
==== Front
Food Chem X
Food Chem X
Food Chemistry: X
2590-1575
Elsevier

S2590-1575(24)00623-0
10.1016/j.fochx.2024.101735
101735
Research Article
Application of Lactiplantibacillus plantarum hydrogel coating in combination with ice temperature for the preservation of fresh yak meat
Jiang Li-Shi a1
Li Yun-Cheng b1
Zheng Fu-Xu b
Zhang Meng-Jiao a
Zheng Wen-Xuan a
Liu Da-Yu bc
Meng Fan-Bing mfb1020@163.com
bc⁎
a School of Public Health, Chengdu University of Traditional Chinese Medicine, Chengdu 611137, PR China
b College of Food and Biological Engineering, Chengdu University, Chengdu 610106, PR China
c China Agricultural University-Sichuan Advanced Agricultural & Industrial Institute, Chengdu 610046, PR China
⁎ Corresponding author: College of Food and Biological Engineering, Chengdu University, No. 2025 Chengluo Road, Chengdu, China. mfb1020@163.com
1 These authors contributed equally to this work.

12 8 2024
30 10 2024
12 8 2024
23 10173510 6 2024
10 8 2024
11 8 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-nc/4.0/).
Fresh yak meat is highly nutritious and prone to spoilage, so developing suitable preservation methods is crucial. In this study, hydrogel coatings composed of konjac glucomannan, Lactiplantibacillus plantarum and gallic acid (KGX) were applied to preserve fresh yak meat under ice temperature (−1 °C). After 16 days, KGX group showed lowest total viable count (5.3 ± 0.1 log cfu/g) and total volatile basic nitrogen (13.02 ± 1.40 mg/100 g), which did not exceed the relevant standards of fresh meat. Combined assessments of color, texture, pH, drip loss rate, and thiobarbituric acid reactive substances indicated that KGX coating effectively prolonged yak meat preservation. High-throughput sequencing revealed that KGX coating effectively reduced the abundance of Pseudomonas and Candida. The application of L. plantarum hydrogel coatings in conjunction with ice temperature increased the shelf life of fresh yak meat to 16–20 days, suggesting its potential as a viable preservation method for fresh meat.

Highlights

• Ice-temperature combined with hydrogel coating was used to preserve fresh yak meat.

• Hydrogel prepared by L. plantarum and gallic acid could extend shelf life to 16–20 d.

• Hydrogel coating showed superior capacity to keep color, texture and moisture.

• Hydrogel coating could effectively control Pseudomonas and Candida growth in meat.

Keywords

Fresh yak meat
Ice temperature
Lactiplantibacillus plantarum
Hydrogel coating
Quality properties
Microbial community
==== Body
pmc1 Introduction

The yak, which is often regarded as the “treasure of the plateau”, is an endemic species that lives in the Himalayas of China (Nie et al., 2020). Yak meat contains high content of protein (20% - 23%) and monounsaturated fatty acid (45.15%). It is also rich in amino acids, with a higher content of essential amino acids compared to ordinary beef. Consequently, fresh yak meat is highly prone to microbial contamination and lipid oxidation (Huang et al., 2022). Given that yaks inhabit remote highland areas, the development of appropriate preservation techniques becomes imperative for marketing fresh yak meat.

Refrigeration and freezing are the conventional preservation methods utilized for fresh meat (Lee et al., 2023). Traditional refrigeration temperatures typically range from 1 to 4 °C, thus providing a storage duration of merely 2 to 4 days for fresh meat without additional measures (You et al., 2020). Frozen storage can prolong shelf life; however, it may introduce challenges such as drip loss, protein denaturation, and diminished product quality due to damage from ice crystal formation. Ice temperature preservation is a novel approach to fresh food preservation involving temperature control ranging from 0 °C to the freezing point (Sun et al., 2020). It has been used to preserve fresh meat and has shown good efficiency (Sun et al., 2020). However, integrated composite preservation technology is a research direction of fresh meat storage because the effect of single preservation technology is limited. Currently, active biopolymer coatings have great potential to extend the shelf life of fresh meat, and their application has received increasing attention (Umaraw et al., 2020).

Previous research had demonstrated the effectiveness of macromolecular polymers, specifically polysaccharides and proteins, in producing edible films with unique barrier properties. This capability reduces moisture diffusion and prevents the penetration of oxygen and microorganisms during food preservation (Abdel-Naeem et al., 2021). Furthermore, incorporating bioactive compounds into these films to create interactive food packaging systems, which offer active functionalities such as antioxidants, antimicrobial properties, and quality monitoring, is gaining recognition as a significant advancement in the field (Cheng et al., 2024).

Konjac glucomannan (KGM), which is a water-soluble polysac-charide and it as a thickener that exhibits a remarkable water-holding capacity and unique gelation activity (Chen et al., 2023). It is often used as a material for preparing hydrogels for fresh food preservation (Zhou et al., 2021). Lactic acid bacteria are often added to hydrogels for fresh food preservation (Yuan et al., 2022) because they can generate various antimicrobial metabolites (lactic acid, acetic acid, low-molecular-weight substances such as diacetyl and fatty acids) during growth and fermentation (Castellano et al., 2017). Moreover, gallic acid (GAL) is a dietary polyphenol renowned for its potent antioxidant activity and is essential for maintaining food quality and extending shelf life (F. Zhu, 2021). It was used to coat and preserve fresh pork, exhibiting excellent antibacterial and antioxidant properties, thus maintaining the freshness of pork at a pH value below 6.5 for 24 h at room temperature (Rong et al., 2023).

In this study, hydrogel coatings (mixed with L. plantarum, GAL and KGM) and ice-temperature preservation techniques were combined for fresh yak meat preservation. The impact of various bio-coating treatments on quality alterations was examined through the assessment of physicochemical parameters and microbial diversity. It was hypothesized that the shelf life of fresh yak meat stored on ice temperature could be prolonged by the combined antimicrobial, antioxidant, and water retention effects of the hydrogel coating. These findings are anticipated to offer valuable insights for related experiments.

2 Materials and methods

2.1 Materials and chemicals

Fresh yak meat was provided from Chengdu Jiaruiyuan Food Co., Ltd. (Sichuan, China). It was slaughtered according to the standard procedures of National Standards of China (GB/T19477–2018), and the hind leg meat was packed in sterile bags, placed on ice and transported to the laboratory within 2 h. KGM (Mw = 2.895 × 106 g/mol, purity: 95.0%) was purchased from Mianyang Anfu Konjac Development Co., Ltd. (Mianyang, China). L. plantarum XZ-14 was isolated from the koji of Tibetan Qingke liquor (Meng et al., 2022). Staphylococcus aureus, Escherichia coli, and Listeria monocytogenes were purchased from Beijing Biowe Biotechnology Co., Ltd. (Beijing, China). PCA （plate count agar）medium was purchased from Solarbio Science & Technology Co., Ltd. (Beijing, China). Ethanol, edetate disodium, boric acid, hydrochloric acid, and methyl red were purchased from Chron Chemicals Co., Ltd. (Chengdu, China). Gallic acid (GAL), trichloroacetic acid, thiobarbituric acid, magnesium oxide, bromothymol blue, sodium chloride, and glucose were purchased from Shanghai Yuanye Bio-Technology Co., Ltd. (Shanghai, China). Unless specified otherwise, all other compounds were of analytical reagent grade.

2.2 Activation and cultivation of strains

L. plantarum strain XZ-14 was first activated in MRS (De Man, Rogosa and Sharpe) liquid medium at 37 °C to the logarithmic phase, after which 200 μL of the culture was inoculated into 5 mL of MRS liquid culture medium and anaerobically incubated at 37 °C for 24 h, thus resulting in first-generation strain solutions. This process was repeated by inoculating 200 μL of the first-generation solution into another 5 mL of MRS liquid culture medium to prepare the second-generation solution for subsequent use. Similarly, two types of gram-positive bacteria (S. aureus and L. monocytogenes), as well as one type of gram-negative bacteria (E. coli), which served as pathogenic indicator bacteria, were activated by using a similar step. Specifically, 200 μL of the activated strain solution was inoculated into LB (Luria-Bertani) culture medium and cultured on a shaker at 37 °C and 150 rpm for 12–16 h to the logarithmic phase (Luo et al., 2023), thus resulting in first-generation strain solutions. The process was then repeated to obtain a second-generation strain solution for subsequent antibacterial experiments.

2.3 L. plantarum bacteriostatic assay

Bacteriostatic inhibition experiments were conducted according to Wang et al. (M. Wang, Li, Meng, et al., 2023) with minor modifications. The second-generation strain solution of the pathogenic indicator bacteria was diluted to 105 cfu/mL by using sterile saline solution, after which 100 μL of the diluted strain solution coating was pipetted onto LB agar plates. Subsequently, two Oxford cups were tightly placed on the surface of the solid media, and 100 μL of a second-generation solution of L. plantarum XZ-14 (107 cfu/mL) was pipetted into it. The plates were then incubated in an incubator at 37 °C for 8–10 h, after which the diameter of the antibacterial zone was recorded.

2.4 Preparation of coating hydrogels

Four types of coating hydrogels were prepared: L. plantarum XZ-14 strains in saline (XZ), gallic acid in konjac glucomannan hydrogel (KG), L. plantarum XZ-14 strains in konjac glucomannan hydrogel (KX), and a combination of gallic acid and L. plantarum XZ-14 strains in konjac glucomannan hydrogel (KGX). First, the L. plantarum suspension (as described in Section 2.2) was centrifuged at 4 °C and 6000 × g for 10 min to obtain the strains by removing the supernatant. One gram of the L. plantarum strain was resuspended in 100 mL of saline (0.9%, w/v) after washing twice to obtain the XZ solution (1%, w/v). Second, 1 g of KGM was added to distilled water (100 mL) at 50 °C with constant stirring until it dissolved completely to formulate the KGM hydrogel (1%, w/v) (Chen et al., 2023). Afterward, the GAL (0.2 g) (Yu Cao et al., 2019) and L. plantarum strains (1 g) were added to 100 mL of KGM hydrogel (1%, w/v) and stirred vigorously until evenly dispersed to prepare the KG and KX hydrogels (Khodaei & Hamidi-Esfahani, 2019). Finally, the KGX hydrogel could be obtained by mixing sufficient amounts of GAL (0.2 g) and L. plantarum strains (1 g) in 100 mL of KGM hydrogel (1%, w/v).

2.5 Rheological properties of the coated hydrogels

Following the method described by Wang et al. (M. Wang, Li, Meng, et al., 2023), the rheological properties of the coated hydrogels were measured by using a rheometer (CSL2100, Antorypa Trading Co. Ltd., Shanghai, China). A concentric cylinder system with a pendulum (d = 28 mm) and a cup (d = 30 mm) was used to connect the apparatus. A volume of 10 mL of the sample was transferred into the rheometer using a micropipette. Shear rates ranging from 1−1 s to 100−1 s were applied for steady shear analysis to obtain the flow curve of the coating hydrogel. To identify the linear viscoelastic region (LVER) of the coating hydrogel, a strain sweep ranging from 0.1% to 1000% was conducted at a frequency of 1 Hz. Frequency sweep measurements were carried out from 0.1 to 100 rad/s at a 5% strain level. All the abovementioned procedures were conducted at 25 °C and repeated twice.

2.6 Meat coating and sampling

Fresh yak hind leg meat was trimmed of visible fat and then cut into uniform pieces (5 × 5 × 3 cm) before being randomly allocated into 5 groups. The meat surface was evenly coated with four types of coating hydrogels (XZ, KG, KX, and KGX, which are described in Section 2.4), whereas a blank control group (DZ) received no coating. Subsequently, all the samples were packaged with polyethylene preservation bags and preserved in a refrigerator (Qingdao Haier Co. Ltd., China) at −1 °C with a humidity of 38% to 43% for 24 days. The physicochemical indices and TVC (total viable count) values were determined for the samples at 0, 4, 8, 12, 16, 20, and 24 days. Samples stored up to day 20 (DZ20, XZ20, KG20, KX20, and KGX20) and the control group on day 0 (DZ0) were collected for high-throughput sequencing analysis of microorganisms.

2.7 Color and texture measurements

A portable colorimeter (NH300, Shenzhen Threenh Technology Co., Ltd. China) with illuminant D65/10° observer angle and aperture size of 8 mm was utilized to measure the L* (brightness), a* (redness), and b* (yellowness) values of the meat, and five measurements were taken at different positions on each sample to calculate the average. The meat cut into 2 cm3 pieces and Textural analysis (TPA) was conducted by TA-XT plus C texture analyzer (Stable Micro System, Godalming, UK) in the direction of the vertical muscle fibers for measurement with P/36R probe model. The test, pretest, and posttest speeds were configured as 1, 2, and 2 mm/s, respectively. The deformation ratio and contact point value were set at 50% and 5, respectively.

2.8 pH value, drip loss rate, TBARS (thiobarbituric acid reactive substances), TVB-N (total volatile basic nitrogen), and TVC (total viable count) measurements

A portable pH meter (Testo 205, Instruments GmbH, Germany) with NTC (negative temperature coefficient) sensor and pH meter (glass electrode) was used to measure the pH value based on the Chinese standard GB 5009.237–2016.

The drip loss rate of the samples was measured as follows. Each meat sample was weighed separately after splitting. The solution was removed every 4 days and left at room temperature for 1 h. Afterward, it was reweighed after the surface moisture was gently drained with dry filter paper to get the post-preservation weight. The drip loss rate was calculated by using the following equation:(1) Driplossrate%=m0−mm0×100%

where m0 is the original weight, and m is the post-preservation weight.

The TBARS value was measured according to the methods of Rao (Rao et al., 2022) with minor modifications. The minced sample (5 g) was weighed and mixed with trichloroacetic acid (TCA, 50 mL) and then oscillated via a constant temperature oscillator (50 °C, 30 min). The mixture was then centrifuged at 2000 × g for 10 min after cooling to room temperature. After centrifugation, 5 mL of the supernatant was mixed with 5 mL of thiobarbituric acid (TBA) and placed in a stoppered test tube to react for 30 min in a water bath (90 °C), followed by cooling with cold water. Finally, the absorbance was measured at a wavelength of 532 nm using a spectrophotometer with the TCA and TBA mixture as the blank. TBARS was calculated by using the following equation:(2) TBARSmg/kg=A532m×9.48

where m is the sample mass. The constant 9.48 is determined based on the absorbance of a specific quantity of thiobarbituric acid-malonaldehyde complex at 532 nm.

The TVB-N was measured according to the methods described in Chinese standards GB 5009.228–2016. Briefly, 20 g of meat was placed into a sealed conical flask, followed by the addition of 100 mL of water with precision. The solution was agitated until uniformly dispersed. After 30 min of maceration, the mixture was filtered. Subsequently, 10 mL of the filtrate was collected to determine the total nitrogen content in the beef samples using a KDN-102C nitrogen tester (Shanghai Qianjian Instrument Co., Ltd., Shanghai, China).

The TVC was determined using the plate count method according to GB 4789.2–2016. Yak meat samples were blended with sterile saline (0.9%, m/v) at a ratio of 1:9 (m/v) and homogenized for 2 min using a SCIENTZ-11 sterile homogenizer (Ningbo Xinzhi Biotechnology Co. Ltd., Ningbo, China). After appropriate dilution, the sample suspension was spread onto count agar plates and incubated at 36 °C for 48 h. Colony counts were enumerated and expressed as log colony forming units (CFU)/g.

2.9 Microbial diversity analysis

Microbial genomic DNA was extracted from each meat sample (day 0 and day 20) by using the FastDNA® Spin Kit for Soil (Omega Biotek, Norcross, GA, U.S.) according to the manufacturer's instructions. The DNA extracted was assessed for concentration and purity using a NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, Waltham, MA), and its quality was verified through 1% agarose gel electrophoresis. For bacterial 16S rRNA gene amplification targeting the V3-V4 region and fungal internal transcribed spacer (ITS) DNA region, the primers 338F (5′-ACTCCTACGGGAGGCAGCAG-3′) and 806R (5′- GGACTACHVGGGTWTCTAAT-3′) were utilized, along with ITS1F (5’-CTTGGTCATTTAGAGGAAGTAA-3′) and ITS2R (5’-GCTGCGTTCTTCATCGATGC-3′). The PCR amplification was performed using an ABI GeneAmp PCR System 9700 (Thermo Fisher). The procedure included an initial denaturation step at 95 °C for 3 min, followed by 27 cycles of denaturation at 95 °C for 30 s, annealing at 55 °C for 30 s, and extension at 72 °C for 45 s, with a final extension step at 72 °C for 10 min, and then held at 4 °C. After amplification, the PCR products were retrieved from 2% agarose gels, purified using a PCR Clean-Up Kit (YuHua, Shanghai, China) according to the manufacturer's protocol, and quantified with a Qubit 4.0 fluorometer (Thermo Fisher Scientific, USA). The purified PCR products were subjected to paired-end sequencing on an Illumina PE300 platform (Illumina, San Diego, USA) following standard protocols, conducted by Majorbio Bio-Pharm Technology Co., Ltd. (Shanghai, China).

2.10 Statistical analysis

Experimental data were performed in three independent experiments (n = 3) and expressed as mean ± standard deviation (SD). Data analysis was conducted using SPSS Statistics 20.0 (IBM, Inc., USA). Statistical significance was determined using one-way analysis of variance (ANOVA) followed by Duncan's multiple-range test, with a significance level set at p < 0.05. Microbiota bioinformatic analysis was conducted utilizing the Majorbio Cloud platform (https://cloud.majorbio.com). To assess differences in alpha diversity among groups, Wilcoxon rank-sum tests were conducted. Principal Coordinate Analysis (PCoA) using the Bray-Curtis distance algorithm was employed to examine similarities in microbial community structures across samples. Additionally, PERMANOVA (permutational multivariate analysis of variance) tests were applied to compare microbial community structures between groups, aiming to identify significant variations. Differential taxa at various taxonomic levels, from phylum to species, were identified among groups using LEfSe (linear discriminant analysis effect size) analysis (http: // huttenhower.sph.harvard.edu/LEfSe), with a threshold of LDA (linear discriminant analysis) > 2 and p < 0.05.

3 Results and discussion

3.1 Evaluation of bacteriostatic activity

Staphylococcus, Escherichia, and Listeria are common genera of pathogenic bacteria found in fresh meat, posing potential risks to human health (Castellano et al., 2017). L. plantarum strains isolated from various food sources frequently exhibit antimicrobial properties (Mao et al., 2020). However, significant diversity within L. plantarum strains has been observed due to the genetic heterogeneity of the species (Shi et al., 2024). To identify the appropriate Lactobacillus strain for the bio-coating hydrogel, antimicrobial efficacy was assessed based on the bacteriosphere diameter. As depicted in Fig. 1A, the antibacterial zones of L. plantarum against S. aureus, L. monocytogenes, and E. coli measured 18.85 ± 0.48, 18.51 ± 0.32, and 16.22 ± 0.21 mm, respectively. All the inhibition zone diameters exceeded 16 mm, thus indicating the antibacterial properties of L. plantarum XZ-14 to all three bacterial strains and highlighting its potential utility as a coating material for antibacterial applications. The antimicrobial efficacy may be attributed to the production of various antimicrobials, including lactic, acetic, propionic, formic, and caprylic acids, as demonstrated by (Mao et al., 2020). These compounds disrupt bacterial cell membrane structures, thereby inhibiting bacterial growth and reproduction (Shi et al., 2024).Fig. 1 Evaluation of the bacteriostatic activity of Lactiplantibacillus plantarum (A) and the rheological properties of the coated hydrogels (B). (A1) Staphylococcus aureus, (A2) Escherichia coli, (A3) Listeria monocytogenes, (B1) shear strain scans from 0.1 to 1000%, (B2) frequency scans, (B3) flow curves.

Fig. 1

3.2 Rheological properties of the coating hydrogel

According to Fig. 1B1, the storage modulus (G′) and loss modulus (G") were constant, thus showing that the sample was in a gel state within the linear viscoelastic region at the beginning of the test. As the amplitude increased, an intersection point occurred between G′ and G", and then G" > G′, thus indicating a flowing state of the sample. A strain of 5% was chosen for frequency scanning within the linear viscoelastic region. In frequency scanning, the storage modulus (G′), loss modulus (G"), and other indices are often used to evaluate the elastic and viscous behaviors of the sample, as well as its mechanical strength (Liu et al., 2024). According to Fig. 1B2, the G" values of the XZ group were always greater than the G′ values, thus indicating a liquid state of the hydrogel, whereas the other groups showed modulus intersection points, thus indicating the presence of typical noncrosslinked polymers.

Hydrogels with moderate viscosity made it easier to form uniform films (Shivangi et al., 2021). As shown in Fig. 1B3, the almost linear relationship between shear rate and viscosity for the XZ group indicated that it was a low-viscosity Newtonian fluid (Li et al., 2017). The other hydrogels, which included KGM, demonstrated clear shear-thinning characteristics, with the viscosity decreasing as the shear rate increased. The KX group exhibited the fastest decrease in viscosity, which is potentially due to the acid produced by L. plantarum, which decreased the viscosity in low-acid environments (Shivangi et al., 2021).

3.3 Evaluation of the preservation effects of different hydrogel coatings on fresh yak meat

3.3.1 Color

Changes in the color of the fresh yak meat were evaluated by using L*, a*, and b* values, as shown in Fig. 2A, B, and C. The L* value of all the samples decreased with the increase in storage time, which is consistent with the current literature (Zeng et al., 2023). The decrease in L* values may be attributed to the decomposition and denaturation of proteins in yak meat by microorganisms, leading to increased light dispersion (Xia et al., 2019).Fig. 2 Effect of different coating treatments on the color difference and overall appearance of fresh yak meat. (A) L* value, (B) a* value, (C) b* value, and (D) Overall appearance. Different letters represent significant differences within different groups at the same storage time (p < 0.05).

Fig. 2

Higher a* values correlate with greater consumer acceptance (W. Zhu et al., 2024). Fluctuations in the a* value predominantly arise from alterations in myoglobin (Mb) in meat product. Three distinct redox forms of Mb can be found in fresh meat: deoxymyoglobin (DMb), oxymyoglobin (OMb), and metmyoglobin (MMb). Discoloration is caused by an accumulation of MMb (brown) on the surface of meat due to the oxidation of OMb (bright cherry red color) and DMb (purple-red) (Tushar et al., 2023). As depicted in Fig. 2B, the gradual decline in a* values during storage likely corresponds to the oxidation of DMb and OMb into MMb over time (Cha et al., 2023). Fig. 2D illustrates the gradual transition of fresh beef color from bright red to brownish during storage. Chemical changes such as lipid and protein oxidation can lead to the oxidation of Mb, resulting in diminished color and acceptability of meat (Tushar et al., 2023). Plant polyphenols can inhibit the lipids and proteins oxidation in meat, thereby promoting brighter red color (W. Zhu et al., 2024). In the later stages (16 – 24 d), the KG groups demonstrated higher a* value compared to the other groups, followed by KGX and KX group. This difference may be attributed to the GAL in the hydrogel coating, which inhibited the formation of MMb and improved the retention of red color in the samples (Zou et al., 2022). High b* values were linked to high lipid oxidation (Cha et al., 2023). The KGX group consistently maintained lower b* values throughout storage, this may be related to its lower degree of fat oxidation. It was further confirmed by the TBARS value in the following section.

3.3.2 Texture

The texture index is an important criterion for the quality of meat product (Zhang et al., 2023). The hardness, springiness, cohesiveness, gumminess, chewiness, and resilience of yak meat under different coating treatments are shown in Fig. 3. Throughout the preservation period, all the groups exhibited a declining trend in texture characteristics. Specifically, on the 24th day, the hardness (Fig. 3A) and chewiness (Fig. 3B) of the KGX group decreased by 65.3% and 11.2%, respectively. Comparatively, regarding hardness and chewiness, the DZ group experienced reductions of 86.2% and 80.6%, the XZ group experienced decreases of 65% and 42.9%, the KG group experienced decreases of 71.5% and 37.7%, and the KX group experienced decreases of 71.9% and 49.1%, respectively. This suggests that the KGX group maintained superior hardness and chewiness of yak meat throughout the preservation process. On the 24th day, the springiness (Fig. 3C), cohesiveness (Fig. 3D), and gumminess (Fig. 3E) of yak meat in the DZ group decreased by 51.4%, 48.7%, and 71.1%, respectively; those in the XZ group decreased by 48.1%, 45.7%, and 61.8%, respectively; those in the KG group decreased by 55.1%, 54.2%, and 51.1%, respectively; those in the KX group decreased by 52.6%, 48.5%, and 76.5%, respectively; and those in the KGX group decreased by 54.2%, 46.9%, and 55.9%, respectively. This indicates that the XZ group demonstrated the most effective preservation of springiness and cohesiveness, followed by the KGX group. Resilience (Fig. 3F) decreased by 59.7%, 48.9%, 35.5%, 64.6%, and 61.3% for the DZ, XZ, KG, KX, and KGX groups, respectively. In summary, samples coated with KGX hydrogel effectively preserved the texture characteristics of fresh yak meat. Previous research (Cui et al., 2021) demonstrated that hydrogel wrapping acted as a barrier, delaying quality deterioration and thereby maintaining fresh meat's texture.Fig. 3 Effect of different coating treatments on the texture of yak meat. (A) Hardness, (B) Chewiness, (C) Springiness, (D) Cohesiveness, (E) Gumminess, and (F) Resilience. Different letters represent significant differences within different groups at the same storage time (p < 0.05).

Fig. 3

3.3.3 pH value

With prolonged storage, the pH tends to increase due to the accumulation of metabolites generated during microbial growth in meat, thus making it a key indicator of refrigerated meat freshness. According to the criteria for assessing chilled meat freshness, fresh meat is typically characterized by pH values ranging from 5.8 to 6.3, whereas those of sub-fresh meat are between 6.3 and 6.6. When the pH value of fresh meat exceeds 6.6, it indicates that it may have already spoiled (Yinjuan Cao et al., 2024). As shown in Fig. 4A, by the 16th day, the pH of the DZ group (6.3) exhibited sub-fresh meat characteristics, whereas the pH of the other coating groups remained within the range of the parameters for fresh meat. This finding underscored the efficacy of biocoating treatments in delaying the spoilage of fresh yak meat. By the 24th day, the pH values had exceeded 6.6 in all the groups except for the XZ group. Throughout storage, the pH values of the XZ group remained stable within the range of 5.4 to 5.6. This stability may be attributed to the introduction of lactobacilli onto the meat surface, which can produce acids (Khodaei et al., 2019) to lower the pH of fresh meat. In the subsequent analysis of microbial diversity, Lactobacillus became dominant in this group by day 20, further confirming this observation.Fig. 4 Effect of different coating treatments on chemical and microbial changes in fresh yak meat. (A) pH, (B) Drip loss rate, (C) Thiobarbituric acid reactive substances (TBARS), (D) Total volatile basic nitrogen (TVB-N), and (E) Total viable count (TVC). Different letters represent significant differences within different groups at the same storage time (p < 0.05).

Fig. 4

3.3.4 Drip loss rate

During preservation, the drip loss rate is a key criterion for assessing fresh yak meat quality (Zhang et al., 2023) because the quality of fresh beef is compromised by water loss stemming from decreased muscle water holding capacity. As shown in Fig. 4B, the drip loss rate of fresh yak meat gradually increased over the storage period. By day 24, the drip loss rates of the DZ (22.05 ± 0.9%) and XZ (19.91 ± 0.6%) groups exceeded those of the KG (12.89 ± 0.5%), KX (13.42 ± 0.7%), and KGX (12.46 ± 1.3%) groups. Research indicated that water evaporation was also a significant factor contributing to drip loss in meat (Chang et al., 2019). The discrepancy may be attributed to the water retention effect of KGM (Zhou et al., 2021). According to Wang et al. (S. Wang, Li, He, et al., 2023), KGM hydrogels effectively inhibited water diffusion in meat while demonstrating excellent water absorption capabilities. This can regulate vapor pressure in the microenvironment surrounding of the meat, thereby maintaining the moisture.

3.3.5 TBARS value

The monounsaturated fatty acid of fresh yak meat is as high as 45.15%, the instability of fat structure leads to its easy oxidation (Huang et al., 2022). As shown in Fig. 4C, fresh yak meat initially exhibited a TBARS value of 0.08 ± 0.01 mg/kg. After 24 days, the TBARS values increased to 0.30 ± 0.01, 0.18 ± 0.01, 0.20 ± 0.01, 0.21 ± 0.01, and 0.19 ± 0.01 mg/kg for the DZ, XZ, KG, KX, and KGX groups, respectively. Compared to those in the blank group, the TBARS values observed in the coating group were notably lower (p < 0.05). It might be due to the GAL, which can inhibit lipid peroxidation (Yu Cao et al., 2019). In addition, when the sample was covered with a hydrogel coating, lipid oxidation of the sample was delayed because oxygen cannot directly contact the sample (Zhou et al., 2021). Particularly the KGX group, which exhibited lower TBARS values compared to the other groups at both 16 and 20 days. This suggests that KGX effectively retards the oxidation of meat fat for a certain period.

3.3.6 TVB-N value

The TVB-N values of fresh meat may increase over time due to protein degradation caused by spoilage bacteria and endogenous enzymes (Chang et al., 2019). Therefore, the TVB-N value is a major freshness indicator for fresh meat during its preservation process (Yinjuan Cao et al., 2022). According to the Chinese standard of GB2707–2016, the acceptable TVB-N value for fresh meat was <15 mg/100 g. As Fig. 4D shows, the fresh meat in the DZ group transitioned to sub-fresh status on 16th day, with a TVB-N value of 17.29 ± 0.99 mg/100 g, whereas the meat in the coating groups became sub-fresh at 20th day, which is consistent with the observed pH values. This finding underscored the ability of biocoating to delay TVB-N accumulation. On 24th day, the TVBN values of the DZ, XZ, KG, KX, and KGX groups increased from 5.22 ± 0.49 mg/100 g to 33.09 ± 0.52, 30.52 ± 1.2, 27.98 ± 0.42, 26.34 ± 0.24, and 25.53 ± 0.51 mg/100 g, respectively. The TVB-N values in the KGX and KX groups were significantly lower compared to those in the other groups (p < 0.05), indicating that samples from these two groups accumulated less volatile basic nitrogen. This reduction may be attributed to the microbial growth inhibition provided by L. plantarum XZ-14. Hydrogels containing L. plantarum have been shown to inhibit the growth of spoilage microorganisms (Khodaei et al., 2019).

3.3.7 TVC value

The total viable count (TVC) of bacteria is pivotal for assessing meat safety and quality (Lee et al., 2023). Due to its rich nutritional content, fresh yak meat is highly susceptible to microbial contamination (Huang et al., 2022). Throughout the preservation process, all groups exhibited an increasing trend in TVC values (Fig. 4E). The TVC values on the 24th day for the DZ, XZ, KG, KX, and KGX groups increased by 140.02 ± 3.76%, 153.00 ± 5.15%, 141.06 ± 4.82%, 125.11 ± 3.34%, and 88.65 ± 2.90%, respectively. This finding helped to clarify the lower TVB-N values observed in the KGX group on 24th day. The TVC threshold of 7 log cfu/g was considered the upper acceptable limit for meat freshness (Yu Cao et al., 2019). By the 16th day, both the control (DZ) and other coating groups (XZ, KG, and KX) exceeded this threshold, while the KGX group (5.3 ± 0.1 log cfu/g) was significantly lower (p < 0.05) and dropped below this limit. It demonstrated superior efficacy in inhibiting microbial growth and reproduction, might due to the synergistic bactericidal action of GAL and L. plantarum on microorganisms in fresh yak meat (Yu Cao et al., 2019).

3.4 Microflora changes identified by high-throughput sequencing of microbes

3.4.1 Alpha and beta diversity analysis

The alpha and beta diversity analysis of bacteria and fungi in fresh yak meat is shown in Fig. 5. Alpha diversity analysis was utilized to assess the abundance and diversity of microbial communities across various samples. The abundance-based coverage estimator (Ace) indicates microbial richness, whereas the Shannon index indicates sample microbial diversity. As depicted in Fig. 5A & B, coverage indices exceeded 0.999 across all the samples, thus confirming sufficient sequencing depth to accurately reflect microbiome composition (Zhong et al., 2022). The decrease in the ACE (Fig. 5C & D) and Shannon indices (Fig. 5E & F) illustrated that the abundance and diversity of microorganisms in fresh meat decreased with increasing storage time, thus suggesting that a subset of bacteria and fungi became dominant in the samples after 20 days (Cha et al., 2023).Fig. 5 Diversity analysis of bacteria (A-G) and fungi (B-H). (A, B) Coverage index, (C, D) Abundance-based coverage estimator (ACE) index, (E, F) Shannon index, (G, H) Principal coordinate analysis (PCoA). Different letters represent significant differences within different groups (p < 0.05).

Fig. 5

Principal coordinate analysis (PCoA) was employed to investigate the similarities and differences in community structures among diverse microbial communities (Fig. 5G & H). The contribution rates of the main components of bacteria were 51.76% for PC1 and 27.43% for PC2, whereas the contribution rates of the main components of fungi were 56.75% for PC1 and 22.07% for PC2. The DZ0 group was distinctly separated from the other groups, thus indicating significant changes in the bacterial and fungal communities in yak meat samples after 20 days of preservation. Additionally, the independent distribution of the XZ20 group suggested unique alterations in bacterial communities within this group.

3.4.2 Bacterial and fungal community composition

The identification of the changes in the relative abundance of microbes during the preservation of yak meat can explain the process of yak meat decay, which is crucial for quality control and the development of preservation techniques for refrigerated yak meat (L. Wang et al., 2022). With respect to the preservation of fresh meat, attention has predominantly centered on bacterial changes, whereas research on fungal changes has been limited. However, when considering that nutrient-rich fresh meat not only facilitates bacterial proliferation but also encourages fungal growth, investigations of fungal dynamics during meat storage are also very important.

The structure of the bacterial and fungal communities in the different meat groups at various time points (0 and 20 days) was analyzed at the phylum and genus levels (Fig. 6). At the bacterial phylum level (Fig. 6A), five major phyla were detected in fresh beef, including Proteobacteria, Firmicutes, Actinobacteriota, Bacteroidota, and Cyanobacteria. However, after 20 days, Proteobacteria and Firmicutes were dominant. Proteobacteria, encompassing both aerobic and anaerobic bacteria, stands as the largest phylum within the bacterial kingdom, closely linked to meat decay. Its abundance significantly increased (except XZ20) after 20 days of preservation, from 38.39% (DZ0) to 70.86% (DZ20), 82.78% (KG20), 71.58% (KX20) and 49.69% (KGX20), thus indicating that the KGX group was more effective at inhibiting Proteobacteria. At the bacterial genus level (Fig. 6B), the proportion of Pseudomonas (3.58%) and Brochothrix (1.35%) in fresh yak meat (DZ0) was relatively low. However, the dominant genera in all the groups (except XZ20) were replaced by Pseudomonas and Brochothrix after 20 days. The inhibition of Pseudomonas growth is highly necessary for the preservation of meat (Castellano et al., 2017). The relative abundance of Pseudomonas increased substantially across all the groups from 3.58% (DZ0) to 68.6% (DZ20), 82.69% (KG20), 70.72% (KX20), and 45.97% (KGX20) after 20 days, thus indicating that the KGX group had superior preservation capabilities. Notably, the bacterial community composition differed significantly in the XZ20 group at both the phylum and genus levels. As shown in Fig. 6B, Lactobacillus emerged as the dominant genus, which is possibly attributable to the growth of L. plantarum added to the meat. Additionally, this suggested that KGM may form a thin film to provide a physical barrier for L. plantarum (Zhou et al., 2021).Fig. 6 Relative abundance of bacterial communities at the phylum (A) and genus (B) levels and fungal communities at the phylum (C) and genus (D) levels.

Fig. 6

The changes in fungal communities at the phylum and genus levels across different groups are illustrated in Fig. 6C & D. The dominant phyla of the fresh samples (ZD0) were Ascomycota (80%) and Basidiomycota (17.17%). After 20 days, the abundance of Ascomycota gradually increased from 80% (DZ0) to 99.67% (DZ20), 99.43% (XZ20), 99.84% (KG20), 99.11% (KX20) and 97.96% (KGX20). At the genus level (Fig. 6D), the dominant genera in fresh yak meat were Cladosporium (30.77%) and Candida (12.2%). After 20 days, Candida rapidly increased in all groups, increasing from 12.2% to 95.3% (DZ20), 65.8% (XZ20), 69% (KG20), 82.75% (KX20) and 64.98% (KGX20). Candida can be separated to a high degree from meat products, and it is an important fungus that can cause meat spoilage (Odeyemi et al., 2020). This result indicated that the KGX treatment markedly restrained the growth of Candida.

To identify significant biomarkers within various coating treatment groups, we conducted an analysis of the bacterial and fungal communities in fresh yak meat by utilizing LEfSe analysis, whereby we employed a linear discriminant analysis threshold of 2.0 (Fig. 7A&B). Within the bacterial community (Fig. 7A), a total of 37 bacterial species were identified as exhibiting significant differences among the four groups, encompassing 6 species at the genus level, such as Acinetobacter, Perlucidibaca, Psychrobacter, Lactobacillus, Pseudomonas, and Brochothrix. Specifically, the abundances of the genera Acinetobacter, Perlucidibaca, and Psychrobacter in the DZ0 group significantly diverged from those in the other groups, whereas the abundances of Lactobacillus in the XZ20 group and Pseudomonas in the KG20 group significantly differed from those in the other groups. Additionally, Brochothrix exhibited significant differences between the KGX20 group and the other groups. Moreover, within the fungal community (Fig. 7B), 14 species displayed significant differences in the DZ0, KG20, and KGX20 groups, with three species diverging at the genus level, including Cladosporium, Cutaneotrichosporon, and Kurtzmaniella.Fig. 7 Histograms of linear discriminant analysis effect size (LEfSe) and linear discriminant analyses (LDA > 2, p < 0.05) representing specific bacteria (A) and fungi (B) as phylogenetic and abundance different.

Fig. 7

4 Conclusion

Microbial hydrogel coatings combined with ice-temperature storage technology were used for the preservation of fresh yak meat. According to the pH, TVB-N, and TVC value, the control group exceeded the relevant standards (pH > 6.6, TVB-N ≥ 15 mg/100 g, TVC > 7 log cfu/g) on the 16th day, while the KGX group exceeded the relevant standards on the 20th day. Other indicators such as drip loss rate, color, texture, and TBARS value showed that the hydrogel coating can maintain color and texture, reduced drip loss, and inhibit fat oxidation in fresh yak meat. This indicated that the coating treatment had a good preservative effect and can effectively delay the spoilage process of fresh yak meat. Microbial diversity analysis demonstrated that the relative abundance of dominant spoilage microorganisms (Pseudomonas and Candida) was inhibited by KGX treatments. With the combined effect of the L. plantarum coating hydrogel and ice-temperature preservation, the shelf life of fresh yak meat can reach to 16–20 days. The KGX hydrogel coating effectively incorporated active ingredients (KGM, GAL, and L. plantarum) with potential biological activity, demonstrating outstanding preservation effects, particularly in inhibiting microbial growth, delaying fat oxidation, and reducing the drip loss in fresh yak meat. Future research should focus on elucidating the mechanisms of L. plantarum and phenolic compounds work synergistically on meat preservation to further understand the preservative function of composite hydrogels in fresh meat storage.

CRediT authorship contribution statement

Li-Shi Jiang: Writing – original draft, Methodology. Yun-Cheng Li: Writing – original draft, Supervision. Fu-Xu Zheng: Resources, Formal analysis. Meng-Jiao Zhang: Visualization, Validation. Wen-Xuan Zheng: Project administration, Data curation. Da-Yu Liu: Resources, Funding acquisition. Fan-Bing Meng: Writing – review & editing, Funding acquisition, Conceptualization.

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.

Data availability

Data will be made available on request.

Acknowledgments

This work was supported by Sichuan Science and Technology Program (2023YFN0014 ) and Science and Technology Program of Aba Tibetan and Qiang Autonomous Prefecture (S24YYJSYJ0097 ).
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