preservation/transportation of living aquatic products have attracted enormous research interests to improve their qualities and increase their trade chain value (Chen et al., 2022).

Depuration is a process required by shellfish for human consumption. It includes keeping shellfish in sterile seawater with sufficient oxygen and without feed for 48 h to reduce the content of potentially pathogenic microorganisms and ensure the health and safety of products (Anacleto et al., 2013). Anhydrous preservation means that fresh aquatic products do not use water as the medium of transportation during transportation, and aquatic animals directly contact with environmental gases (Chen et al., 2015). Recently, most investigations have mainly focused on the changes in microbe (Fuhrmann, Delisle, Petton, Corporeau, & Pernet, 2018), chemical contaminations (Freitas et al., 2012), metal levels (Marin et al., 2005, Sun et al., 2018), physiological/ecological responses and immune responses (Chen et al., 2021, Guo et al., 2015) of shellfish during depuration and anhydrous preservation. Temperature is an important factor in shellfish depuration. At present, most studies focus on the effect of purification temperature on heavy metals and microorganisms in shellfish (Chinnadurai et al., 2022, Tokarskyy et al., 2019), only a few studies have investigated the changes in the qualities of oysters during the reduction of temperature stress in depuration process. Especially, the effect of different cooling rates during the depuration on the quality of oysters in anhydrous transportation is a gap. In this study, five cooling rates were applied to study their effects on the survival rates of the Pacific oyster, as well as its glycogen contents, pH values, adenosine 5-triphosphate (ATP)-related compounds, free amino acids (FAAs), and fatty acids, during depuration. Furthermore, the quality change of oyster during anhydrous preservation was also investigated. The results of the biochemical and nutritional compositions of oysters were essential for sustaining the supply chain value of the shellfish.

2. Materials and methods

2.1. Sample collection

Fresh and live one-year-old Pacific oysters were collected from Rushan (36° 49′38.66′' N, 121° 42′3.84′'E), Shandong Province, China. Afterward, they were packed in a container with ice at -°C4°C and transported immediately to the laboratory (2 h). In total, 700 animals were sampled (they were harvested in October 2020).

2.2. Sample preparation

Following their transportation to the laboratory, all of the oysters were washed under running water (20 °C) to remove impurities from their shells. Afterward, they were divided into five groups (140 samples per group) and placed in a recirculating aquaculture and depuration system (seawater exhibiting a temperature of 20 °C and without food) in our laboratory for 24 h. Notably, all of the experimental samples from each group exhibited uniform sizes (shell height, 35.0 ± 7.2 mm, shell length, 108.4 ± 11.0 mm, shell width, 59.8 ± 5.0 mm and weight, 128.8 ± 14.4 g). Thereafter, the water temperature of the recirculating aquaculture and depuration system reduced from 20 °C to °C4°C by cooling rates of 1, 3, 7, 11 and 16 °C/h before preservation (CR1, CR3, CR7, CR11 and CR16 groups). Afterward, anhydrous preservation was conducted in a Midea BCD-450WTPM(E) refrigerator (Hefei Midea refrigerator Co., Ltd., Hefei, Anhui, China), which was set to °C4°C. The anhydrous preservation process was sustained for three days. During the experiment, the oysters were examined for gaping and death (defined as the absence of adductor muscle contraction when tapped or broken shells due to physical trauma). Although the oysters with broken shells were alive, they were also discarded because they did not satisfy the quality criteria of the industry. The samples were collected at the following stages: the transportation to the laboratory stage (d0-T), the depuration for 24 h stage (d1-D), the temperature declining process to °C4°C stage (d2-D), and the anhydrous preservation stage which was further divided into the preservation for 24 (d3-P), 48 (d4-P) and 72 h (d5-P) stages. At each stage, 20 oysters were randomly selected for inspection to evaluate their overall survival rate, after which they were husked by hand, treated with liquid nitrogen, and stored at −80 °C for further analyses.

2.3. Survival rate

The survival rate of the oysters was determined, following a previously reported method (Goncalves, Pedro, Duarte, & Nunes, 2009). Briefly, 20 oysters were collected from each group and placed in seawater (20 °C) for 1 h. Their survival rate was determined by observing their valves. The oysters whose shells were opened were tapped with a glass rod, after which their responses were observed. An oyster was considered dead if its shell remained open for a long time. The survival rate was calculated, as follows:

Survivalrate(%)=(liveanimals/totalanimals)×100 (1)

2.4. Analysis of the glycogen contents

The glycogen contents of the oysters were measured by the anthrone–sulfuric acid method, as described by Bi et al. (2021a), following the protocol of the glycogen analysis kit (Beyotime; Nanjing Jiancheng Bioengineering Institute, Nanjing, China). Briefly, fresh soft tissue was rinsed with normal saline, drained with a filter paper, and weighed. Thereafter, the sample was dissolved in an alkaline solution (molar ratio, 1:3 (w/v)), homogenized, and placed in a boiling water bath for 20 min (before boiling the water bath, the end of the tube was tied with a preservative film to prevent water evaporation, and a small hole was drilled on the film with a needle to ensure the expansion and contraction of the gas under hot and cold conditions, respectively). Thereafter, they were cooled under running water and reheated in the boiling water bath for 5 min, following the addition of the chromogenic reagent of the kit. After cooling, the glycogen content was determined at a wavelength of 620 nm employing a WFJ-7200 spectrophotometer (Unico Ltd., Shanghai, China). The glycogen concentration was calculated from the absorbance of the samples at 620 nm employing an equivalent glucose standard. All the samples were analyzed in triplicates.

2.5. Analysis of pH

The pH value was determined according to the method described by Aru. (2016). An edible tissue (about 5 g) was homogenized in boiling water (50 mL), which was subsequently cooled to room temperature. The pH was measured on an ST3100 pH electrode (Ohau instrument co., LTD., Changzhou, China) after standing for 30 min.

2.6. Analysis of ATP-related compounds

The ATP-related compounds were identified via a method that was reported by Bi. (2021). An edible tissue (about 5 g) was homogenized in 15 mL of 5% cold perchloric acid for 30 s and placed in a refrigerator for 30 min at °C4°C. Thereafter, the homogenate was centrifuged for 10 min at °C4°C and 5000 rpm, and the supernatant was maintained at °C4°C. The precipitate was treated again via the aforementioned procedure to obtain another supernatant, and the two obtained supernatants were combined. The processed samples were neutralized to pH 6.70 with 10 and 1 M potassium hydroxide, diluted to a final volume, 50 mL, with Milli-Q purified water (Millipore Sigma, Burlington, MA, USA), filtered (pore size = 0.22 μm), and analyzed on a 1260 high-performance liquid chromatography (HPLC) system (Agilent Technologies Inc., Santa Clara, CA, USA). A 10-μL portion of the filtrate was injected into a Capcell Pak C18 SG120 S5 column (4.6 mm × 150 mm, Shiseido Co., Ltd., Tokyo, Japan). The temperature was 40 °C, and the eluents included 20, 20 and 40 mM acetic acid, citric acid, and triethylamine, respectively. The eluents were neutralized to pH 4.80 with 10 and 1 M potassium hydroxide. The flow rate was set at 0.8 mL/min, and the wavelength of the detector was set at 260 nm. The identities and quantities of the nucleotides were assessed by comparing them with the retention times and peak areas of their corresponding nucleotide standards. The nucleotide standards, ATP (99%), adenosine 5-diphosphate (ADP, 99%), adenosine 5′-monophosphate (AMP, 99%), inosine 5′-monophosphate (IMP, 99%), adenosine (AdR, 99%), adenine (Ad, 99%), xanthine (Xt, 99%), inosine (HxR, 99%), and hypoxanthine (Hx, 99%) were purchased from Sigma-Aldrich (St. Louis, MO, USA). All the samples were analyzed in triplicates.

The adenylate energy charge (A.E.C.) value, which corresponded to the index of freshness, was calculated according to the following equation:

A.E.C%=ATP+0.5ADP/ATP+ADP+AMP×100 (2)

2.7. Analysis of FAAs

The FAAs were extracted according to the method of Liu et al. (2021). Briefly, 5 g of an edible tissue was dissolved in 10 mL of 0.02 M dilute hydrochloric acid and homogenized for 30 s, afterward, the resulting solution was subjected to ultrasound for 5 min. Thereafter, the homogenate was centrifuged for 10 min at 5000 rpm and °C4°C, and the supernatant was maintained at °C4°C. The precipitate was treated again, following the aforementioned procedure, to obtain another supernatant, and the two obtained supernatants were combined. The processed samples were diluted to a final volume (25 mL) with Milli-Q purified water (Millipore Sigma). Subsequently, 2 mL of 5% sulfosalicylic acid was mixed with 2 mL of the diluent, and the mixed diluent was centrifuged again (1 × 104 rpm, °C4°C) for 10 min. Next, the supernatant was filtered through a 0.22-μm filter membrane-aquo system and analyzed with an L-8900 automatic amino acid analyzer (Hitachi High-Technologies Corporation, Tokyo, Japan). All the samples were analyzed in triplicates.

2.8. Analysis of fatty acid composition

The total lipids of oyster were extracted according to Ronquillo’s method (2012) Briefly, 0.3 g of freeze-dried oyster sample was mixed with 2 mL of methanol and 4 mL of chloroform, and the homogenate was centrifuged for 5 min at 8000 rpm. Afterward, a certain volume of lipid extract (chloroform layer) was added to the triglyceride C15:0 and dried with nitrogen. The hydrochloric acid: methanol (1:5 v/v) solution for deriving the fatty acid methyl ester reacted for 2 h at 90 °C after nitrogen filling and sealing. Afterward, n-hexane was added for the extraction process, the n-hexane layer (about 1 mL) was passed through a 0.22 μm organic filter membrane to analyze the fatty acids with GC detection.

This analysis was performed by 7820 gas chromatography (GC) system (Agilent Technologies Inc., Santa Clara, CA, USA). The capillary column SUPELCOWAXR 10 (30 m × 0.32 mm, 0.25 μm) and flame ionization detector were used to analyzed. The analysis of FAMEs was performed by injecting 2.0 μL no shunt ratio. The column oven conditions were as follows: injection temperature was 220, the oven origin temperature was held at 150℃ originally, then increased to 220 at 3℃ min−1 and maintained at this temperature for 20 min. The standard reference was used or qualitative analysis and the area normalization method was used for quantitative analysis.

2.9. Statistical analysis

The data of the nucleotides, FAAs, survival rates, and glycogen contents of the clams were processed via the one-way analysis of variance (ANOVA) and Duncan’s multiple range test. The statistical analysis was performed on SPSS 20.0 (SPSS Inc., Chicago, IL, USA), and the statistical significance was set at P < 0.05. Origin 2019b was used for drawing. All the experiments were performed in triplicates, and the experimental data were expressed as mean ± standard deviation.

3. Results and discussion

3.1. Survival rates

Fig. 1 showed the changes in the survival rates of oysters during the depuration, transported to laboratory and anhydrous preservation processes. At the depuration stage, no death was recorded, the survival rate of all groups was sustained (100%). This result indicated that the survival of oysters was not affected by the cooling rates during depuration. Previous study reported that the survival of clam was not negatively affected by depuration (Anacleto et al., 2013), several reports even indicated that the depuration process prolonged the half-lethal times of Paphia undulata and Chamelea gallina (El-Gamal, 2011), further confirming that the depuration process did not exert any bad effect on the survival rate of oysters.

Fig. 1.

Fig. 1

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The survival curve of Crassostrea gigas during depuration and anhydrous preservation at different cooling rates. Note: d0-T: the transportation to the laboratory stage. d1-D: the stage of depuration for 24 h at 20 °C. d2-D: the process of temperature declining to 4 °C. d3-P, d4-P and d5-P respectively represented the stage of preservation for 24 h, 48 h and 72 h at 4 °C. CR1, CR3, CR7, CR11 and CR16 respectively represented the cooling rates of 1, 3, 7, 11 and 16 °C/h during the depuration (d2-D). Mean values with different letters are significantly different.

At the anhydrous preservation stage, a clear contrast was observed in the survival rates under the different treatment conditions. First, there were no deaths during the CR1 and CR3 treatments. However, increased mortality was observed when the cooling rate was increased. The mortality for CR7 treatment was observed after 72 h of anhydrous preservation, and the survival rate was 96%. Regarding to the CR11 treatment, the mortality was observed from the second day of anhydrous preservation, and the survival rates were 93% and 85% after 48 and 72 h of anhydrous preservations, respectively. The highest mortality was observed in the CR16 treatment, mortality occurred initially with anhydrous preservation (24 h), and the survival rate was only 71% after 72 h of anhydrous preservation. These results indicated that the survival rates of the oysters during anhydrous preservation were affected by the cooling rates at the depuration stage. It is known that shellfish can survive for a long time when they are exposed to the air and maintained at low temperatures (Mi et al., 2012). Buen-Ursua and Ludevese (2011) evaluated the survival rate of abalone employing polyethylene containers with different ice contents, and the results indicated that both modeling groups that abalone were subjected to simulated transportations respectively for 8 and 10 h, exhibited 100% survival under low-temperature conditions for 48 h because shellfish assume a dormant or semi-dormant state with weak metabolic activities at low temperatures. Further, the growth of microorganisms was inhibited at low temperatures, and low temperature could maintain and prolong clam life vitality (Anacleto et al., 2013). Additionally, for surviving under dry conditions, bivalves tend to close their valves and retract their soft tissues into their shells for avoiding exposure to the air to minimize water loss (Collas, Koopman, Hendriks, van der Velde, Verbrugge, & Leuven, 2014), this behavior allows bivalve shellfish breathe effectively, thus reducing mortality caused by anoxia (Chen et al., 2021). Here, the cooling rate during depuration could be the factor that affected the survival rate of the oysters during anhydrous preservation. A lower cooling rate exerted less effects than a higher cooling rate on the survival of the oysters. Regarding to the group that was subjected to a rapid change in the cooling rate, the oysters might have suffered to temperature stresses, which caused their mortality. Therefore, the differences in the survival rates under the different treatment conditions of cooling rate could be attributed to the distinct depuration conditions that resulted in different adaptations during anhydrous preservation.

3.2. Glycogen content

The energy of shellfish is mainly stored as glycogen (Bi et al., 2021). When shellfish suffer from stress from the surrounding environment, the glycogen content could decrease for supporting energy (Anacleto et al., 2014, Patrick et al., 2006). Fig. 2A showed the glycogen content of Crassostrea gigas during depuration and anhydrous preservation. With time extension, the glycogen content exhibited a downward trend. This result could be explained as follows: at the early stage, the oysters consumed sufficient glycogens to adapt to the temperature-stressed environment (Ivanina et al., 2013). At the later stage, the decrease of glycogen content might be attributed to the consumption of blood glucose (Chen et al., 2021). Without external supply of nutrients, the shellfish would begin to decompose large amounts of the glycogen produced in their muscles and livers for sustenance. Regarding some bivalves, such as mussels, cockles, and clams, previous researches had reported that glycogen was the biochemical reserve to be primarily consumed within the first few days during starvation (Ivanina, Froelich, Williams, Sokolov, Oliver, & Sokolova, 2011).

Fig. 2.

Fig. 2

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The glycogen content and pH of Crassostrea gigas during depuration and anhydrous preservation at different cooling rate. Note: Mean values with different letters are significantly different. Take CR1 group as an example, mark the significant difference of glycogen change with time.

The consumption of glycogen by the shellfish decreased when the cooling rates increased under the different treatment conditions. Namely, the CR1 and CR16 groups exhibited the highest and lowest glycogen contents, respectively, and this result could be explained as follows: when compared with slow cooling, fast cooling would enhance stress to the oysters. Under stressful conditions, such as anhydrous preservation, the stored glycogens would be consumed to satisfy the maintenance needs of the oysters, thus reflecting the capacity of the bivalve to resistance further stress. glycogen is the preferred form of energy reserve in some benthic groups, such as the oysters (Chen et al., 2015). First, glycogen catabolism can rapidly supply energy. Second, glycogen catabolism can be performed under hypoxia or hypoxia conditions (Patrick et al., 2006), and it is particularly beneficial for oyster since the oyster shells might be closed for a long time. The oyster is a variable-temperature animal. Thus, the temperature exerts a significant influence on its physiological activities. When oysters are kept alive at high temperature, their metabolic activities are significantly strengthened, thus rapidly decreasing their glycogen contents (Berthelin, Kellner, & Mathieu, 2000). Large amounts of glycogen can be readily consumed within a short time and restored when it is not required (Berthelin, Kellner, & Mathieu, 2000). In this study, large temperature changes led to oyster stress. In order to alleviate this stress, oysters consumed glycogen to maintain body balance, so CR16 group consumed more glycogen. Therefore, the detected glycogen content of oysters could significantly reflect their energy storage. The storage of glycogen under stress reflects the ability of shellfish to tolerate environmental pressure. Based on current findings, glycogen could be a good indicator for the stress status of oysters.

3.3. pH

The pH changes in seafoods are generally a good index for evaluating their qualities (Khan, Parrish, & Shahidi, 2005). The pH changes therein are generally related to the accumulation of glycogen-produced lactic acid or the accumulation of alkaline substances, such as ammonia and trimethylamine, under anoxic conditions mainly because of the action of the alkalizing bacteria. As described in the literature (Khan, Parrish, & Shahidi, 2005), the pH values of fresh high-quality bivalves are between 6 and 7. In this study, the pH values of oysters under the different treatment conditions decreased significantly from 6.89 to 6.53 (Fig. 2B). During anhydrous preservation, the pH values decreased when the cooling rates increased under the different treatment conditions. The CR1 and CR16 groups respectively exhibited the highest and lowest pH values, which may be that glycogen was the main energy-consuming substance at the depuration and anhydrous preservation stage, which was degraded into lactic acid via glycolysis, thereby leading the decrease of the pH value (Chen et al., 2021, Chen et al., 2015). Similarly, Aru et al. (2016) reported that the pH values of mussels decreased significantly from 6.56 (fresh samples) to 6.17 and 5.9 after six and ten days of storage at 0 °C, respectively. Indeed, the pH values decreased with the increase of cooling rate. It was expected that glycogen degradation was more evident when the temperature fluctuated significantly. The results of the pH values were correlated with those of the glycogen contents. Thus, it could be assumed that the pH was a good indicator for reflecting the stress status of oysters.

3.4. ATP-related compounds

The contents of the ATP-related compounds in the oysters are closely related to their physiological states (Guevelou, Huvet, Galindo-Sanchez, et al., 2013). These compounds participate actively in muscle metabolism and supply energy for physiological processes, When shellfish are stressed or produce stress responses, the ATPs in their bodies will be degraded (Guevelou, Huvet, Sussarellu, et al., 2013). The ATP-related compounds contents in oysters are shown in Fig. 3. In this study, the ATP degradation pathway was proposed as follow: ATP → ADP → AMP → IMP → HxR → Hx, and the results were consistent with those of previous studies by Yang et al. (2016). IMP and AMP were the most prominent nucleotides, whereas ATP, HxR, and Hx exhibited very low concentrations under all the treatment conditions. Generally, the ATP-related compounds act as the coenzymes that participate in the metabolism (Anacleto et al., 2013). During depuration and anhydrous preservation, the IMP and AMP were observed with high concentrations, while ATP was detected with low concentration. ATP might have been degraded by endogenous enzymes to cause the temporary accumulation of IMP in the mollusks (Gao et al., 2021). The degradation of ATP into IMP is mainly attributed to endogenous autolytic enzyme activity (Dong et al., 2020). AMP has also been reported as a dominant nucleotide in shellfish, and its accumulation is the result of a highly reduced or nonexistent AMP deaminase activity (Quinta & Nunes, 2001).

Fig. 3.

Fig. 3

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The ATP-related compounds of Crassostrea gigas during depuration and anhydrous preservation at different cooling rate. Note: Mean values with different letters are significantly different. Take CR1 group as an example, mark the significant difference of glycogen change with time.

As shown in Fig. 3, The concentrations of ATP, ADP, AMP, and IMP increased during depuration, whereas those of HxR and Hx decreased. During anhydrous preservation, CR16 exhibited lower ATP, ADP, AMP, and IMP concentrations than that of CR1. But differently, the concentrations of ATP, ADP, AMP, and IMP decreased with the increased of cooling rate. Concurrently, CR16 exhibited higher concentrations of HxR and Hx than those in CR1. Further, the concentrations of HxR and Hx increased with the increased cooling rate. IMP could induce the accumulations of HxR and Hx via enzymatic activities and bacterial growth (Dong et al., 2020). It has been reported that HxR and Hx might be the stress indicators in the oysters (Anacleto et al., 2013), indicating that a high cooling rate could easily cause stress in the oysters in this study.

It is known that the A.E.C. values of invertebrates vary greatly depending on the influence of the natural or anthropogenic stressors (Bi et al., 2021b). The more stressed animals were, the more energy they consumed, which reduced their A.E.C. level (Marin et al., 2005). Fig. 4 showed the changes of the A.E.C. values in the oysters during depuration and anhydrous preservation. In this study, the A.E.C. values were all <50%, indicating that the oysters did not recover from the stress state of the initial harvesting during depuration. Furthermore, they maintained a stressful condition during anhydrous preservation.

Fig. 4.

Fig. 4

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The A.E.C value of Crassostrea gigas during depuration and anhydrous preservation at different cooling rate. Note: Mean values with different letters are significantly different. Take CR1 group as an example, mark the significant difference of glycogen change with time.

3.5. FAAs

Oysters are rich in proteins that could be hydrolyzed to produce large amounts of FAAs and peptides. Amino acids contribute significantly to the growth and development of organisms and endow the organisms with rich flavors (Sun et al., 2016). Their tastes are determined by the hydrophilic and hydrophobic groups in their molecular structures. Most hydrophilic groups taste pleasant, whereas hydrophobic groups generally taste unpleasant. In this study, 17 FAAs were estimated by an amino acid analyzer. The FAA contents obtained in this study were listed in Table 1. The FAA composition of the oysters was dominated by taurine, and other major FAAs in the oysters that were subjected to different treatments were Asp, Ala, Gly, Glu and Pro, which accounted for 85.63%–92.15% of the total FAA contents (they were the main FAAs in the Pacific oysters (Yuasa et al., 2018)). Liu et al. (2021) reported that Ala, Gly, Glu and His were the major FAAs in the oysters, accounting for 76.79%–80.24% of the total FAAs. Our previous study confirmed that the main FAAs that accounted for the umami flavor of oysters were Asp and Glu, whereas Ala, Gly, Thr, Ser, Lys and Pro accounted for the pleasant tastes of oysters (Bi et al., 2021). Fresh amino acids, such as glutamic and aspartic acids, produced fresh tastes during the presence of sodium salt. The amino acid analysis of fermented condiments/foods worldwide indicated that glutamate, which was the most abundant amino acid and the most valuable taste-active component, exhibited significant freshness (Kawai, Uneyama, & Miyano, 2009). In addition to the fragrance and sweetness produced by Gly, it could also reduce bitter tastes and remove unpleasant tastes from food (Yue, Zhang, Jin, Deng, & Zhao, 2016). In this study, the proportions of the umami amino acids and sweet amino acids in the total amino acids, were 31.37%–38.80%, and their proportions in CR1 were higher than that in CR16. It was evident that the proportions of the total umami amino acids and sweet amino acids decreased with the increased cooling rate. Regarding to the bitter amino acids (Ile, Leu, Tyr, His, Val, Lys, Met, and Sar), their proportions in the total amino acids were 6.50%–10.01%. No significant difference was observed among the different treatment groups. This study showed that the proportion of umami amino acids and sweet amino acids in oysters was relatively high when the purification and cooling rate was slow, while the proportion of bitter amino acids had no significant effect. Generally speaking, the slow cooling rate during depuration was beneficial to the maintenance of oyster quality. Additionally, during preservation, FAAs were produced after protein hydrolysis by protein hydrolase, and the amino acids would also produce putrefactive substances through desorption and ammonia removal. Therefore, the change in the FAA contents during preservation was closely related to the changes in the flavors and qualities of the fish and shellfish (Liu, Zhang, & Chen, 2013).

Table 1.

The free amino acid contents (mg/100g) of Crassostrea gigas during depuration and anhydrous preservation at different cooling rate.

FAA d0 d1-D d2-CR1 d2-CR3 d2-CR7 d2-CR11 d2-CR16 d3-CR1 d3-CR3 d3-CR7 d3-CR11 d3-CR16
Tau 143.02 ± 6.53 167.18 ± 25.53 174.18 ± 18.68 223.46 ± 25.95 242.96 ± 17.46 250.04 ± 0.97 223.24 ± 22.39 205.39 ± 37.58 188.29 ± 32.88 210.74 ± 14.88 204.50 ± 4.11 179.40 ± 18.34
Asp 19.10 ± 2.96 27.53 ± 4.75 30.89 ± 2.27 28.09 ± 2.60 30.84 ± 3.81 30.83 ± 0.17 28.13 ± 3.20 22.99 ± 4.98 21.30 ± 4.43 28.89 ± 1.91 26.75 ± 3.30 26.08 ± 3.77
Thr 2.22 ± 0.54 2.01 ± 0.72 1.95 ± 0.35 2.75 ± 1.02 6.61 ± 3.94 6.19 ± 0.09 2.58 ± 0.65 3.57 ± 1.96 3.75 ± 2.04 3.65 ± 3.07 2.57 ± 1.19 3.47 ± 2.95
Ser 2.46 ± 0.32 3.85 ± 1.16 2.84 ± 0.13 4.78 ± 1.20 10.67 ± 4.02 11.09 ± 0.20 5.56 ± 0.68 4.11 ± 2.15 3.95 ± 1.13 5.61 ± 3.51 3.99 ± 1.58 4.34 ± 1.92
Glu 21.07 ± 1.74 27.24 ± 3.53 28.13 ± 2.71 30.25 ± 3.21 30.58 ± 5.04 30.13 ± 0.75 29.90 ± 3.10 34.04 ± 8.01 33.82 ± 4.81 38.51 ± 6.87 34.13 ± 8.06 28.03 ± 4.61
Gly 23.53 ± 2.23 25.46 ± 8.37 27.33 ± 0.29 24.71 ± 4.73 30.22 ± 11.50 30.16 ± 1.15 27.20 ± 1.96 29.90 ± 11.34 29.52 ± 9.68 26.43 ± 7.32 28.43 ± 7.25 25.65 ± 6.66
Ala 16.76 ± 1.28 13.03 ± 0.83 18.63 ± 1.78 21.05 ± 3.01 20.58 ± 4.12 19.86 ± 0.37 16.11 ± 3.10 26.17 ± 11.28 24.49 ± 6.55 22.16 ± 6.73 18.94 ± 5.83 17.14 ± 7.58
Val 4.89 ± 0.42 3.20 ± 0.97 3.30 ± 0.84 3.49 ± 0.31 4.44 ± 0.82 4.81 ± 0.07 2.74 ± 1.55 1.62 ± 0.74 1.40 ± 0.38 0.78 ± 0.18 0.63 ± 0.30 1.03 ± 0.67
Met 3.41 ± 1.60 1.87 ± 1.03 1.77 ± 0.74 3.56 ± 0.28 5.50 ± 3.06 6.86 ± 0.13 3.58 ± 2.29 1.65 ± 0.87 2.32 ± 0.47 4.48 ± 2.64 2.18 ± 1.12 3.70 ± 1.31
Ile 0.91 ± 0.63 0.36 ± 0.07 0.45 ± 0.05 0.68 ± 0.18 1.29 ± 0.63 2.98 ± 0.32 1.60 ± 0.99 0.84 ± 0.45 0.85 ± 0.37 1.61 ± 1.03 0.92 ± 0.71 2.93 ± 0.27
Leu 1.69 ± 0.51 1.05 ± 0.22 1.05 ± 0.09 1.58 ± 0.30 2.90 ± 1.44 4.01 ± 0.12 2.39 ± 1.09 2.14 ± 0.91 2.03 ± 0.74 3.01 ± 1.48 2.09 ± 0.99 3.14 ± 1.03
Tyr 1.04 ± 0.19 1.16 ± 0.36 1.09 ± 0.24 1.84 ± 0.49 2.56 ± 1.10 5.34 ± 0.11 2.78 ± 1.35 2.53 ± 1.18 2.48 ± 0.80 3.22 ± 1.85 2.20 ± 1.06 4.03 ± 1.32
Phe 0.25 ± 0.15 0.84 ± 0.86 0.31 ± 0.18 0.54 ± 0.09 0.85 ± 0.39 2.56 ± 0.05 2.87 ± 0.41 2.51 ± 0.32 6.23 ± 6.05 3.25 ± 0.65 2.67 ± 0.65 3.31 ± 0.23
Lys 1.94 ± 0.13 1.34 ± 0.49 1.00 ± 0.36 1.88 ± 0.57 3.02 ± 1.30 2.82 ± 0.04 1.21 ± 0.33 1.56 ± 0.80 1.35 ± 0.53 1.79 ± 1.12 1.13 ± 0.35 3.21 ± 1.61
His 1.13 ± 0.24 1.10 ± 0.71 1.15 ± 0.14 1.62 ± 0.67 4.17 ± 2.49 4.08 ± 0.04 1.39 ± 0.60 2.76 ± 1.59 2.25 ± 1.09 2.43 ± 1.99 1.58 ± 0.86 2.28 ± 1.82
Arg 6.49 ± 0.51 10.10 ± 2.41 9.98 ± 1.14 13.04 ± 2.59 16.40 ± 3.62 15.57 ± 0.32 12.28 ± 1.71 13.02 ± 3.72 12.21 ± 3.19 13.05 ± 2.44 12.28 ± 1.70 10.97 ± 2.47
Pro 12.52 ± 3.15 15.45 ± 2.75 13.09 ± 2.39 19.09 ± 0.76 25.62 ± 13.38 34.23 ± 0.34 12.35 ± 4.73 16.63 ± 8.13 16.92 ± 7.73 26.75 ± 12.01 19.73 ± 10.51 20.13 ± 5.74
FAA d4-CR1 d4-CR3 d4-CR7 d4-CR11 d4-CR16 d5-CR1 d5-CR3 d5-CR7 d5-CR11 d5-CR16
Tau 195.04 ± 28.21 218.92 ± 37.76 209.39 ± 17.80 242.20 ± 54.56 190.19 ± 7.31 210.21 ± 31.31 195.00 ± 13.57 209.87 ± 13.72 195.21 ± 40.75 210.39 ± 4.37
Asp 20.39 ± 5.60 19.10 ± 1.61 24.76 ± 2.29 24.62 ± 5.58 21.18 ± 3.09 19.11 ± 3.82 17.01 ± 1.99 21.58 ± 0.77 19.50 ± 2.35 21.93 ± 1.27
Thr 2.10 ± 0.59 2.35 ± 1.31 3.01 ± 0.17 2.75 ± 1.14 2.80 ± 1.55 4.20 ± 3.34 1.45 ± 0.24 3.18 ± 1.42 1.90 ± 0.40 3.48 ± 1.15
Ser 3.06 ± 0.64 3.41 ± 2.30 4.67 ± 0.90 4.47 ± 1.10 4.58 ± 2.28 4.83 ± 3.62 2.04 ± 0.54 4.43 ± 2.06 3.17 ± 0.52 4.41 ± 0.55
Glu 41.97 ± 23.53 40.32 ± 4.64 39.99 ± 2.51 33.06 ± 11.70 31.40 ± 4.48 37.03 ± 6.98 30.13 ± 2.16 34.02 ± 4.63 35.64 ± 7.92 35.22 ± 3.93
Gly 26.80 ± 6.54 22.01 ± 9.62 24.53 ± 4.40 28.62 ± 6.44 26.45 ± 7.36 30.41 ± 5.65 21.74 ± 3.58 29.84 ± 10.68 26.82 ± 4.77 26.37 ± 18.91
Ala 22.10 ± 2.93 22.97 ± 10.11 22.30 ± 1.07 24.34 ± 8.14 19.39 ± 3.27 24.72 ± 5.80 19.04 ± 2.66 22.02 ± 4.88 18.75 ± 3.48 19.87 ± 6.69
Val 1.30 ± 0.70 2.25 ± 0.63 3.61 ± 0.27 3.17 ± 0.01 3.61 ± 0.83 4.07 ± 0.76 3.34 ± 0.15 3.42 ± 1.26 2.58 ± 0.64 3.73 ± 0.41
Met 3.09 ± 0.29 2.88 ± 0.13 3.57 ± 0.77 3.26 ± 0.91 3.68 ± 1.55 5.25 ± 2.51 4.32 ± 1.03 3.35 ± 1.45 1.25 ± 0.62 3.84 ± 0.89
Ile 3.31 ± 0.03 2.10 ± 1.09 1.52 ± 0.65 1.69 ± 0.68 2.02 ± 1.28 2.50 ± 0.77 2.14 ± 0.22 2.02 ± 1.32 0.63 ± 0.05 2.32 ± 0.56
Leu 3.02 ± 0.43 2.42 ± 0.36 2.45 ± 0.66 2.59 ± 0.59 3.34 ± 1.20 3.55 ± 1.35 2.49 ± 0.04 2.69 ± 1.26 1.37 ± 0.16 3.32 ± 0.73
Tyr 4.18 ± 0.74 3.41 ± 1.04 2.58 ± 0.79 3.01 ± 0.50 2.94 ± 1.02 3.92 ± 1.72 2.67 ± 0.29 2.85 ± 1.44 1.69 ± 0.08 3.39 ± 0.51
Phe 3.60 ± 0.27 1.72 ± 1.54 0.61 ± 0.04 1.05 ± 0.28 1.58 ± 0.34 0.98 ± 0.60 0.65 ± 0.08 0.89 ± 0.21 0.77 ± 0.11 1.41 ± 0.63
Lys 2.02 ± 1.07 2.03 ± 1.15 1.73 ± 0.29 1.00 ± 1.01 1.20 ± 0.38 1.85 ± 1.44 0.84 ± 0.09 1.78 ± 0.87 1.12 ± 0.08 1.37 ± 0.58
His 1.45 ± 0.25 1.79 ± 0.75 1.65 ± 0.05 2.13 ± 0.87 1.68 ± 0.77 3.17 ± 2.74 1.03 ± 0.40 2.11 ± 0.82 1.53 ± 0.19 2.63 ± 1.09
Arg 9.46 ± 1.56 11.60 ± 2.38 10.62 ± 2.35 13.72 ± 4.30 10.91 ± 2.24 12.19 ± 2.33 10.15 ± 0.93 13.03 ± 3.06 11.00 ± 2.75 11.65 ± 2.10
Pro 23.75 ± 7.08 12.86 ± 5.55 18.35 ± 1.78 19.39 ± 7.53 15.43 ± 5.91 19.10 ± 9.82 9.11 ± 2.78 20.29 ± 5.88 14.14 ± 3.39 16.65 ± 5.90
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3.6. Fatty acids

Although oysters are low-fat aquatic products, but proportion of fatty acids in their fat is relatively high, especially the proportions of polyunsaturated fatty acids, DHA and EPA (Fuhrmann et al., 2018). Table 2 revealed the fatty acid contents of oysters. A total of 18 fatty acids, including six saturated ones, four monounsaturated ones, and eight polyunsaturated ones, were detected. The saturated fatty acid contents of the oysters in all the treatment groups were the highest (up to 37.83%–54.07%) than the monounsaturated fatty acids and polyunsaturated fatty acids, the C15:0 and C16:0 contents accounted for 29.92%–52.68% and 27.65%–41.12%, respectively. The results were similar to those reported by Zhou et al. (2021), which indicated that the highest C16:0 content was observed in the oysters. Furthermore, the ∑MUFA and ∑PUFA contents were different between the various treatment conditions, while the scales ranged from 16.65% to 24.07% and 27.20% to 42.20%, respectively. The EPA and DHA contents among the polyunsaturated fatty acids were relatively high. Particularly, EPA accounted for about 40% of the polyunsaturated fatty acids. The World Health Organization and the Food and Agriculture Organization of the United Nations (FAO) recommended ΣPUFA/ΣSFA > 0.4 as the ideal fatty acid standard (FAO, 2020). The ΣPUFA/ΣSFA values of oysters were higher than 0.4 in this study. The fatty acid contents between each group were significantly different, it was irregular in this study. Thus, the fatty acid could not be employed as an indicator of the changes in the qualities of oysters during anhydrous preservation in this study.

Table 2.

The fatty acid content ((mg/g dw)) of Crassostrea gigas during depuration and anhydrous preservation at different cooling rate.

Fatty acid d0 d1-D d2-CR1 d2-CR3 d2-CR7 d2-CR11 d2-CR16 d3-CR1 d3-CR3 d3-CR7 d3-CR11 d3-CR16
C14:0 8.44 ± 5.06 3.07 ± 0.00 3.23 ± 0.06 2.31 ± 0.11 2.01 ± 1.03 2.35 ± 0.48 2.20 ± 1.14 3.29 ± 0.21 3.17 ± 0.05 3.18 ± 0.02 3.92 ± 0.30 3.12 ± 0.07
C15:0 14.79 ± 3.64 16.73 ± 0.53 19.16 ± 0.09 28.48 ± 1.17 19.67 ± 9.45 18.22 ± 2.09 22.86 ± 12.10 15.06 ± 0.79 17.59 ± 1.60 14.24 ± 0.53 15.64 ± 1.69 19.57 ± 0.47
C16:0 16.78 ± 0.78 15.98 ± 0.36 18.40 ± 0.07 14.95 ± 1.73 10.93 ± 3.47 15.61 ± 3.32 14.40 ± 6.98 15.78 ± 0.67 14.00 ± 0.00 14.42 ± 0.27 17.75 ± 1.36 15.52 ± 0.48
C17:0 1.72 ± 0.08 2.10 ± 0.37 2.89 ± 0.01 2.16 ± 0.64 2.01 ± 0.22 2.34 ± 0.71 2.28 ± 1.30 1.68 ± 0.12 1.99 ± 0.29 1.57 ± 0.11 1.60 ± 0.72 2.01 ± 0.28
C18:0 4.82 ± 0.72 3.60 ± 0.07 4.41 ± 0.01 3.84 ± 0.00 3.94 ± 0.42 4.18 ± 0.62 3.71 ± 1.90 3.72 ± 0.14 3.73 ± 0.04 3.38 ± 0.01 3.92 ± 0.12 3.62 ± 0.05
C20:0 2.51 ± 0.54 2.03 ± 0.03 2.12 ± 0.05 2.33 ± 0.02 2.19 ± 0.01 1.66 ± 0.12 2.75 ± 1.44 1.68 ± 0.35 2.19 ± 0.10 1.81 ± 0.24 1.58 ± 0.07 1.87 ± 0.17
∑SFA 49.05 ± 1.53 43.51 ± 2.14 50.21 ± 2.43 54.07 ± 4.32 40.74 ± 2.34 44.36 ± 3.56 48.19 ± 2.58 41.21 ± 2.15 42.66 ± 3.14 38.59 ± 1.95 44.41 ± 1.34 45.72 ± 2.75
C16:1 3.70 ± 1.74 4.66 ± 0.13 5.11 ± 0.15 2.15 ± 0.44 2.01 ± 0.22 2.15 ± 0.65 3.98 ± 1.96 4.74 ± 0.28 4.28 ± 0.26 4.70 ± 0.20 1.79 ± 0.01 4.76 ± 0.22
C17:1 2.17 ± 0.49 1.28 ± 0.21 1.54 ± 0.02 1.88 ± 0.39 1.70 ± 0.18 4.51 ± 4.45 2.19 ± 1.26 1.76 ± 0.14 2.08 ± 0.10 1.83 ± 0.12 10.14 ± 0.96 1.71 ± 0.08
C18:1 10.56 ± 0.49 9.71 ± 0.29 11.35 ± 0.21 8.14 ± 0.53 10.94 ± 1.17 9.12 ± 0.22 8.12 ± 4.18 9.65 ± 0.34 9.03 ± 0.40 10.08 ± 0.14 8.17 ± 0.19 9.48 ± 0.23
C20:1n-9 7.32 ± 0.34 7.04 ± 0.07 3.24 ± 0.01 6.91 ± 0.20 7.49 ± 1.37 6.93 ± 0.10 7.06 ± 3.66 6.35 ± 0.62 6.87 ± 0.30 7.45 ± 0.10 2.49 ± 0.02 6.99 ± 0.75
∑MUFA 23.75 ± 2.45 22.68 ± 3.56 21.23 ± 2.98 19.08 ± 1.69 22.14 ± 1.67 22.71 ± 1.88 21.35 ± 1.09 22.49 ± 3.10 22.26 ± 2.46 24.07 ± 2.43 22.60 ± 1.67 22.93 ± 1.90
C20:2 1.42 ± 0.07 0.80 ± 0.27 0.88 ± 0.27 1.24 ± 0.26 3.31 ± 2.03 1.47 ± 0.45 1.95 ± 1.07 0.83 ± 0.38 1.39 ± 0.22 2.36 ± 1.38 1.54 ± 0.22 1.35 ± 0.05
C20:3 1.06 ± 0.05 0.89 ± 0.06 0.93 ± 0.06 1.06 ± 0.12 1.33 ± 0.14 1.43 ± 0.43 1.46 ± 0.82 0.99 ± 0.04 0.99 ± 0.04 0.47 ± 0.01 1.03 ± 0.02 0.87 ± 0.14
C18:2n-6 1.30 ± 0.46 2.88 ± 0.05 3.30 ± 0.04 2.53 ± 0.66 2.69 ± 0.34 2.18 ± 0.40 2.66 ± 1.16 1.61 ± 0.07 1.60 ± 0.12 5.29 ± 3.43 0.94 ± 0.02 2.24 ± 0.57
C18:3n-6 1.18 ± 0.31 0.53 ± 0.02 0.37 ± 0.02 0.72 ± 0.15 2.36 ± 0.25 2.07 ± 0.67 1.29 ± 0.82 1.25 ± 0.15 1.50 ± 0.14 1.56 ± 0.10 2.36 ± 0.84 1.12 ± 0.12
C18:3n-3 1.61 ± 0.25 1.94 ± 0.06 3.25 ± 0.03 1.65 ± 0.12 3.32 ± 0.48 3.14 ± 0.10 2.58 ± 1.48 2.54 ± 0.35 2.58 ± 0.21 2.12 ± 0.89 1.22 ± 0.03 2.36 ± 0.15
C20:4n-6 3.51 ± 0.16 3.30 ± 0.03 8.13 ± 0.35 3.28 ± 0.30 3.90 ± 0.48 3.44 ± 0.48 3.82 ± 2.04 2.67 ± 0.68 3.42 ± 0.17 2.88 ± 0.77 2.90 ± 0.07 2.72 ± 0.30
EPA 10.93 ± 2.92 14.08 ± 0.19 15.16 ± 0.41 10.16 ± 0.32 11.95 ± 4.22 11.77 ± 2.01 10.20 ± 5.46 15.75 ± 0.06 14.15 ± 0.01 13.80 ± 0.56 14.62 ± 1.64 12.76 ± 0.24
DHA 6.19 ± 1.96 9.40 ± 0.32 10.18 ± 0.01 6.20 ± 0.58 8.27 ± 2.91 7.43 ± 0.82 6.50 ± 3.41 10.66 ± 0.30 9.46 ± 0.10 8.86 ± 0.10 8.37 ± 1.06 7.92 ± 0.09
∑PUFA 27.20 ± 1.64 33.81 ± 1.65 42.20 ± 2.57 26.85 ± 2.75 37.12 ± 2.05 32.93 ± 2.82 30.46 ± 1.95 36.30 ± 3.69 35.08 ± 3.01 37.33 ± 2.64 32.99 ± 3.67 31.35 ± 3.09
DHA+EPA 17.12 ± 3.53 23.47 ± 0.64 25.34 ± 0.67 16.36 ± 0.64 20.22 ± 3.67 19.20 ± 1.78 16.70 ± 4.64 26.40 ± 0.06 23.60 ± 0.10 22.65 ± 0.53 22.99 ± 1.05 20.68 ± 0.19
∑PUFA/∑SFA 0.55 ± 0.02 0.78 ± 0.04 0.84 ± 0.02 0.50 ± 0.04 0.91 ± 0.03 0.74 ± 0.01 0.63 ± 0.04 0.88 ± 0.03 0.82 ± 0.01 0.97 ± 0.04 0.74 ± 0.03 0.69 ± 0.03
Fatty acid d4-CR1 d4-CR3 d4-CR7 d4-CR11 d4-CR16 d5-CR1 d5-CR3 d5-CR7 d5-CR11 d5-CR16
C14:0 2.96 ± 0.07 2.66 ± 0.05 3.23 ± 0.09 2.79 ± 0.03 3.21 ± 0.00 3.66 ± 0.09 2.43 ± 0.03 3.18 ± 0.15 3.01 ± 0.05 2.82 ± 0.18
C15:0 23.98 ± 0.21 21.02 ± 1.46 15.86 ± 0.91 21.18 ± 1.09 15.53 ± 0.00 11.32 ± 0.74 20.55 ± 1.96 15.18 ± 0.12 18.43 ± 1.59 15.28 ± 0.25
C16:0 17.11 ± 2.11 13.58 ± 0.17 18.41 ± 1.88 13.11 ± 0.21 14.03 ± 0.00 15.55 ± 0.02 18.08 ± 0.09 18.86 ± 1.45 14.72 ± 0.18 16.79 ± 1.38
C17:0 2.67 ± 0.09 2.50 ± 0.06 2.50 ± 0.05 1.76 ± 0.36 3.48 ± 0.00 1.85 ± 0.41 2.57 ± 0.10 2.09 ± 0.43 2.01 ± 0.31 1.92 ± 0.47
C18:0 3.72 ± 0.07 3.70 ± 0.20 3.81 ± 0.22 3.49 ± 0.03 5.24 ± 0.00 3.51 ± 0.21 3.75 ± 0.12 3.91 ± 0.29 3.88 ± 0.09 3.62 ± 0.30
C20:0 2.35 ± 0.25 2.32 ± 0.24 2.00 ± 0.23 1.84 ± 0.24 2.03 ± 0.00 1.93 ± 0.16 2.70 ± 0.20 2.32 ± 0.07 2.04 ± 0.31 2.12 ± 0.26
∑SFA 52.79 ± 1.45 45.77 ± 1.54 45.80 ± 1.89 44.17 ± 2.05 43.51 ± 2.90 37.83 ± 2.05 50.08 ± 1.85 45.54 ± 3.01 44.10 ± 3.58 42.55 ± 2.01
C16:1 3.99 ± 0.24 4.09 ± 0.20 4.06 ± 0.45 4.46 ± 0.16 5.20 ± 0.00 5.17 ± 0.19 4.14 ± 0.31 3.60 ± 1.45 4.65 ± 0.18 3.89 ± 0.47
C17:1 1.81 ± 0.13 1.75 ± 0.15 1.61 ± 0.21 1.34 ± 0.40 1.56 ± 0.00 1.81 ± 0.01 1.99 ± 0.04 10.08 ± 0.16 1.77 ± 0.01 1.88 ± 0.11
C18:1 8.77 ± 0.19 8.82 ± 0.34 9.57 ± 0.04 9.06 ± 0.25 10.58 ± 0.00 9.94 ± 0.21 8.64 ± 0.00 9.01 ± 0.52 9.39 ± 0.12 8.95 ± 0.13
C20:1n-9 2.08 ± 0.16 7.79 ± 1.35 6.96 ± 0.31 6.61 ± 0.08 1.88 ± 0.00 5.00 ± 0.42 6.89 ± 0.52 3.80 ± 0.22 6.02 ± 0.90 6.87 ± 0.29
∑MUFA 16.65 ± 1.94 22.45 ± 3.10 22.20 ± 2.11 21.47 ± 1.53 19.22 ± 1.91 21.93 ± 3.01 21.66 ± 3.04 26.49 ± 1.59 21.83 ± 2.02 21.59 ± 1.92
C20:2 1.25 ± 0.32 1.21 ± 0.22 1.17 ± 0.23 1.17 ± 0.30 1.36 ± 0.00 0.96 ± 0.06 1.39 ± 0.14 1.43 ± 0.05 1.25 ± 0.01 1.14 ± 0.02
C20:3 0.94 ± 0.26 1.08 ± 0.22 0.99 ± 0.14 1.04 ± 0.21 1.22 ± 0.00 0.84 ± 0.00 1.06 ± 0.03 1.21 ± 0.01 1.00 ± 0.04 0.92 ± 0.11
C18:2n-6 2.95 ± 0.18 2.22 ± 0.58 1.61 ± 0.02 1.60 ± 0.04 1.86 ± 0.00 1.63 ± 0.05 2.94 ± 0.09 3.34 ± 0.01 2.95 ± 0.03 1.04 ± 0.00
C18:3n-6 1.60 ± 0.02 0.92 ± 0.42 1.32 ± 0.04 1.38 ± 0.13 1.61 ± 0.00 1.44 ± 0.04 0.64 ± 0.02 0.54 ± 0.03 0.50 ± 0.07 2.43 ± 0.66
C18:3n-3 1.36 ± 0.09 1.67 ± 0.08 2.58 ± 0.11 2.38 ± 0.21 1.84 ± 0.00 2.68 ± 0.03 1.74 ± 0.03 3.10 ± 0.18 1.50 ± 0.22 2.05 ± 0.62
C20:4n-6 2.99 ± 0.44 3.61 ± 0.21 3.06 ± 0.21 3.53 ± 0.25 3.17 ± 0.00 3.41 ± 0.06 3.79 ± 0.05 3.68 ± 0.10 3.54 ± 0.02 3.43 ± 0.10
EPA 11.44 ± 0.56 12.54 ± 0.04 13.00 ± 0.28 14.29 ± 0.44 11.35 ± 0.00 17.92 ± 0.33 11.83 ± 0.39 15.59 ± 0.22 13.97 ± 0.46 14.27 ± 0.05
DHA 8.02 ± 0.19 8.52 ± 0.19 8.25 ± 0.28 8.97 ± 0.14 8.26 ± 0.00 11.36 ± 0.40 9.02 ± 0.61 10.96 ± 0.73 9.37 ± 0.18 10.58 ± 0.49
∑PUFA 30.56 ± 1.34 31.78 ± 1.54 32.00 ± 1.03 34.36 ± 1.54 30.67 ± 3.51 40.25 ± 1.02 32.41 ± 2.05 39.84 ± 1.45 34.07 ± 1.25 35.86 ± 1.51
DHA+EPA 19.46 ± 0.34 21.07 ± 0.51 21.25 ± 0.25 23.26 ± 0.13 19.60 ± 0.13 29.29 ± 0.34 20.85 ± 0.41 26.54 ± 0.33 23.34 ± 0.13 24.85 ± 0.13
∑PUFA/∑SFA 0.58 ± 0.01 0.69 ± 0.03 0.70 ± 0.03 0.78 ± 0.01 0.42 ± 0.03 1.06 ± 0.09 0.65 ± 0.03 0.87 ± 0.06 0.77 ± 0.04 0.84 ± 0.03
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The content of fatty acids has a great relationship with temperature. In order to adapt to temperature changes, some fatty acids (such as polyunsaturated fatty acids) can maintain the fluidity and permeability of the cell membrane of animals at variable temperatures. The saturation of membrane fatty acids increases during the thermal reaction to compensate for the negative effect of membrane fluidity. With the rapid rise of temperature, the increase of fluidity exceeds the optimal range, and the membrane becomes “superfluid”. These changes are usually caused by the activation of acyltransferase, phosphoglycerate transferase and fatty acid desaturase. Van Doormalen observed that with the increase of temperature, the main SFA (PA and SA) in insects decreased, which is contrary to the expected reaction, because it has a solidification effect on membrane fluidity. This reduction of SFA may be related to the metabolic demand of bivalves under extreme warming conditions (such as a source of energy). The trend above 20℃ is unknown, but it seems to behave in a similar way. Surface water temperature can be used as a reference index to measure the growth environment of oysters in the four seasons, and is an important environmental factor that affects the physiology and enzyme activity of oysters (Nøstbakken et al., 2012). Oysters may live in the deep sea or shallow sea, or even in the salt water of estuarine habitat. Individual differences caused by vertical distribution also have a significant impact on these results (Nøstbakken et al., 2012). In this study, there were significant differences in the content of fatty acids in each group, but there were no regular changes, which might be closely related to the individual differences of oysters.

4. Conclusion

In this study, the effects of different cooling rates on the qualities of oysters during depuration and anhydrous preservation were reported. The indices, including the survival rates, glycogen contents, pH values, ATP-related compounds, FAAs, and fatty acids, were investigated. The results indicated that the different cooling rates during depuration affected the survival rates of the oysters during anhydrous preservation. Thus, the greater the temperature difference, the greater the mortality of the oysters. Furthermore, the different cooling rates in the depuration process also affected the quality of the oysters during anhydrous preservation: the higher the cooling rate, the greater the temperature stress on the oysters, causing a decline in their qualities. Thus, the determined optimum cooling rate for the depuration process was 1 °C/h in this study. These results could provide a theoretical basis for regulating the water environment during the depuration of oysters.

CRediT authorship contribution statement

Shijie Bi: Methodology, Data curation, Writing – original draft. Changhu Xue: Funding acquisition, Resources. Yunqi Wen: Conceptualization. Xin Du: Conceptualization. Qianqian Xue: Methodology. Zhaojie Li: Supervision. Hongying Liu: Writing – review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study is supported by the National Key R&D Program of China (2018YFD0901004), Innovation Team Project of Hebei (Province) Modern Agricultural Industry Technology System (HBCT2018170207), Innovation Center of Hebei Agricultural Products Processing Technology (199676183H) and the modern agricultural industry technology system (CARS-49).

Data availability

The authors do not have permission to share data.

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