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. 2025 Aug 25;30:102952. doi: 10.1016/j.fochx.2025.102952

Evaluation of aroma characteristics of Eriocheir sinensis meat as affected by environmental ammonia

Tianyu Wang a, Hang Lu a, Yuanyong Tian a, Hui Zhao a, Xuefeng Lu a, Zhaoxia Wu b,⁎, Shiwei Niu c,⁎
PMCID: PMC12409456  PMID: 40917115

Abstract

Ammonia accumulation in aquaculture systems affects the sensory quality of Eriocheir sinensis, and mechanisms linking ammonia to aroma changes remain unclear. This study investigated how ammonia exposure in aquatic environments (0, 10.47, and 41.87 mg/L total ammonia-N, 48 h) alters aroma profiles of E. sinensis meat. Using HS-SPME-GC–MS and HS-GC-IMS, we identified 26 key volatile organic compounds (VOCs) defining aroma differences. Concurrently, fatty acid profiles were analyzed through GC–MS. Ammonia exposure reduced fishy (trimethylamine, 1-octen-3-ol) and meaty (methional) aromas while enhancing plant-like (phenylethyl alcohol) and nutty (2-methylbutanal) aromas in the low-concentration group; high-concentration ammonia diminished hexanal and sulfur-containing compounds, aligning with aroma evaluation trends. Further, n-3 polyunsaturated fatty acids increased after ammonia exposure, correlating with VOCs derived from lipid metabolism. These findings reveal ammonia-induced metabolic changes in flavor precursors (e.g., fatty acids) and flavor compounds (e.g., VOCs) and provide feasible insights for optimizing aquaculture practices to improve crab quality.

Keywords: Eriocheir sinensis, Ammonia exposure, Volatile organic compounds, N-3 polyunsaturated fatty acids, HS-SPME-GC-MS, HS-GC-IMS, Aroma evaluation

Graphical abstract

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Highlights

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    Low-level ammonia raised pentanal and 2-methylbutanal contents in crab meat.

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    High/low ammonia levels reduced the trimethylamine and methional contents.

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    High/low ammonia levels raised the n-3 polyunsaturated fatty acids (PUFAs) content.

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    PUFAs-derived volatile organic compounds correlated with PUFAs, such as C18:2 n6.

1. Introduction

The Chinese mitten crab (Eriocheir sinensis), a delicacy in Asian markets, derives its commercial value from unique aroma profiles. In 2023, the E. sinensis breeding output reached 888,629 tons in China, with an output value exceeding 50 billion Chinese yuan (CNY) (Ministry of Agriculture and Rural Affairs et al., 2024). However, intensive aquaculture practices often expose E. sinensis to elevated ammonia levels from metabolic waste and feed residues, which may affect its flavor development. High-level ammonia is known to disrupt physiological processes in E. sinensis, potentially altering flavor-related metabolites, including free amino acids and nucleotides, and polyunsaturated fatty acids (PUFAs) (Wang et al., 2023). PUFAs serve not only as critical components of biological membranes but also as precursors for volatile organic compounds (VOCs) via oxidative degradation pathways (Liu et al., 2020). E. sinensis is rich in PUFAs, such as C20:5 n3 (eicosapentaenoic acid, EPA) and C22:6 n3 (docosahexaenoic acid, DHA) (Wang et al., 2022). Previous studies focused on the correlation between oxidative degradation of PUFAs and aroma quality in processed crab meat (Sun et al., 2022; Zhao, Zhang, & Wang, 2022), but neglected the effect of environmental factors in crab aquaculture on its fatty acid metabolism and aroma quality. While our previous studies have linked ammonia exposure to metabolic changes in E. sinensis, the specific mechanisms underlying ammonia-induced VOCs alterations—particularly the interplay between ammonia, oxidative degradation of PUFAs, and VOCs—remain unclear. This gap limits our understanding of how environmental ammonia reshapes aroma profiles of E. sinensis meat through fatty acid-mediated pathways.

Aroma plays a vital role in determining the overall sensory characteristics of aquatic products and greatly affects consumer preference. The VOCs detection is the main indicator used to evaluate the aroma profiles of aquatic products, and the accuracy and precision of their detection methods are crucial. Headspace solid-phase microextraction gas chromatography–mass spectrometry (HS-SPME-GC–MS) is a well-established method for studying VOCs in E. sinensis. A previous HS-SPME-GC–MS study has identified 67 VOCs in E. sinensis, such as aldehydes, alcohols, and aromatic compounds (Gu, Wang, Tao, & Wu, 2013). Headspace gas chromatography-ion mobility spectrometry (HS-GC-IMS) is a rising and convenient analytical method for VOCs detection because of its simple sample pretreatment, intuitive visualization of the results, and rapid detection speed (Fan et al., 2021). HS-GC-IMS has been applied to monitor the responses of the VOCs in aquatic products to changes in culture environments, such as salinity (Chen et al., 2022). Electronic nose (E-nose) analysis is also a non-subjective and sensitive detection method that distinguishes samples and provides their overall aroma information using specific sensors and pattern recognition systems (Chen et al., 2021). Integrated the use of these methods has recently proven effective in tracking flavor changes in aquatic products, such as fermented shrimp paste (Li et al., 2023) and grass carp mince (Xiao et al., 2022), yet their application to E. sinensis exposed to ammonia remains unexplored.

Thus, this study combined the above techniques to comprehensively evaluate the changes in the VOCs in E. sinensis meat when exposed to different concentrations of ammonia and pinpoint specific ammonia-sensitive aroma markers. Further, we performed a fatty acid analysis to analyze the mechanisms underlying the changes in the PUFAs-derived VOCs. This mechanistic understanding will inform practical strategies for farmers and technicians, such as optimizing ammonia management in aquaculture systems and developing functional feeds to regulate PUFAs content or fatty acid oxidation pathways, ultimately enhancing the desirable aroma profiles and market value of E. sinensis.

2. Materials and methods

2.1. Materials and chemicals

Adult male E. sinensis individuals (82.62 ± 3.55 g) were obtained from a commercial crab farm (Panjin, China) and acclimated in tanks (65 × 42.5 × 35 cm) for one week. During the acclimation period, the E. sinensis were reared in aerated municipal water and fed a commercial feed at their 2 % body weight twice daily. Fecal matter was cleaned, and half of the tank water was replaced daily.

All reference standards for the aroma attributes, including 4-heptenal, hexenal, maltol, 3-heptanone, and methional, were purchased from Sigma-Aldrich Co., Ltd. (Shanghai, China). The internal standard substance, 2-octanol, was purchased from TCI Shanghai Co., Ltd. (Shanghai, China). A C4-C9 n-alkanes standard for the GC-IMS was purchased from Aladdin Biochemical Technology Co., Ltd. (Shanghai, China).

2.2. Ammonia exposure and sample preparation

After acclimatization, 72 healthy crabs with intact appendages and uniform size were randomly selected for ammonia exposure testing. Based on the maximum ionic ammonia concentration (7.6 mg/L) in the aquaculture water of the E. sinensis in Panjin and the sub-lethal concentration of ammonia on E. sinensis (90.92 mg/L) measured by our previous research (Wang et al., 2021), low-concentration ammonia treatment (LT) and high-concentration ammonia treatment (HT) groups were set, with ammonia concentrations of 10.47 and 41.87 mg/L total ammonia-N (or 0.20 and 0.80 mg/L NH3), respectively. Different concentrations of ammonia were obtained by adding NH4Cl to the culture water. The control group (CK) was exposed to aerated municipal water, without additional nitrogen sources. Each group was equipped with three replicate tanks containing eight crabs. The culture water was replaced with fresh water including the corresponding concentrations of ammonia every 12 h to ensure the stability of the ammonia concentrations. The water temperature and pH were controlled at 17.8 ± 0.7 °C and 7.77 ± 0.11, respectively. After 48 h, three live crabs in each group were steamed at 100 °C for 20 min in a steamer. The remaining crabs were anesthetized using ice. The raw and cooked crabs were then dissected and their abdomen meat was collected using high-temperature sterilized scissors and tweezers, respectively, frozen in liquid nitrogen, and stored at −80 °C prior to further analysis. The cooked sample was used for the fatty acid analysis. The raw sample was subjected to E-nose, GC–MS, GC-IMS, and sensory analyses. In addition, the raw sample was put into a 20 mL headspace bottle, steamed in a 90 °C water bath for 40 min, and cooled to 25 °C before the aroma-related indicators determination.

2.3. Fatty acid analysis

The fatty acid analysis was conducted as previously described (Yang, Han, Xia, Xu, & Wu, 2021), with some modifications. Briefly, total lipid was extracted from 5.00 g of crab meat using a chloroform-methanol solution (2:1, v/v) and converted into fatty acid methyl esters. For derivatization, 50 mg of the extracted lipid was dissolved in a petroleum ether-benzene solution (1:1, v/v), mixed with 0.4 mol/L potassium hydroxide-methanol solution, and vortexed for 3 min. After standing for 1 h, the supernatant was filtered and analyzed.

A GC–MS system (6890-5973 N, Agilent lnc., Santa Clara, CA, USA) equipped with a TR-FAME capillary column (30 m × 250 μm × 0.25 μm; Thermo Scientific lnc., Waltham, MA, USA) was used for separation. The initial column temperature was 80 °C, then raised to 220 °C at a rate of 4 °C/min and maintained for 4 min. The detector and injector temperatures were both kept at 230 °C, with nitrogen carrier gas flowing at 0.9 mL/min. The mass spectrometer operated in electron impact (EI) ionization mode with a scan range of 41–520 m/z. The detector interface, quadrupole, and ion source temperature were maintained at 285, 150, and 230 °C, respectively. Fatty acid identification was conducted by matching mass spectrometry with NIST 98 library, and the relative fatty acid content was calculated based on the relative peak area percentage.

2.4. Aroma evaluation

The aroma profiles of the E. sinensis meat were evaluated using the quantitative descriptive sensory analysis (QDA) method based on Zhang, Ji, Liu, and Gao (2020), with minor modifications. Ten sensory panelists (five males and five females, aged 24–28 years) with professional training and previous olfactory testing experience were invited from the College of Food Science, Shenyang Agricultural University. Before the aroma evaluation, the written informed consent was obtained from all panelists and they participated in three training sessions, each lasting 4 h. First, the panelists were required to familiarize themselves with the aroma descriptors of E. sinensis meat. They then discussed the aroma characteristics of E. sinensis meat regarding the aroma attributes and proposed as many aroma attribute descriptors as possible. Five attributes—fishy, grassy, sweet, earthy, and meaty—were determined after intensive discussion. To evaluate the intensities of the five selected attributes, these attributes of samples were compared with aqueous solutions of the following reference odorants: 4-heptenal for “fishy,” hexenal for “grassy,” maltol for “sweet,” 3-heptanone for “earthy,” and methional for “meaty.” All reference odorants were selected based on the literature (Jiang, Zhang, Liu, Bhandari, & Yang, 2020; Zhang et al., 2020). Finally, the panelists were trained to smell the references for each attribute to ensure that they could all correctly recognize 100 % of the references. A 20 mL sealed bottle containing a 2 g sample was labeled with a randomly assigned 3-digit code and incubated at 60 °C for 15 min. The panelists then evaluated and recorded aroma attribute intensities of the sample in an aroma-free room at 20 °C. The aroma attribute intensities were quantitatively evaluated on a scale of 0–5 (0 = no aroma, 5 = extremely strong aroma).

2.5. E-nose analysis

The aroma profiles of the E. sinensis meat were evaluated using the PEN3 E-nose system (Airsense Analytics Inc., Schwerin, Germany). The PEN3 system has 10 metal oxide semiconductor (MOS) sensors that provide selectivity toward VOC categories. Table S1 presents the performance characteristics of the MOS sensors. A sealed headspace bottle containing a 5.00 g sample was left at 25 °C for 30 min before analysis. The detection parameters were as follows: sampling time, 1 s/group; sensor automatic cleaning time, 80 s; sensor return to zero time, 5 s; pre-injection time, 5 s; and sample measurement time, 80 s. The experiments for all samples were conducted at 25 °C, with an injection flow rate of 400 mL/min.

2.6. HS-SPME-GC–MS analysis

The VOCs in the E. sinensis meat were extracted using the HS-SPME system equipped with a 50/30 μm DVB/CAR/PDMS needle (Supelco, Bellefonte, PA, USA). Prior to extraction, 10 μL of 1 mg/L 2-octanol (internal standard) was quickly added to 5.00 g of crab meat sample in a headspace bottle. The sample was equilibrated at 60 °C for 15 min, followed by VOCs adsorption onto the SPME fiber exposed to the headspace for 30 min at the same temperature. After extraction, the fiber was thermally desorbed in the GC injector at 250 °C for 4 min.

GC–MS analysis was performed using an Agilent 7890-5977B system equipped with an Agilent DB-Wax capillary column (30 m × 250 μm × 0.25 μm). Helium (He: ≥ 99.999 % purity) was used as the carrier gas, with a flow rate of 1 mL/min. The initial temperature was maintained at 40 °C for 4 min and then increased to 245 °C at a rate of 5 °C/min and kept for 5 min. Mass spectra were obtained in the electron impact (EI) mode at 70 eV, with quadrupole and ion source temperatures set to 150 and 230 °C, respectively. Data were acquired in full-scan mode (20–400 m/z). VOCs were identified by spectrum matching with the NIST 17 library. The relative VOC content in the crab meat samples was calculated by comparing the peak area of each VOC with that of 2-octanol. Aroma-active compounds were determined using the relative odor activity value (rOAV), where rOAV >1 indicates a significant contribution to odor. The VOCs odor thresholds were obtained from the previous studies (Guo, Schwab, Ho, Song, & Wan, 2022; Olivares, Navarro, & Flores, 2011).

2.7. HS-GC-IMS analysis

The VOCs in the E. sinensis meat were further detected using the HS-GC-IMS. Briefly, 2.00 g of crab meat sample was sealed in a headspace bottle and equilibrated at 65 °C for 10 min. A 200 μL aliquot of the headspace gas was automatically injected into an MXT-5 capillary column (30 m × 0.53 mm × 1.0 μm; Restek lnc., PA, USA) operated in splitless mode. Chromatographic separation was performed on an Agilent 490 GC system coupled to a FlavourSpec IMS detector (G.A.S., Dortmund, Germany) under the following conditions: injector temperature 70 °C, column temperature 45 °C, and nitrogen carrier gas with a programmed flow rate (2 mL/min for 5 min, ramped to 100 mL/min over 20 min, then held for 5 min). The retention indices (RI) of the detected VOCs were calculated with n-alkanes C4-C9 as the external references. The VOCs were qualitatively analyzed by comparing the RI and drift times of the standards in the GC-IMS library. The relative abundances of the detected VOCs were represented by the averages of the peak areas.

2.8. Statistical analysis

All analyses were replicated three times, and the results were expressed as the mean ± standard deviation. Data were analyzed using one-way analysis of variance (ANOVA) with multiple comparison (Duncan) tests using SPSS 22.0 software (SPSS Inc., Chicago, IL, USA). Statistical significance was set at p < 0.05. Heat maps were generated using R 4.2.1. The GC-IMS data were analyzed using instrumental analysis software, including the Reporter and Gallery Plot plug-ins. These plug-ins were used to compare the differences in the crab meat samples from different angles by constructing topographic maps and fingerprints, respectively. The multivariate statistical analyses, including principal component analysis (PCA), partial least squares discriminant analysis (PLS-DA), and variable importance in projection (VIP), were conducted using SIMCA 14.1 (Umetrics, Umea, Sweden). The radar graphs and other figures were constructed using Origin 2018 (Origin Lab Inc., USA).

3. Results and discussion

3.1. Fatty acid composition

Table 1 presents the fatty acid composition of the E. sinensis meat after ammonia exposure. A total of 24 fatty acids were identified in each group. The proportion of C16:0 was the largest among saturated fatty acids (SFAs), the proportion of C18:1 n9 was the largest among monounsaturated fatty acids (MUFAs) and the proportions of EPA and DHA were the largest among PUFAs. These results were in agreement with those of a previous fatty acid analysis of E. sinensis meat (Wang et al., 2022).

Table 1.

Fatty acid composition (% of total fatty acids) of the E. sinensis meat after ammonia exposure.

Fatty acids CK LT HT
C12:0 0.06 ± 0.01b 0.03 ± 0.01c 0.31 ± 0.02a
C14:0 0.46 ± 0.01a 0.22 ± 0.02c 0.30 ± 0.02b
C15:0 0.43 ± 0.01a 0.29 ± 0.02c 0.38 ± 0.02b
C16:0 15.77 ± 0.27a 12.30 ± 0.79c 14.25 ± 0.52b
C17:0 1.11 ± 0.09b 1.28 ± 0.05a 1.23 ± 0.05ab
C18:0 6.06 ± 0.04c 7.15 ± 0.12a 6.83 ± 0.08b
C19:0 0.21 ± 0.01a 0.18 ± 0.01b 0.17 ± 0.00b
C20:0 0.10 ± 0.01a 0.08 ± 0.01b 0.07 ± 0.01c
∑SFA 24.20 ± 0.33a 21.54 ± 1.00b 23.55 ± 0.70a
C16:1 n9 0.12 ± 0.00a 0.11 ± 0.01ab 0.10 ± 0.01b
C16:1 n7 4.48 ± 0.08a 2.04 ± 0.14c 3.06 ± 0.15b
C18:1 n9 18.67 ± 0.12a 16.42 ± 0.45b 16.26 ± 0.30b
C18:1 n7 1.88 ± 0.04a 1.57 ± 0.07b 1.70 ± 0.14ab
C18:1 n5 0.05 ± 0.01b 0.08 ± 0.01a 0.06 ± 0.01ab
C19:1 n9 0.13 ± 0.01a 0.08 ± 0.01b 0.09 ± 0.00b
C20:1 n9 0.86 ± 0.02a 0.74 ± 0.01b 0.74 ± 0.03b
∑MUFA 26.18 ± 0.21a 21.03 ± 0.65c 22.01 ± 0.37b
C18:2 n6 12.86 ± 0.11a 11.75 ± 0.27b 10.44 ± 0.37c
C18:3 n3 2.17 ± 0.03b 1.81 ± 0.03c 3.01 ± 0.16a
C18:2 n8 0.21 ± 0.00a 0.10 ± 0.01b 0.11 ± 0.01b
C20:2 n7 1.28 ± 0.02b 2.04 ± 0.08a 1.97 ± 0.12a
C20:4 n6 4.84 ± 0.04c 8.34 ± 0.24a 6.62 ± 0.05b
C16:3 n3 0.39 ± 0.00b 0.42 ± 0.02b 0.70 ± 0.02a
C20:4 n3 0.25 ± 0.02b 0.16 ± 0.01c 0.34 ± 0.00a
C20:5 n3 14.04 ± 0.16c 19.24 ± 0.39a 15.92 ± 0.27b
C22:6 n3 13.58 ± 0.40a 13.57 ± 1.23a 15.32 ± 0.82a
∑PUFA 49.62 ± 0.54c 57.43 ± 1.63a 54.44 ± 0.51b
∑n-3PUFA 30.43 ± 0.59b 35.19 ± 1.60a 35.29 ± 0.93a
∑n-6PUFA 17.70 ± 0.07b 20.09 ± 0.07a 17.07 ± 0.42c
n3/n6 1.72 ± 0.04b 1.75 ± 0.08b 2.07 ± 0.10a
PUFAs/SFAs 2.05 ± 0.05c 2.67 ± 0.20a 2.31 ± 0.09b
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Note: CK, control group; LT, low-concentration ammonia treatment group; HT, high-concentration ammonia treatment group. Values are shown as the mean ± standard deviation (n = 3). Different lowercase letters within a row indicate significant differences (p < 0.05).

In the E. sinensis meat, SFAs and MUFAs were consumed after ammonia exposure. Compared with the CK group, the MUFAs content in LT and HT groups significantly decreased, while the SFAs content in the LT group also significantly decreased. SFAs, characterized by their straight-chain structure, tend to rigidify cell membranes (Xiang et al., 2019). The reduction of SFAs in the LT group could enhance membrane fluidity, which is crucial for maintaining cellular function and permeability under suboptimal environmental conditions. This adjustment may help E. sinensis in the LT group maintain membrane integrity and physiological processes without excessive energy expenditure, as SFAs are also important energy storage molecules (Karageorgou et al., 2023). Shan, Geng, Ma, and Wang (2019) found that the demand for fatty acid consumption in aquatic animals increased with higher environmental ammonia concentrations. However, the SFAs content was significantly higher in the HT group than that in the LT group in this study. This may be because high concentrations of ammonia may increase the free radical level in the E. sinensis meat (Wang et al., 2021), leading to the conversion of PUFAs into SFAs. The HT group had significantly lower PUFAs content compared to the LT group confirmed this speculation. This phenomenon has also been reported in a previous study on ivory shell (Babylonia areolata) after exposure to high levels of ammonia (Zhou et al., 2023). In addition, ammonia exposure significantly increased the PUFAs content in the E. sinensis meat compared to the CK group, indicating that PUFAs may be more valuable as functional components of biological membranes than as energy sources under ammonia exposure.

The n-3 PUFAs contribute to the nutritional value of the E. sinensis meat. DHA and EPA have preventive effects on cardiovascular and Alzheimer's diseases, as well as anti-inflammatory and immunomodulatory properties. In this study, low and high concentrations of ammonia significantly increased the n-3 PUFAs content, particularly EPA, in the E. sinensis meat. Similarly, Ran et al. (2017) revealed that the contents of EPA and DHA in razor clams (Sinonovacula constricta) increased when cultured in high-level salinity environments. We used the n-3/n-6 PUFAs and PUFAs/SFAs ratios as indices to evaluate the fatty acid nutrition of the E. sinensis meat; the ratios in each group ranged from 1.72 to 2.07 and 2.05–2.67, respectively. These values exceeded the minimum ratios of n-3/n-6 PUFAs and PUFAs/SFAs recommended by the FAO/WHO, which are approximately 0.1–0.2 and 0.4, respectively (FAO/WHO, 1994). The HT group had the highest n3/n6 ratio, while the LT group had the highest PUFAs/SFAs ratio. Regarding the fatty acid content, E. sinensis cultured in ammonia-accumulating environments may be better able to provide n-3 PUFAs. It is beneficial for balancing the fatty acid proportion of the human diet. In addition, Elmore, Mottram, Enser, and Wood (1999) demonstrated that the higher the PUFAs content in meat products, the richer their characteristic aromas. Thus, we speculate that the changes in the PUFAs content in the E. sinensis meat after ammonia exposure may lead to changes in its aroma profiles.

3.2. Aroma evaluation

Based on the aroma evaluation results of the E. sinensis meat samples exposed to different concentrations of ammonia, we constructed a radar plot (Fig. 1A) and intensity score distribution plots (Fig. S1) of the samples' aroma attributes. The fishy and meaty aromas were the strongest sensory attributes in the CK group, which similar to the finding of Yang et al. (2021). In addition, the fishy aroma of the E. sinensis meat was significantly attenuated by ammonia exposure. The meaty aroma was significantly weaker in the HT group than that in the CK group. The grassy and earthy aromas were the strongest aroma attributes in the LT group and were stronger than those in CK and HT groups. The overall aroma of the E. sinensis meat was weaker in the HT group than that in the CK and LT groups. These results indicated that the presence of ammonia in the culture environment was an important factor that affected the aroma profiles of the E. sinensis meat. Instrumental analyses were performed to further investigate the changes in the VOCs.

Fig. 1.

Fig. 1

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Aroma profiles and E-nose analyses of the Eriocheir sinensis meat after exposure to different ammonia concentrations. (A) The radar plot of the sensory scores. (B) The score plot of the principal component analysis (PCA) of the E-nose data. (C) The radar plot of the E-nose data. CK, control group; LT, low-concentration ammonia treatment group; HT, high-concentration ammonia treatment group. Different lowercase letters within a row indicate significant differences (p < 0.05).

3.3. E-nose analysis results

PCA is used to classify and visualize the differences between sample data. Fig. 1B shows the PCA results of the three group samples based on the E-nose data. The accumulated variance contribution rate of the PC1 and PC2 was 86 %, which indicated that the samples contained sufficient information. The CK, LT, and HT groups were well separated by PC1 and PC2. The radar graph (Fig. 1C) shows the response characteristics of the VOCs in the E. sinensis meat samples. The W1W, W1S, and W2W sensors exhibited the strongest responses to the VOCs in each group, indicating that the E. sinensis meat may contain high concentrations of inorganic sulfur compounds, methyl compounds, and organic sulfur compounds. These results resembled those of a previous research in which the W1W, W2W, W5S, and W1S sensors showed the strongest responses to the VOCs in E. sinensis meat from three ecological environments (Cheng et al., 2019). Further, we found that response intensities of sensors to the E. sinensis meat were significantly weaker in the LT group than those in CK and HT groups; this result differed from the sensory evaluation results. This may be because the E-nose analysis ignored the trace VOCs with extremely low aroma thresholds that significantly contributed to the aroma profiles of the E. sinensis meat.

3.4. HS-SPME-GC-MS analysis of the VOCs

In total, the HS-SPME-GC–MS analysis identified 140 VOCs in the E. sinensis meat (Table S2 and Fig. 2A). The relative contents of various categories of VOCs were counted in the E. sinensis meat (Fig. 2B). Alcohols had the highest relative content in each group (40.46–46.38 μg/kg) followed by S-containing compounds (21.51–44.12 μg/kg), aromatic compounds (26.49–38.41 μg/kg), and aldehydes (26.39–35.56 μg/kg). Ammonia exposure significantly reduced the content of the N-containing compounds (e.g., trimethylamine) in the E. sinensis meat. Compared with the other groups, both the total content of VOCs and contents of the aromatic compounds (e.g., toluene), S-containing compounds (e.g., methanethiol), and hydrocarbons (e.g., d-limonene) in the LT group also significantly decreased, alike the E-nose results. However, the content of alcohols (e.g., 4-dodecenol (Z)) significantly increased in the HT group compared to CK and LT groups while that of aldehydes (e.g., hexanal) significantly decreased, differing from the E-nose W2S sensor results. This may be because the HS-SPME-GC–MS detection technology is more sensitive and precise in chemical analysis than the E-nose. For example, Cheng et al. (2015) reported that the E-nose analysis cannot fully characterize the aroma characteristics of Chinese bayberry (Myrica rubra). Fig. 2C presents the hierarchical cluster heatmap of the VOCs, which more intuitively reveals the differences between the VOCs in the E. sinensis meat among the three groups. VOCs' contributions to the overall aroma of a food item depend on both their concentrations and thresholds. Table S3 presents the rOAV results for 72 of the 140 VOCs. In all three groups, six aroma-active compounds had rOAVs of greater than 1, and the contents of these compounds decreased significantly as the ammonia concentrations increased. Moreover, the rOAV results for octanal and nonanal were only greater than 1 in the CK group.

Fig. 2.

Fig. 2

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The volatile organic compounds (VOCs) in the E. sinensis meat after exposure to different ammonia concentrations. (A) The proportion of the VOC classes identified by the HS-SPME-GC–MS. (B) The relative content of the VOC classes identified by the HS-SPME-GC–MS. (C) The heat map clustering of the VOCs identified by the HS-SPME-GC–MS. (D) Topographic plots of the VOCs identified by the HS-GC-IMS. (E) Gallery plots of the VOCs identified by the HS-GC-IMS. CK, control group; LT, low-concentration ammonia treatment group; HT, high-concentration ammonia treatment group.

3.5. HS-GC-IMS analysis of the VOCs

The HS-GC-IMS analysis further detected the VOCs in the three groups' E. sinensis meat samples. Fig. 2D presents the top view of the GC-IMS topographic map of the samples. Each dot in the image represents the VOCs identified in the samples. The dot colors reflect the abundance of the VOCs; red represents a high abundance and white represents a low abundance. As shown in Fig. 2D, the abundance of some of the VOCs was significantly higher in LT and HT groups than in the CK group. A total of 36 peaks were obtained in the E. sinensis meat samples, among which 32 VOCs were identified and 4 other VOCs were unidentified. In particular, of the 32 VOCs, 10 compounds, such as butanal and ethyl acetate, were detected in both the monomer and dimer forms. Therefore, 22 distinct VOCs were identified in the E. sinensis meat samples, including eight aldehydes, five ketones, five alcohols, and four esters (Table S4). Among them, 11 VOCs (e.g., 3-methylbutanal) were simultaneously identified by the GC–MS and GC-IMS, whereas the other 11 VOCs (e.g., propanal) were not detected by the GC–MS. Moreover, hydrocarbons (e.g., pentane) detected by the GC–MS could not be discovered using the GC-IMS. These results confirmed the sensitivity and globality of the GC–MS and GC-IMS combination for obtaining information on the VOCs present in the E. sinensis meat. Fig. 2E presents the characteristic fingerprints of the VOCs. Each square represents a compound identified in a sample, and the color depth of the square is proportional to the abundance of the compound. Fig. 2E-a showed four VOCs (e.g., butanal (M)) with reduced abundance in LT and HT groups when compared to the CK group. Fig. 2E-b showed 10 VOCs (e.g., 2-methylbutanal (D)) with increased abundance in the LT group when compared to the CK group, while propanal (D) and butan-1-ol (M) showed increased abundance in both LT and HT groups (Fig. 2E-c).

3.6. Multivariate statistical analyses of the VOCs by the GC–MS and GC-IMS

Fig. 3A–B shows the PCA score plots of the VOCs in the E. sinensis meat among three groups as detected by the GC–MS and GC-IMS. The first two components cumulatively accounted for 74.5 % and 71.3 % of the total variance in the GC–MS and GC-IMS PCA score plots, respectively. The CK, LT, and HT groups were well-discriminated in both plots. The LT and CK groups displayed a significant difference regarding the aroma characteristics of the E. sinensis meat. PLS-DA, as a supervised discriminant analysis approach, can maximize interclass variance and has a better separation performance than PCA. We performed the PLS-DA to construct correlation models between the VOCs in the E. sinensis meat as detected by the GC–MS and GC-IMS analyses in the three treatments (Fig. 3C–D). In the GC–MS and GC-IMS PLS-DA score plots, the three groups were scattered across different locations, and the accumulated variance contribution rates of PC1 and PC2 were 91.6 % and 84.6 %, respectively. The model fits (R2) of the GC–MS and GC-IMS PLS-DA were 0.998 and 0.988, respectively, and their predictive abilities (Q2) were 0.979 and 0.909, respectively, suggesting that both models were feasible. The VIP can also be used to assess the contribution of variables to the discrimination of a PLS-DA model. In this study, there were 17 and 9 VOCs with VIP values over 1 in the GC–MS and GC-IMS PLS-DA models, respectively (Fig. 3E–F). These 26 key VOCs were considered as biomarkers to distinguish the aroma profiles of the E. sinensis meat among the three groups and are systematically presented in Table 2.

Fig. 3.

Fig. 3

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Multivariate statistical analyses of the volatile organic compounds (VOCs) in the E. sinensis meat after exposure to different ammonia concentrations. (A) The score plot of the principal component analysis (PCA) of the GC–MS data. (B) The score plot of the PCA of the GC-IMS data. (C) The score plot of the partial least squares-discriminant analysis (PLS-DA) of the GC–MS data. (D) The score plot of the PLS-DA of the GC-IMS data. (E) The VIP scores of PLS-DA of the GC–MS data. (F) The VIP scores of PLS-DA of the GC-IMS data. CK, control group; LT, low-concentration ammonia treatment group; HT, high-concentration ammonia treatment group.

Table 2.

Key volatile organic compounds in the E. sinensis meat after ammonia exposure as detected by the GC–MS and GC-IMS.

Compounds Relative concentration (μg/kg) or abundance
 VIP Odor attributes Detection method
CK LT HT
Trimethylamine 11.176 ± 2.04a 6.133 ± 1.42b 7.181 ± 0.50b 3.43 Fishy odor GC–MS
1-Octen-3-ol 10.127 ± 0.09a 8.768 ± 0.77b 8.141 ± 0.76b 1.44 Mushroom-like and fishy odors GC–MS
4-Dodecenol (Z) 0.524 ± 0.03c 2.484 ± 0.44a 1.511 ± 0.12b 1.32 Unknown GC–MS
5-Decen-1-ol (Z) 0.889 ± 0.04c 1.647 ± 0.10b 4.581 ± 0.26a 2.52 Unknown GC–MS
Hexanal 12.873 ± 1.15a 10.407 ± 5.33ab 5.590 ± 1.75b 5.32 Grassy and earthy odors GC–MS
Pentanal (D) 576.00 ± 45.21b 988.00 ± 120.50a 653.67 ± 166.00b 1.99 Grassy and earthy odors GC-IMS
Ethyl formate (D) 134.00 ± 24.27b 413.67 ± 114.15a 172.00 ± 37.04b 1.66 Fruity odor GC-IMS
Ethyl formate (M) 465.67 ± 36.91b 694.67 ± 75.14a 501.00 ± 49.96b 1.35 Fruity odor GC-IMS
Phenylethyl Alcohol 0.890 ± 0.03b 3.972 ± 2.31a 0.775 ± 0.08b 1.39 Floral odor GC–MS
Propanal (D) 970.00 ± 40.11b 1553.67 ± 291.08a 1448.00 ± 237.31a 2.95 Pungent odor GC-IMS
Butanal (M) 676.00 ± 17.52a 549.33 ± 63.44b 497.67 ± 58.77b 1.53 Pungent odor GC-IMS
Butanal (D) 299.33 ± 27.50a 199.67 ± 70.09ab 150.33 ± 48.21b 1.33 Pungent odor GC-IMS
Benzaldehyde 7.509 ± 0.67a 5.906 ± 0.29b 6.634 ± 0.55ab 1.08 Nutty odor GC–MS
Benzaldehyde, 3-methyl- 0.336 ± 0.01b 1.739 ± 1.08a 1.187 ± 0.23ab 1.36 Nutty odor GC–MS
2-Methylbutanal (D) 1402.67 ± 45.08b 1608.33 ± 94.48a 1370.33 ± 80.43b 1.59 Nutty odor GC-IMS
Methional 2.537 ± 0.17a 1.698 ± 0.32b 1.030 ± 0.10c 1.05 Onion-like, roasted, and meaty odors GC–MS
Borane-methyl sulfide complex 29.556 ± 1.82a 11.710 ± 4.46b 32.805 ± 8.00a 7.07 Onion-like, roasted, and meaty odors GC–MS
Thiophene, 2-methyl- 2.604 ± 0.28b 2.233 ± 0.22b 5.001 ± 0.56a 1.59 Onion-like, roasted, and meaty odors GC–MS
5-Methyl-2-thiophenecarboxaldehyde 4.249 ± 0.19a 3.094 ± 0.17b 1.199 ± 0.22c 2.10 Onion-like, roasted, and meaty odors GC–MS
Toluene 19.447 ± 1.83a 14.389 ± 1.29b 19.572 ± 1.68a 2.94 Plastic and metal-like odors GC–MS
Styrene 4.846 ± 0.58a 2.756 ± 0.62b 5.408 ± 0.53a 1.09 Plastic and metal-like odors GC–MS
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Note: CK, control group; LT, low-concentration ammonia treatment group; HT, high-concentration ammonia treatment group. VIP, variable importance in projection. Values are shown as the mean ± standard deviation (n = 3). Different lowercase letters within a row indicate significant differences (p < 0.05).

3.7. Characteristic VOCs identified by the GC–MS and GC-IMS

After exposure to ammonia, the changes in the key VOCs in the E. sinensis meat were analyzed to elucidate the effect of ammonia on the aroma profiles at the molecular level. Among these 26 key VOCs (VIP > 1) screened from the GC–MS PLS-DA model, trimethylamine, 1-octen-3-ol, hexanal, and methional were of concern because they were also aroma-active compounds (rOAV >1) that contributed to the aroma formation of the E. sinensis meat.

3.7.1. Trimethylamine

Trimethylamine, characterized by its typical fishy aroma, is produced through the reduction of trimethylamine oxide (TMAO) mediated by microorganisms and trimethylamine reductase (Huang et al., 2023). Consistent with the fishy aroma score in the aroma evaluation, the trimethylamine content was significantly lower in LT and HT groups compared to the CK group, suggesting that ammonia exposure may have weakened the fishy aroma of the E. sinensis meat. The indigenous microbiota carried by aquatic products plays a critical role in trimethylamine biosynthesis. Some specific spoilage organisms, such as Shewanella putrefaciens, have been reported to be main amine-producing bacteria in aquatic products (Yang et al., 2019). The decrease in trimethylamine content may be related to changes in the metabolic activities of microbiota in E. sinensis meat affected by ammonia exposure. However, further research is needed to thoroughly clarify the specific contribution of microbial metabolic changes to the observed reduction in trimethylamine production under ammonia exposure in this study through metagenomic analysis combined with in vitro microbial culture experiments. The TMAO in E. sinensis serves as both a metabolic substrate for microorganisms and an osmoprotectant for the host. Another reason for the decrease in trimethylamine content might be that more TMAO participated in osmoregulation under environmental stress, rather than being degraded into trimethylamine (Chen, Ye, Chen, & Yan, 2016).

3.7.2. Alcohols

Alcohols often present plant and floral aromas. Because of their high thresholds, most alcohols contribute little to the aromas of E. sinensis meat. However, some unsaturated enols have lower thresholds and may significantly contribute to the aromas of E. sinensis meat. 1-octen-3-ol is an oxidative degradation product of C18:2 n6 or C18:3 n3 and gives mushroom-like and fishy aromas (Mu et al., 2017). In this study, the 1-octen-3-ol content was significantly lower in LT and HT groups than in the CK group. Although the effect of ammonia on the aromas of aquatic products has not been previously investigated, the research on other environmental factors that affect the aromas of aquatic products is increasing. For example, Luo et al. (2021) found that low salinity reduced the trimethylamine and 1-octen-3-ol contents in mud crabs (Scylla paramamosain), which is similar to our results. In the present study, the 4-dodecenol (Z) and 5-decen-1-ol (Z) contents were significantly higher in LT and HT groups than in the CK group. These two enols may play a role in enriching the aromas of the E. sinensis meat; however, their aroma attributes are unknown and need to be further explored. Further, the phenylethyl alcohol content, which has a floral aroma, also increased significantly after low-concentration ammonia exposure.

3.7.3. Aldehydes

Straight-chain aldehydes are primarily derived from the oxidative degradation of PUFAs and have low thresholds; thus, they can greatly contribute to the aroma profiles of E. sinensis meat. Propanal and butanal give aquatic products a pungent aroma and have been identified in the meat of the large yellow croaker (Larimichthys crocea) (Mu et al., 2021). We found that the abundance of propanal (D) significantly increased in LT and HT groups compared to the CK group. The accumulation of propanal in LT and HT groups may have negatively affected the aroma profiles of the E. sinensis meat. As the carbon-chain length of the aldehydes increases, the pungent aromas gradually decreases. The C5-C9 aldehydes have a grassy aroma and are considered the main VOCs that give E. sinensis meat an earthy aroma (Phetsang et al., 2021). We found that compared with the CK group, the hexanal content in the HT group significantly decreased and the abundance of pentanal (D) in the LT group significantly increased, which was similar to the variation trends of the grassy and earthy aromas observed in the aroma evaluation. Moreover, the fruity and sweet aromas of the E. sinensis meat in the LT group may have been enriched by the accumulation of ethyl formate. Branched-chain aldehydes, including benzaldehyde, 3-methylbenzaldehyde, and 2-methylbutanal, give the E. sinensis meat a nutty aroma. The 3-methylbenzaldehyde and 2-methylbutanal (D) contents significantly increased in the LT group compared to the CK group. Wang et al. (2016) reported differences in the aldehyde contents, such as hexanal, nonanal, and benzaldehyde, in E. sinensis meat that stem from three different sources. Overall, the results suggest that the culture environment and concentration of environmental factors may significantly affect the aroma profiles of E. sinensis meat, while a low concentration of ammonia may enhance its plant and nutty aromas.

3.7.4. S-containing compounds

S-containing compounds generally have onion-like, roasted, and meaty aromas, which are derived from the Strecker degradation of S-containing amino acids (Ding et al., 2020). Nitrogen sources in the culture environment significantly impact the emissions of S-containing compounds. Coleman et al. (2023) observed an increased methional content in marine chlorophyte (Tetraselmis chuii) cultivated under the N-depleted condition. We found that compared with the CK group, the contents of most of the key S-containing VOCs in the E. sinensis meat, such as methional and borane-methyl sulfide complex, significantly decreased after ammonia exposure. In particular, the methional (rOAV >1) content significantly decreased when the ammonia concentration increased. Similarly, compared with the other groups, the contents of some of the N-containing compounds in the HT group, such as 2-methylpyrazine and 2-acetylthiazole, significantly decreased. These compounds can also produce roasted and meaty aromas in the E. sinensis meat. Although their rOAVs and VIP values were less than 1, they might have played modifying roles in the formation of the E. sinensis meat's aromas. These results indicate that ammonia exposure may reduce the onion-like, roasted, and meaty aromas of the E. sinensis meat in a dose-dependent way, which could explain the lower scores for the meaty aroma attribute in LT and HT groups.

3.7.5. Aromatic compounds

Aromatic compounds give E. sinensis meat plastic and metal-like aromas, which are produced through the Strecker degradation of aromatic amino acids (Wang et al., 2024). We found that the toluene and styrene contents were significantly lower in the LT group than in the other groups, suggesting that exposure to low concentrations of ammonia may have reduced the plastic and metal-like aromas. However, the naphthalene content was significantly higher in LT and HT groups than in the CK group. Gu et al. (2013) also detected naphthalene in E. sinensis meat and attributed it to environmental pollution. The poor metabolic status of E. sinensis when exposed to ammonia may facilitate the transfer of naphthalene from the environment to the E. sinensis.

3.8. Correlation analysis

To elucidate the mechanisms underlying the changes in the key VOCs in the E. sinensis meat after ammonia exposure, a Pearson's correlation analysis was performed between the key PUFAs-derived VOCs and PUFAs (Fig. 4). Multiple VOCs that gave the E. sinensis meat its different aromas were associated with the same fatty acids, indicating that the fatty acid composition may have greatly affected the aroma profiles of the E. sinensis meat. For example, 1-octen-3-ol, benzaldehyde, butanal (M), butanal (D), and hexanal were all positively correlated with C18:2 n6 (p < 0.05); 4-dodecenol (Z), pentanal (D), and propanal (D) were all positively correlated with C20:4 n6 and EPA (p < 0.05), while 2-methylbutanal (D) exhibited a positive correlation with EPA (p < 0.05). PUFAs are oxidized through oxidative degradation pathways, such as lipoxygenase (LOX) oxidation and lipid peroxidation to generate reactive intermediates, which further decompose into aldehydes, alcohols, and ketones—key contributors to aroma profiles of E. sinensis meat (Shchepinov, 2020). Based on the linear relationship between PUFAs-derived VOCs and PUFAs presented by the correlation analysis results, coupled with our previous findings on ammonia-induced oxidative stress in E. sinensis (Wang et al., 2021), we speculate that the changes in PUFAs-derived VOCs in crab meat exposed to ammonia may be caused by lipid peroxidation.

Fig. 4.

Fig. 4

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Correlation heatmap of the key volatile organic compounds (VOCs) with polyunsaturated fatty acids in the E. sinensis meat after exposure to different ammonia concentrations. * indicates 0.01 < p ≤ 0.05, ** indicates 0.001 < p ≤ 0.01, and *** indicates p ≤ 0.001.

3.9. Limitations and prospects

Although a correlative relationship was established between VOCs and fatty acid oxidative degradation in this study, direct validation of the presumed mechanism by which lipid peroxidation-triggered oxidative degradation pathways of PUFAs contribute to the altered aroma profiles of crab meat under ammonia exposure remains lacking. Future studies will prioritize analyzing the content of lipid peroxidation markers (malondialdehyde), while integrating multi-omics approaches (lipidomics and transcriptomics) to validate and map the regulatory network of ammonia-induced lipid peroxidation on aroma profiles of crab meat.

Additionally, evaluating the effect of ammonia exposure on the aroma profiles of E. sinensis meat in a laboratory environment may have certain limitations. In actual aquaculture water environments, the concentration of ammonia fluctuates because of other environmental factors, such as pH and temperature. The potentially beneficial low-level ammonia (10.47 mg/L) identified in this study requires verification and optimization in practical production. For high-level ammonia exposure environments, it is necessary to develop functional feed additives, such as exploring the efficacy of dietary antioxidants in counteracting ammonia-induced lipid peroxidation, ensuring the health of E. sinensis while pursuing ideal aroma characteristics.

4. Conclusion

This study screened 26 key VOCs as biomarkers to differentiate aroma profiles of the E. sinensis meat exposed to varying ammonia concentrations. Ammonia exposure attenuated fishy and meaty aromas while enhancing plant and nutty aromas at low concentrations. The LT group exhibited reduced plastic/metallic aromas and improved sensory acceptability, while the HT group presented a weakened overall aroma. Notably, the ammonia-treated E. sinensis meat contained higher levels of n-3 PUFAs, particularly EPA. The strong correlations between the PUFAs-derived VOCs and PUFAs may suggest potential pathways involved in the production of PUFAs-derived VOCs after ammonia exposure, namely lipid peroxidation under oxidative stress. These findings provide feasible insights for optimizing aquaculture practices. Specifically, this means that maintaining environmental ammonia at a low level (10.47 mg/L) could enhance desirable flavors and n-3 PUFAs content.

CRediT authorship contribution statement

Tianyu Wang: Writing – original draft. Hang Lu: Software. Yuanyong Tian: Methodology. Hui Zhao: Resources. Xuefeng Lu: Writing – review & editing. Zhaoxia Wu: Project administration. Shiwei Niu: Funding acquisition.

Ethics statement

Animal experiments were reviewed and approved by the Institutional Animal Care and Use Committee of Shenyang Agricultural University, with the approval number 2021092205. All procedures for sensory evaluation complied with relevant laws and institutional guidelines and were approved by the Scientific Research Academic Committee of College of Food Science, Shenyang Agricultural University.

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.

Acknowledgments

This work was supported by the Science and Technology Program Joint Foundation Project of Liaoning Province (2024-BSLH-036) and Application and Foundation Research Project of Liaoning Province (No. 2023JH6/100100033).

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.fochx.2025.102952.

Contributor Information

Zhaoxia Wu, Email: wuzxsau@163.com.

Shiwei Niu, Email: niushiwei@126.com.

Appendix A. Supplementary data

Supplementary material 1

mmc1.docx (259.5KB, docx)

Data availability

Data will be made available on request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary material 1

mmc1.docx (259.5KB, docx)

Data Availability Statement

Data will be made available on request.

Articles from Food Chemistry: X are provided here courtesy of Elsevier

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