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The Changes Occurring in Proteins during Processing and Storage of Fermented Meat Products and Their Regulation by Lactic Acid Bacteria

College of Food Science and Engineering, Inner Mongolia Agricultural University, Hohhot 010018, China
Ministry of Agriculture and Rural Affairs Integrative Research Base of Beef and Lamb Processing Technology, Hohhot 010018, China
Department of Cooking & Food Processing, Inner Mongolia Business and Trade Vocational College, Hohhot 010070, China
Authors to whom correspondence should be addressed.
Foods 2022, 11(16), 2427;
Received: 1 July 2022 / Revised: 8 August 2022 / Accepted: 11 August 2022 / Published: 12 August 2022
(This article belongs to the Special Issue Meat Quality and Microbial Analysis)


Protein, which is the main component of meat, is degraded and oxidized during meat fermentation. During fermentation, macromolecular proteins are degraded into small peptides and free amino acids, and oxidation leads to amino acid side chain modification, molecular crosslinking polymerization, and peptide chain cleavage. At different metabolic levels, these reactions may affect the protein structure and the color, tenderness, flavor, and edible value of fermented meat products. Lactic acid bacteria are currently a research hotspot for application in the fermented meat industry. Its growth metabolism and derivative metabolites formed during the fermentation of meat products regulate protein degradation and oxidation to a certain extent and improve product quality. Therefore, this paper mainly reviews the changes occurring in proteins in fermented meat products and their effects on the quality of the products. Referring to studies on the effects of lactic acid bacteria on protein degradation and oxidation from all over the world, this review aims to provide a relevant reference for improving the quality of fermented meat products.

1. Introduction

Fermented meat products refer to meat products with a long shelf life, special flavor, texture, and color formed through fermentation of raw meat with the natural or artificial addition of microorganisms under specific temperature and humidity conditions [1]. Due to the differences in customs, raw materials, recipes, and manufacturing processes in different countries and regions, there are diverse products in the fermented meat products market [2], such as sausages that originate in the Mediterranean region and have spread to other countries such as Germany, the United States, and Hungary, which have created products with different characteristics due to the differences in each region’s own environment and processing methods [2,3]; the dry-cured hams of Jinhua and Xuanwei in China, Iberia and Serrano in Spain, Parma and San Daniele in Italy, and Bayonne in France all have strong regional characteristics [1,3]; in addition, there are also regional specialties such as salami, cured meat and sour fish in China, Thailand and India [1,4,5].
Protein, a molecularly large and structurally complex compound composed of amino acids, is a crucial dry matter component of meat. During fermentation, maturation, and storage of meat products, moderate protein degradation can effectively improve the flavor and nutritional value of fermented meat, but excessive protein oxidation can adversely affect meat quality such as texture, color, and flavor. In addition, oxidative induction of proteins may affect their digestive utilization, reduce the content of essential amino acids, reduce the nutritional value of meat products, and even cause product spoilage and deterioration, thereby severely affecting the safety of the product for consumption [6,7]. Therefore, we need to determine the optimal degree of protein changes to prevent excessive protein oxidation, thus maximizing the quality and nutritional value of fermented meat products through protein changes.
Lactic acid bacteria (LAB) are dominant bacteria in meat product fermentation. During fermentation, dynamic changes in the flora and the metabolites produced affect the flora structure in the product, act on each meat component, and have a certain impact on the flavor and other product indicators [8,9]. The effect of LAB on the quality of meat products has attracted considerable research attention. Although the research on lactic acid bacteria has developed in recent years, there is still a lack of review on how lactic acid bacteria affect the changes occurring in proteins of fermented meat and further improve the quality of products [10,11,12,13,14]. Therefore, this paper reviews the changes and influence on protein in fermented meat products, the regulation of protein degradation and oxidation by LAB, and its effect on the quality of fermented meat products, aiming to provide a relevant reference for the use of LAB for regulating the moderate change of protein in fermented meat.

2. Protein Changes in Fermented Meat Products

2.1. Protein Degradation

Protein degradation is among the most crucial biochemical phenomena that occurs during fermentation and maturation of meat products. Degradation of proteins in these fermented meat products is mainly influenced by endogenous enzymes in muscle tissue and proteases produced by microorganisms involved in fermentation. The endogenous proteases can be classified as endopeptidases and exopeptidases. Endopeptidases mainly include cathepsin B, cathepsin L, cathepsin D, and calpain, and exopeptidases mainly include aminopeptidases and carboxypeptidases [15]. Sarcoplasmic protein and myofibrillar protein (MP) were mainly decomposed into polypeptides by endogenous proteases such as cathepsin B and cathepsin L at the early fermentation stage. The polypeptides were further decomposed into small peptides, free amino acids, aldehydes, organic acids, and amines by endogenous aminopeptidases, microbial proteases, and microbial metabolites, which lead to changes in physical and chemical criterion [16]. This is reflected in both fermented sausages and hams; in the early stages of sausage fermentation, although lactic acid produced by microbial metabolism such as LAB decreases the pH of the product, the alkaline metabolites accumulated by protein degradation in the later stages may act as a buffer against organic acids and cause a rebound in the pH of the product [17,18]; in the production of hams, the pH of dry-cured ham was found higher after ageing due to massive release of low-weight nitrogen molecules and ammonia formation ascribed to endogenous and exogenous proteolytic, deaminase and deamidase activities [19].
The protein hydrolysis index, total volatile base nitrogen, and free amino acid content of meat significantly increased during fermentation [20]. The trial of Yu et al. [21] verified that degradation of large molecules of myogenic fibronectin and myosin in fermented sausage results in an increase in the concentration of small molecule peptides. As shown in Table 1, antioxidant peptides in sausage and ham are mainly derived from myosin and actin hydrolysis [22]. Myosin, actin, myoglobin, troponin, and pyruvate kinase are generally the main proteins affecting differential peptides [23]. Using dry cured ham, Li et al. [24] identified 66 peptides from myosin, β-enolase, and actin with antioxidant, angiotensin-converting enzyme, and platelet-activating factor-acetylhydrolase inhibitory activities and found that peptides of <3 kDa were most effective. By measuring dry cured ham at different stages of storage, Virgili et al. [19] verified that free amino acids are released from the ham, biogenic amines are produced as storage time increases and protein degradation continues, and tyramine and putrescine formed due to the conversion of arginine to ornithine were the most abundant at 23 months of storage.
Thus, during the maturation of fermented meat products, large molecule proteins tend to be degraded into small molecule substances; however, excessive degradation can lead to the production of non-healthy factors such as biogenic amines.

2.2. Protein Oxidation

Although protein oxidation is similar to lipid oxidation because it is also a chain reaction consisting of initiation, transmission, and termination caused by free radicals [25], the targets and pathways of protein oxidation are more complex and are closely related to the types and properties of oxidation products [26]. Protein oxidation refers to covalent modification of proteins directly induced by active substances such as reactive oxygen species (ROS) and reactive nitrogen species (RNS) or indirectly by secondary products of oxidative stress such as lipids and carbohydrate oxides. The ROS can result in the oxidation of amino acid side chains and protein skeleton, leading to protein fragmentation or protein–protein crosslinking [27]. Among them, the ROS generation system is mainly affected by the radiation, irradiation, and lipid oxidation system; myoglobin-mediated oxidation system; and metal catalytic oxidation system [28].
The possible mechanisms of protein oxidation in fermented meat products are shown in Figure 1. The blue color represents the protein oxidation mechanism catalyzed by metal ions: in stage 1, the hydrogen atom in protein (PH) is deprived of ROS such as a hydroxyl radical (OH·), thereby generating a carbon-centered protein free radical (P·); in stage 2, the protein free radical (P) is oxidized to alkyl free radical (POO·) under the condition of O2 [29]; a cross-linked derivative (P-P) was generated by carbon-carbon bonding (C-C) with another protein free radical (P·) without O2; in stage 3, an alkyl radical (POO·) generates alkyl peroxide (POOH) by seizing the hydrogen atom in another protein, participating in the redox reaction of transition metal ions (Mn+ such as Fe2+ or Cu+), or reacting with a protonated superoxide radical; and then, in stages 4 and 5, alkyl peroxides (POOH) react with ROS such as HO2· radical or with reduced forms of transition metal ions (Mn+) to form alkane oxidation radicals (PO·), respectively. Further, hydroxyl derivatives (POH) are generated in stages 6 and 7. In addition, alkyl peroxide (POOH) and hydroxyl derivative (POH) can break the peptide chain through α-amidation or the diamide pathway to produce related derivatives [30]. The green color is the speculated mechanism of lipid peroxidation-induced protein oxidation. Similar to protein oxidation catalyzed by metal ions, lipids generate free radicals through the initiation and transmission of oxidation to seize hydrogen atoms in proteins, and then form polymers or protein–lipid complexes through several reaction stages of hydrogen extraction, extension, recombination, and polymerization.
Park et al. [31] compared the sensitivity of common amino acids in meat to the oxidation reactions of different catalytic systems, and confirmed that the amount of essential amino acids such as cysteine, methionine, and tyrosine significantly reduced in metal ion-catalyzed oxidation. This is mainly due to the generation of carbonyl derivatives of these amino acid side chains and the loss of sulfhydryl groups; therefore, experimental studies often use the carbonyl and sulfhydryl content as a measure of the degree of protein oxidation.

2.3. Effects of Protein Changes

2.3.1. Effects on Protein Structure

Myofibrillar protein is the main protein in meat, accounting for 55–60% of the total and is mainly composed of myosin, actin, and other regulatory proteins. Many myofibrils form muscle fibers and further connect through the connective tissue to form muscles [32]. Both protein degradation and oxidation during fermentation and maturation change the natural structure of proteins and consequently their properties.
Changes in the protein secondary structure are observed using Fourier transform infrared spectroscopy, circular dichroism spectroscopy, and Raman spectroscopy; UV absorption spectroscopy or endogenous fluorescence spectroscopy are used to detect the tertiary structure of proteins. The relaxation time and proportion of different water are observed through NMR spectroscopy. Thus, we can speculate that changes occur in protein during the production of fermented meat products.
Through Raman spectroscopy, some scholars analyzed that oxidation expands the protein structure in meat and transforms α-helix into β-sheet, β-turn, and random coil [33]. The increase in the hydrophobicity of a protein surface indicates that oxidation exposes hydrophobic amino acids. The change in the spectral wavelength can be used to modify, expose, or cover the oxidation of aromatic amino acid residues, and finally reveal the changes in secondary and tertiary structures of proteins [34]. Lipid oxidation-induced protein oxidation affects the structure and functional properties of protein gels through the expansion and crosslinking of MP. Moderate MP oxidation leads to protein crosslinking through disulfide bonds to maintain a good water-holding capacity of gels. However, excessive exposure of hydrophobic residues and formation of protein polymers during excessive MP oxidation hinder the water-holding capacity of gels [35].
Thus, we can consider that a protein’s structure is directly related to the texture of fermented meat products, and ultimately reflects the hardness, chewing type, elasticity, and tenderness of the products. In addition, the protein structure determines the degree of binding to flavor compounds, especially the number of hydrophobic binding sites on the surface of the protein. Thus, structural changes caused by protein degradation and oxidation affect product quality to some extent.

2.3.2. Impact on Product Quality

The effects of protein changes on fermented meat products are often directly reflected through the color, tenderness, flavor, and edible quality of products. As shown in Figure 2, different levels of the changes occurring in proteins have positive or negative effects on quality.
(1) Color gives the first impression about a product to consumers. According to previous studies, 80–90% of the stability of meat color is determined by the content and chemical state of myoglobin [36]. As shown in Figure 2, myoglobin, which gives the meat its purplish red color, can be oxygenated to form bright red oxygenated myoglobin, while these two myoglobins are oxidized to form brown high-iron myoglobin under an anaerobic condition. Excessive accumulation of high-iron myoglobin in fermented meat products during maturation deteriorates meat color. However, high-iron myoglobin can be reduced with reductase to maintain the stability of meat color [37]. Thus, enzymes related to redox regulation of sarcoplasmic proteins are also closely related to meat color [38].
Moreover, light scattering has a certain influence on meat color, especially meat brightness [38]. By studying dry cured ham, some scholars have speculated that protein degradation and oxidation affect the muscle tissue microstructure and change the distance between muscle filaments, thereby affecting the absorption, transmission, and scattering of light by the muscle and thus changing the color of meat [39,40]. In summary, changes in myoglobin content and state, reductase activity, and muscle structure are critical factors affecting the color of the meat product.
(2) Tenderness, as a crucial index for evaluating meat grade, is determined by many factors. In general, the type of muscle, integrity of muscle fiber, and activity of endogenous enzymes in muscle are all related to muscle tenderness [41]. As shown in Figure 2, protein degradation affects meat tenderness by degrading numerous MPs in muscle tissue [42]. In addition, ROS-induced protein oxidation may damage the MPs and activate the proteasome, thereby promoting the degradation of structural proteins in muscle and improving meat tenderness [43].
However, some researchers have pointed out that over-oxidation of proteins also adversely affects tenderness. Strong oxidation often leads to the formation of cross-linked MPs, loss of thiol groups, and formation of Schiff bases and disulfide bonds, and thus, the activity of calpain is reduced [44]. These cross-linking compounds also increase the distance between muscle fibers, and the non-flowable water in myofibrils is transformed into free water that can be easily lost, thereby reducing the water-holding capacity of meat [45], and resulting in increased hardness of meat and decreased tenderness [7,46].
Based on proteomics, Zhu et al. [47] found that tenderness is closely related to muscle structure, energy metabolism, heat shock protein, oxidative stress response, and apoptosis-related pathways. Thus, moderate protein degradation can improve meat tenderness, whereas excessive oxidation can reduce it.
(3) Lipid hydrolysis and oxidation are generally believed to be the main methods of producing volatile flavor compounds. However, as shown in Figure 3, protein degradation also has a major impact on flavor changes.
Protein degradation produces free amino acids as a taste substance. In ham, taste amino acids such as glutamic acid and aspartic acid are directly positively correlated with the product’s taste. Alanine is related to sweetness, lysine is related to a mature taste, and tryptophan is related to a salty taste. Phenylalanine and isoleucine contribute to an acidic taste. Tyrosine and histidine have very low taste thresholds, which may also affect the flavor of ham [39,50]. Microbial transaminases can convert free amino acids into α-keto acids, which can be directly or indirectly metabolized into corresponding aldehydes as intermediates. Aldehydes are converted to corresponding alcohols and acids by alcohol dehydrogenase and aldehyde dehydrogenase, respectively. Microorganisms are also an indispensable part of flavor substance production by amino acids. In the presence of bacteria such as LAB and Staphylococcus, branched-chain amino acids are converted into corresponding methyl branched-chain compounds such as 2-methylbutyraldehyde, 2-methylpropanal, 3-methylbutyraldehyde, and benzaldehyde, contributing to the malt, fruit, and sweet tastes of the product [14,51]. Estévez et al. [52] reported the formation of Strecker aldehyde from leucine and isoleucine through α-amino aliphatic semialdehyde and γ-glutamic acid semialdehyde. Thus, carbonyl derivatives were believed to be involved as precursors in the degradation of Strecker aldehyde to produce volatile flavor compounds.
On the other hand, although protein itself is tasteless, some researchers believe that it can contribute to product flavor by binding with flavor compounds [53]. Studies have shown that the interaction between proteins and flavor substances depends on physical binding, chemical interaction, and mass transfer effects. For example, hydrogen bonds and van der Waals forces are the key driving forces for the interaction between myosin and ethyl octanoate [54], and hydrophobic forces are also crucial for maintaining the interaction between protein and flavor substances [55]. Notably, ketone and aldehyde are more difficult to bind to the MP gel with an increase in the carbon chain length. By contrast, in the protein solution system, the ability of flavor compounds to bind to proteins increases with an increase in the carbon chain length, which may be because the gel structure hinders the mass transfer of flavor compounds and affects their release [56].
However, excessive protein degradation leads to excessive accumulation of bitter amino acids and peptides such as hypoxanthine, conferring bitterness and rancidity to the products [48]. Excessive oxidation of proteins leads to changes in protein conformation, reduces the hydrophobicity of the protein surface, and reduces the binding sites between proteins and flavor compounds, thereby affecting the ability of proteins to bind flavor compounds [55]. Moderate protein degradation and oxidation enrich the products’ flavor through the Strecker degradation reaction, but excessive protein changes can lead to flavor deterioration.
(4) The edible quality of products, especially safety, is a major concern for consumers. As shown in Figure 2, moderate protein degradation can improve the edible quality of products, but excessive protein oxidation poses a threat to the quality, digestibility, and even, safety of products. Oxidation of meat protein leads to the oxidative modification of amino acid side chain groups, reduction of essential amino acids, and generation of irreversible carbonyl compounds, which thereby reduce the edible value of meat [57]. Ma et al. [58] proposed that during the processing of air-dried yak meat, the digestibility of MPs decreases with an increase in protein oxidation, which may be because the over-oxidation modification of proteins hinders protein hydrolysis, weakens the binding of proteolytic enzymes to proteins, affects the sensitivity of proteins to pepsin, and reduces protein digestibility [59]. Moreover, excessive protein oxidation can directly lead to meat corruption and the formation of derivatives (such as furans, biogenic amines, acrylamide, and nitrosamines), thus causing food safety problems [60].
Therefore, to ensure the quality of fermented meat products and to improve this quality, the degree of protein changes must be adequately controlled. At present, the degree of protein degradation or oxidation is regulated by adding NaCl, auxiliary additives, and fermenting agents and by controlling the production temperature.

3. Regulatory Role of LAB

As organisms generally recognized as safe, LAB have become the most widely used probiotics in food production. Currently, Lactobacillus lactis, Lactobacillus plantarum, Pediococcus lactis, and Pediococcus pentosaceus and so on are widely used in fermented meat products [61,62]. They regulate the degradation or oxidation of protein mainly through acid and protease production, and their antioxidant capacity.

3.1. Acid Production

Endogenous enzymes play a major role in protein degradation during meat product fermentation; however, LAB contribute to the degradation of muscle protein and the release of small peptides and amino acids through metabolic acid production. Studies have shown that some endopeptidases, such as cathepsin, exhibit higher activity at low pH, and increasing pH inhibits cathepsin B activity to a certain extent [63,64]. By comparing fermented sausages under the two acidification curves, Berard et al. found that the number of actin-derived peptides identified at low pH increased from 42 to 144, which was 88 more than that identified at high pH. Most of these derivatives were released at the cleavage sites of cathepsin B and cathepsin D. This shows that cathepsin can degrade proteins to produce more peptides under acidic conditions [65].
The LAB can produce organic acids such as lactic acid through carbohydrate metabolism in fermented meat, resulting in a decrease in environmental pH [66]. Therefore, the acid production capacity is often used as one of the criteria for measuring the suitability of a LAB starter culture. Fermented sausages experience a decline in the pH value at the beginning of fermentation. The pH decline added with a LAB starter is more obvious, which thus provides a better environment for protease activity. At the late stage of fermentation, the pH of sausages show a certain rebound, which is mainly due to protein degradation by protease and the production of peptides, amino acids, amines, and organic acids [62]. By analyzing a protein degradation model at pH 4.0, Fadda et al. [67] found that the degradation under acidic conditions was affected by the synergistic effect of acid-induced changes by acidic endogenous protease, protease hydrolysis activity of L. plantarum CRL 681, and fermentation metabolism. Therefore, LAB can be speculated to assist in the initial degradation of proteins by producing acid and reducing pH to improve cathepsin activity [68]. In addition, the metabolism and acid production of LAB will affect the structure of other microorganisms, thus inhibiting the growth of spoilage bacteria, and reducing the impact of spoilage bacteria metabolism [69].

3.2. Protease Production

Protein degradation is mainly affected by endogenous protease, but LAB-secreted protease during fermentation can also increase the concentration of free amino acids and short peptides by affecting the degradation of sarcoplasmic proteins [70].
Compared with dairy products, the research and application of lactobacillus protease in fermented meat are less. On screening LAB isolated from fermented sausages, Cao et al. [10] obtained seven strains with good fermentation performance and high protease activity, and identified one strain as L. pentosus, one strain as L. fermentum, and the others as L. plantarum. Through SDS-PAGE and molecular docking, Sun et al. verified that proteases purified from P. pentosaceus R1 [71], L. brevis R4 [72], L. curvatus R5 [73], and L. fermentum R6 [74,75] isolated from Harbin dry sausage can catabolize sarcoplasmic proteins and myogenic fibrous proteins, and interact with the myosin light chain, myosin heavy chain, and actin and myoglobin in meat. They also predicted that protease consists of a β-strand and an α-helix, the properties of protease are altered by changes in a tandem conserved structural domain consisting of a protease structural domain and a PDZ structural domain, and the active site of protease is related to protease properties and substrate specificity [71]. This demonstrates the potential of protease-producing LAB to influence proteolysis as a meat fermenter.
In addition, Cao et al. [10] inoculated LAB with high protease activity into fermented sausage and identified the metabolites of sausage protein through LC-MS/MS. Lactobacillus plantarum CD101 could help to produce more peptides and small peptides, and the content of antioxidant peptides also significantly increased, indicating that LAB has a certain application prospect as a meat fermentation starter.

3.3. Antioxidant Properties

The LAB are considered a natural antioxidant, as shown in Figure 4. At present, the antioxidant properties of LAB are believed to be jointly regulated through multiple mechanisms such as regulation of the redox system, production of antioxidant metabolites, scavenging of free radicals, and chelation of metal ions [12].
First, transition metal ions inhibit the enzyme-catalyzed phosphate substitution reaction and produce related ROS by decomposing hydrogen peroxide. The cell-free extract of LAB cells exhibited a good chelating ability of Fe2+ and Cu+. Therefore, LAB cells are speculated to contain related metal ion-chelating agents and their high antioxidant activity is positively correlated [76,77].
Second, several studies have shown that the intracellular antioxidant activity of LAB is based on the activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), nicotinamide adenine dinucleotide (NADH) oxidase, NADH-peroxidase, and glutathione (GSH) [78,79,80]. Thus, antioxidant enzymes play an indispensable role in the high antioxidant properties of LAB. The SOD regulates the ROS level by catalyzing superoxide decomposition [81], while CAT and GPx decompose H2O2 formed by SOD-mediated superoxide anion radical scavenging into water and oxygen, thereby preventing the formation of the hydroxyl radical (·OH). Regulation of some ROS-producing enzymes can also play an antioxidant role [82]. The NADH oxidase produces H2O2 that causes NADH peroxidase to remove H2O2 [80]. The thioredoxin–thioredoxin reductase system (Trxs) and glutathione–glutathioredoxin system (GSHs) in LAB cells can regulate intracellular disulfide/disulfide, thus helping to maintain redox homeostasis [83]. Under the premise of hydrogen supply by NADPH oxidase, TrxR converts oxidized Trx into reduced Trx, GR converts oxidized GSH into reduced GSH, and GSH activates GPx activity to remove lipid peroxides and H2O2 [84].
Furthermore, LAB can produce various metabolites with antioxidant activities, such as cell wall polysaccharides, peptidases, lipid acids, and protein derivatives [85,86]. Exopolysaccharide is a type of polysaccharide produced by LAB during metabolism that adheres to the surface of bacteria and binds to cells [87]. Lactobacillus plantarum AAS3 screened from fermented dried fish can scavenge DPPH free radicals and hydroxyl free radicals through metabolism to produce extracellular polysaccharide, thus reflecting a good in vitro antioxidant capacity [88]. Fatty acids such as palmitic acid and stearic acid are considered indirect antioxidants. In saturated fatty acids, the antioxidant activity increases with an increase in chain length, while unsaturated fatty acids are mainly oxidized in an unsaturated-dependent manner [85]. Some amino acid derivatives such as N-(5-amino-2-hydroxy-1-oxopentyl)-tyrosine, (S)-8-hydroxy-4-hydroxy-phenylpropionic acid, (S)-8-hydroxy-phenylpropionic acid, and indole-3-(S)-3-lactic acid can scavenge DPPH free radicals, which proves the antioxidant activity of metabolites of LAB [89].
In addition, in the face of oxidative stress, through proteomics, some researchers analyzed that LAB can inhibit biochemical processes related to the ribosome structure, transcription, translation, and protein synthesis through the oxidation defense system, oxidation protein repair system, ABC transporter system, and the expression of proteins involved in carbohydrate energy metabolism, and carry out antioxidant stress reactions [90].
Mei et al. [11] added L. plantarum P3 with antioxidant properties to fermented sausage, and detected the thiobarbituric acid value, carbonyl content, thiol content and other indicators. The P3 could inhibit the activity of lipoxygenase and prevent adverse consequences caused by lipid peroxidation by reducing lipid oxidation through its antioxidant properties and chelating with ferrous ions, which verified the slowing effect of P3 on protein oxidation of sausage. Scavenging free radicals, chelating metal ions, and preventing lipid peroxidation are the ways through which LAB with antioxidant function reduce protein oxidation and improve the quality of fermented meat.

3.4. Effect on Quality

People currently want to develop more green, safe, healthy, and delicious functional foods. The safety of fermented meat products is the focus of consumers. As a key factor leading to spoilage and deterioration of products, LAB can compete with other microorganisms for nutritional substrates in fermented meat products and metabolize them to produce lactic acid, acetic acid, hydrogen peroxide, antimicrobial peptides, and other compounds. These compounds can destroy the stability of biofilms of spoilage bacteria through coordination, interfere with the proton gradient of spoilage bacteria, passivate the enzyme activity of spoilage bacteria and generate ROS after entering cells, inhibit the growth and metabolism of spoilage bacteria, and improve product safety [69]. They can also reduce the residual amount of nitrite through acid degradation or enzyme degradation and reduce the potential harm caused by nitrite [91]. At the same time, LAB can improve the color by increasing the brightness value of the product [13]. Some special strains can convert myoglobin and high-iron myoglobin (Met-Mb) to red nitro myoglobin (Mb-NO), with the potential of natural biological colorants [92]. LAB-produced enzymes can promote the decomposition of protein lipids, which is closely related to the production of esters, aldehydes, and ketones [8,14].
Moreover, LAB can maintain intestinal stability, coordinate digestion, regulate cholesterol content [93], and regulate Nrf2-Keap1-ARE [94], NFκB [95], and MAPK [96] signaling pathways through antioxidant characteristics to alleviate oxidative stress, improve inflammation, reduce toxins, and alleviate injury.
Therefore, based on the functional characteristics of metabolic acid production and protease production, and antioxidant properties, LAB can be used as a starter culture for regulating the degree of protein changes in fermented meat products, ensuring the quality of the products, and further assisting in the development of green and healthy products.

4. Summary

Protein changes occur through the whole process of fermentation, ripening, and storage of fermented meat products. In this paper, the mechanism of protein degradation and oxidation, its effect on the quality of fermented meat products, and the regulation of protein degradation and oxidation by LAB are described in detail. The use of LAB as a starter culture for meat fermentation can not only improve sensory qualities such as color, tenderness, and flavor of fermented meat products but also affect the degree of protein degradation and oxidation in the products through acid production and protease production, and antioxidant properties. However, few studies have currently investigated whether the addition of LAB can affect the protein structure and improve the binding ability of proteins to various flavor substances. Therefore, studies on LAB starters are warranted.
With the advancement of omics technology and computer simulation software, in the future, we can use multi-omics technology combined with molecular docking and other models to clarify the dynamic process of the changes occurring in proteins of fermented meat, determine the key differential metabolites of proteins that affect product quality, and identify how to maintain the best quality of products. The effects of LAB or their interactions with other influencing factors on each component in fermented meat were clarified to optimize the LAB starter, explore the improvement mechanism of strain compounding on fermented meat products, and develop more high-quality fermented meat products.

Author Contributions

Conceptualization, D.W.; writing—original draft preparation, D.W.; writing—review and editing, D.W., F.C., Y.W., J.H., F.G., J.T., K.Z.; project administration, J.T., K.Z., Y.J.; funding acquisition, J.T., Y.J. All authors have read and agreed to the published version of the manuscript.


This review was funded by National Natural Science Foundation of China (31960514 and 32160589), Science and Technology Projects of Inner Mongolia Autonomous Region (2019GG239), Transformation project of scientific and technological achievements in Inner Mongolia Autonomous Region (2019CG066) and Inner Mongolia Natural Science Foundation Project (2021MS03090).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest or relationship.


  1. Wang, Z.L.; Wang, Z.X.; Ji, L.L.; Zhang, J.M.; Zhao, Z.P.; Zhang, R.; Bai, T.; Hou, B.; Zhang, Y.; Liu, D.Y.; et al. A review: Microbial diversity and function of fermented meat products in China. Front. Microbiol. 2021, 12, 645435. [Google Scholar] [CrossRef] [PubMed]
  2. Talon, R.; Leroy, S.; Lebert, I. Microbial ecosystems of traditional fermented meat products: The importance of indigenous starters. Meat Sci. 2007, 77, 55–62. [Google Scholar] [CrossRef] [PubMed]
  3. Halagarda, M.; Wójciak, K.M. Health and safety aspects of traditional European meat products. A review. Meat Sci. 2022, 184, 108623. [Google Scholar] [CrossRef] [PubMed]
  4. Aarti, C.; Khusro, A.; Varghese, R.; Arasu, M.V.; Agastian, P.; Al-Dhabi, N.A.; Ilavenil, S.; Choi, K.C. In vitro studies on probiotic and antioxidant properties of Lactobacillus brevis strain LAP2 isolated from Hentak, a fermented fish product of North-East India. LWT-Food Sci. Technol. 2017, 86, 438–446. [Google Scholar] [CrossRef]
  5. Pringsulaka, O.; Thongngam, N.; Suwannasai, N.; Atthakor, W.; Pothivejkul, K.; Rangsiruji, A. Partial characterisation of bacteriocins produced by lactic acid bacteria isolated from Thai fermented meat and fish products. Food Control 2012, 23, 547–551. [Google Scholar] [CrossRef]
  6. Soladoye, O.P.; Juárez, M.L.; Aalhus, J.L.; Shand, P.; Estévez, M. Protein oxidation in processed meat: Mechanisms and potential implications on human health. Compr. Rev. Food Sci. Food Saf. 2015, 14, 106–122. [Google Scholar] [CrossRef]
  7. Berardo, A.; Claeys, E.; Vossen, E.; Leroy, F.; De Smet, S. Protein oxidation affects proteolysis in a meat model system. Meat Sci. 2015, 106, 78–84. [Google Scholar] [CrossRef]
  8. Ying, H.Y.; Lang, Z.; Qian, L.; Yan, W.; Qian, C.; Hua, K.B. The potential correlation between bacterial diversity and the characteristic volatile flavour of traditional dry sausages from Northeast China. Food Microbiol. 2020, 91, 103505. [Google Scholar] [CrossRef]
  9. Zhang, Y.; Qin, Y.X.; Wang, Y.; Huang, Y.X.; Li, P.F.; Li, P.L. Lactobacillus plantarum LPL-1, a bacteriocin producing strain, changed the bacterial community composition and improved the safety of low-salt fermented sausages. LWT-Food Sci. Technol. 2020, 128, 109385. [Google Scholar] [CrossRef]
  10. Cao, C.C.; Feng, M.Q.; Sun, J.; Xu, X.L.; Zhou, G.H. Screening of lactic acid bacteria with high protease activity from fermented sausages and antioxidant activity assessment of its fermented sausages. CyTA-J. Food 2019, 17, 347–354. [Google Scholar] [CrossRef]
  11. Mei, L.; Pan, D.M.; Guo, T.T.; Ren, H.J.; Wang, L. Role of Lactobacillus plantarum with antioxidation properties on Chinese sausages. LWT-Food Sci. Technol. 2022, 162, 113427. [Google Scholar] [CrossRef]
  12. Feng, T.; Wang, J. Oxidative stress tolerance and antioxidant capacity of lactic acid bacteria as probiotic: A systematic review. Gut Microbes 2020, 12, 1801944. [Google Scholar] [CrossRef] [PubMed]
  13. Hu, Y.Y.; Li, Y.J.; Li, X.-a.; Zhang, H.W.; Chen, Q.; Kong, B.H. Application of lactic acid bacteria for improving the quality of reduced-salt dry fermented sausage: Texture, color, and flavor profiles. LWT-Food Sci. Technol. 2022, 154, 112723. [Google Scholar] [CrossRef]
  14. Chen, Q.; Kong, B.H.; Han, Q.; Xia, X.F.; Xu, L. The role of bacterial fermentation in lipolysis and lipid oxidation in Harbin dry sausages and its flavour development. LWT-Food Sci. Technol. 2017, 77, 389–396. [Google Scholar] [CrossRef]
  15. Zhou, C.Y.; Pan, D.D.; Cao, J.X.; Zhou, G.H. A comprehensive review on molecular mechanism of defective dry-cured ham with excessive pastiness, adhesiveness, and bitterness by proteomics insights. Compr. Rev. Food Sci. Food Saf. 2021, 20, 3838–3857. [Google Scholar] [CrossRef]
  16. Dalmis, U.; Soyer, A. Effect of processing methods and starter culture (Staphylococcus xylosus and Pediococcus pentosaceus) on proteolytic changes in Turkish sausages (sucuk) during ripening and storage. Meat Sci. 2008, 80, 345–354. [Google Scholar] [CrossRef]
  17. Ruiz-Moyano, S.; Martín, A.; Benito, M.J.; Hernández, A.; Casquete, R.; de Guia Córdoba, M. Application of Lactobacillus fermentum HL57 and Pediococcus acidilactici SP979 as potential probiotics in the manufacture of traditional Iberian dry-fermented sausages. Food Microbiol. 2011, 28, 839–847. [Google Scholar] [CrossRef]
  18. Ikonić, P.; Tasić, T.; Petrović, L.; Škaljac, S.; Jokanović, M.; Mandić, A.; Ikonić, B. Proteolysis and biogenic amines formation during the ripening of Petrovská klobása, traditional dry-fermented sausage from Northern Serbia. Food Control 2013, 30, 69–75. [Google Scholar] [CrossRef]
  19. Virgili, R.; Saccani, G.; Gabba, L.; Tanzi, E.; Bordini, C.S. Changes of free amino acids and biogenic amines during extended ageing of Italian dry-cured ham. LWT-Food Sci. Technol. 2007, 40, 871–878. [Google Scholar] [CrossRef]
  20. Wang, D.B.; Hu, G.H.; Wang, H.T.; Wang, L.M.; Zhang, Y.H.; Zou, Y.F.; Zhao, L.H.; Liu, F.; Jin, Y. Effect of mixed starters on proteolysis and formation of biogenic amines in dry fermented mutton sausages. Foods 2021, 10, 2939. [Google Scholar] [CrossRef]
  21. Yu, D.; Feng, M.Q.; Sun, J. Influence of mixed starters on the degradation of proteins and the formation of peptides with antioxidant activities in dry fermented sausages. Food Control 2021, 123, 107743. [Google Scholar] [CrossRef]
  22. Luan, X.X.; Feng, M.Q.; Sun, J. Effect of Lactobacillus plantarum on antioxidant activity in fermented sausage. Food Res. Int. 2021, 144, 110351. [Google Scholar] [CrossRef] [PubMed]
  23. Wang, J.Y.; Guo, M.T.; Wang, Q.L.; Dong, J.; Lu, S.L.; Lyu, B.; Ma, X.L. Antioxidant activities of peptides derived from mutton ham, Xuanwei ham and Jinhua ham. Food Res. Int. 2021, 142, 110195. [Google Scholar] [CrossRef] [PubMed]
  24. Li, H.Y.; Wu, J.P.; Wan, J.; Zhou, Y.; Zhu, Q.J. Extraction and identification of bioactive peptides from Panxian dry-cured ham with multifunctional activities. LWT-Food Sci. Technol. 2022, 160, 113326. [Google Scholar] [CrossRef]
  25. Estévez, M. Protein carbonyls in meat systems: A review. Meat Sci. 2011, 89, 259–279. [Google Scholar] [CrossRef]
  26. Davies, M.J. The oxidative environment and protein damage. BBA-Proteins Proteom. 2005, 1703, 93–109. [Google Scholar] [CrossRef]
  27. Zhang, W.G.; Xiao, S.; Ahn, D.U. Protein oxidation: Basic principles and implications for meat quality. Crit. Rev. Food Sci. Nutr. 2013, 53, 1191–1201. [Google Scholar] [CrossRef]
  28. Wang, Z.M.; Zhou, H.; Zhou, K.; Tu, J.; Xu, B.C. An underlying softening mechanism in pale, soft and exudative—Like rabbit meat: The role of reactive oxygen species—Generating systems. Food Res. Int. 2022, 151, 110853. [Google Scholar] [CrossRef]
  29. Davies, M.J. Protein oxidation and peroxidation. Biochem. J. 2016, 473, 805–825. [Google Scholar] [CrossRef]
  30. Stadtman, E.R.; Levine, R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 2003, 25, 207–218. [Google Scholar] [CrossRef]
  31. Park, D.; Xiong, Y.L. Oxidative modification of amino acids in porcine myofibrillar protein isolates exposed to three oxidizing systems. Food Chem. 2007, 103, 607–616. [Google Scholar] [CrossRef]
  32. Lv, C.Y.; Xu, C.; Gan, J.; Jiang, Z.H.; Wang, Y.M.; Cao, X.L. Roles of proteins/enzymes from animal sources in food quality and function. Foods 2021, 10, 1988. [Google Scholar] [CrossRef] [PubMed]
  33. Sun, Y.Y.; Luo, H.L.; Cao, J.X.; Pan, D.D. Structural characteristics of Sheldrake meat and secondary structure of myofibrillar protein: Effects of oxidation. Int. J. Food Prop. 2017, 20, 1553–1566. [Google Scholar] [CrossRef]
  34. Zhang, D.; Li, H.J.; Emara, A.M.; Hu, Y.; Wang, Z.F.; Wang, M.Q.; He, Z.F. Effect of in vitro oxidation on the water retention mechanism of myofibrillar proteins gel from pork muscles. Food Chem. 2020, 315, 126226. [Google Scholar] [CrossRef] [PubMed]
  35. Jiang, Y.; Li, D.H.; Tu, J.C.; Zhong, Y.J.; Zhang, D.; Wang, Z.M.; Tao, X.Q. Mechanisms of change in gel water-holding capacity of myofibrillar proteins affected by lipid oxidation: The role of protein unfolding and cross-linking. Food Chem. 2021, 344, 128587. [Google Scholar] [CrossRef] [PubMed]
  36. Yu, Q.P.; Feng, D.Y.; Xiao, J.; Wu, F.; He, X.J.; Xia, M.H.; Dong, T.; Liu, Y.H.; Tan, H.Z.; Zou, S.G.; et al. Studies on meat color, myoglobin content, enzyme activities, and genes associated with oxidative potential of pigs slaughtered at different growth stages. Asian-Australas. J. Anim. Sci. 2017, 30, 1739–1750. [Google Scholar] [CrossRef]
  37. Mitacek, R.M.; Ke, Y.L.; Prenni, J.E.; Jadeja, R.; VanOverbeke, D.L.; Mafi, G.G.; Ramanathan, R. Mitochondrial degeneration, depletion of NADH, and oxidative stress decrease color stability of wet-aged beef longissimus steaks. J. Food Sci. 2019, 84, 38–50. [Google Scholar] [CrossRef]
  38. Purslow, P.P.; Gagaoua, M.; Warner, R.D. Insights on meat quality from combining traditional studies and proteomics. Meat Sci. 2021, 174, 108423. [Google Scholar] [CrossRef]
  39. Guo, X.; Wang, Y.Q.; Lu, S.L.; Wang, J.Y.; Fu, H.H.; Gu, B.Y.; Lyu, B.; Wang, Q.L. Changes in proteolysis, protein oxidation, flavor, color and texture of dry-cured mutton ham during storage. LWT-Food Sci. Technol. 2021, 149, 111860. [Google Scholar] [CrossRef]
  40. Harkouss, R.; Astruc, T.; Lebert, A.; Gatellier, P.; Loison, O.; Safa, H.; Portanguen, S.; Parafita, E.; Mirade, P.-S. Quantitative study of the relationships among proteolysis, lipid oxidation, structure and texture throughout the dry-cured ham process. Food Chem. 2015, 166, 522–530. [Google Scholar] [CrossRef]
  41. Lonergan, E.H.; Zhang, W.; Lonergan, S.M. Biochemistry of postmortem muscle—Lessons on mechanisms of meat tenderization. Meat Sci. 2010, 86, 184–195. [Google Scholar] [CrossRef] [PubMed]
  42. Zhou, Y.; Wang, Y.; He, J.; Pan, D.D.; Wang, H.F.; Cao, J.X. Evaluating the profile of myofibrillar proteins and its relationship with tenderness among five styles of dry-cured hams. Int. J. Food Sci. Technol. 2020, 56, 259–268. [Google Scholar] [CrossRef]
  43. Malheiros, J.M.; Braga, C.P.; Grove, R.A.; Ribeiro, F.A.; Calkins, C.R.; Adamec, J.; Chardulo, L.A.L. Influence of oxidative damage to proteins on meat tenderness using a proteomics approach. Meat Sci. 2019, 148, 64–71. [Google Scholar] [CrossRef]
  44. Zhang, M.; He, L.C.; Li, C.L.; Yang, F.; Zhao, S.L.; Liang, Y.H.; Jin, G.F. Effects of gamma ray irradiation-induced protein hydrolysis and oxidation on tenderness change of fresh pork during storage. Meat Sci. 2020, 163, 108058. [Google Scholar] [CrossRef] [PubMed]
  45. Sun, W.Z.; Zhou, F.B.; Zhao, M.M.; Yang, B.; Cui, C. Physicochemical changes of myofibrillar proteins during processing of Cantonese sausage in relation to their aggregation behaviour and in vitro digestibility. Food Chem. 2011, 129, 472–478. [Google Scholar] [CrossRef] [PubMed]
  46. Lametsch, R.; Lonergan, S.; Huff-Lonergan, E. Disulfide bond within µ-calpain active site inhibits activity and autolysis. BBA-Proteins Proteom. 2008, 1784, 1215–1221. [Google Scholar] [CrossRef] [PubMed]
  47. Zhu, Y.; Gagaoua, M.; Mullen, A.M.; Kelly, A.L.; Sweeney, T.; Cafferky, J.; Viala, D.; Hamill, R.M. A proteomic study for the discovery of beef tenderness biomarkers and prediction of warner-bratzler shear force measured on longissimus thoracis muscles of young limousin-sired bulls. Foods 2021, 10, 952. [Google Scholar] [CrossRef]
  48. Liao, R.Y.; Xia, Q.; Zhou, C.Y.; Geng, F.; Wang, Y.; Sun, Y.Y.; He, J.; Pan, D.D.; Cao, J.X. LC-MS/MS-based metabolomics and sensory evaluation characterize metabolites and texture of normal and spoiled dry-cured hams. Food Chem. 2022, 371, 131156. [Google Scholar] [CrossRef]
  49. Wang, Y.; Zhang, C.; Liu, F.; Jin, Z.; Xia, X. Ecological succession and functional characteristics of lactic acid bacteria in traditional fermented foods. Crit. Rev. Food Sci. Nutr. 2022, 1–15. [Google Scholar] [CrossRef]
  50. Tian, Z.Q.; Zhu, Q.J.; Chen, Y.S.; Zhou, Y.; Hu, K.; Li, H.Y.; Lu, K.; Zhou, J.; Liu, Y.; Chen, X. Studies on flavor compounds and free amino acid dynamic characteristics of fermented pork loin ham with a complex starter. Foods 2022, 11, 1501. [Google Scholar] [CrossRef]
  51. Chen, Q.; Hu, Y.Y.; Wen, R.X.; Wang, Y.; Qin, L.G.; Kong, B.H. Characterisation of the flavour profile of dry fermented sausages with different NaCl substitutes using HS-SPME-GC-MS combined with electronic nose and electronic tongue. Meat Sci. 2021, 172, 108338. [Google Scholar] [CrossRef] [PubMed]
  52. Estévez, M.; Ventanas, S.; Heinonen, M. Formation of Strecker aldehydes between protein carbonyls—α-Aminoadipic and γ-glutamic semialdehydes-and leucine and isoleucine. Food Chem. 2011, 128, 1051–1057. [Google Scholar] [CrossRef]
  53. Guichard, E. Flavour retention and release from protein solutions. Biotechnol. Adv. 2006, 24, 226–229. [Google Scholar] [CrossRef]
  54. Wang, H.T.; Guan, H.N.; Zhang, H.W.; Liu, H.T.; Chen, Q.; Kong, B.H. Elucidation of interaction mechanisms between myofibrillar proteins and ethyl octanoate by SPME-GC-MS, molecular docking and dynamics simulation. LWT-Food Sci. Technol. 2022, 154, 112787. [Google Scholar] [CrossRef]
  55. Zhou, F.B.; Zhao, M.M.; Su, G.W.; Sun, W.Z. Binding of aroma compounds with myofibrillar proteins modified by a hydroxyl-radical-induced oxidative system. J. Agric. Food Chem. 2014, 62, 9544–9552. [Google Scholar] [CrossRef]
  56. Zhang, J.; Kang, D.-C.; Zhang, W.-G.; Lorenzo, J.-M. Recent advantage of interactions of protein-flavor in foods: Perspective of theoretical models, protein properties and extrinsic factors. Trends Food Sci. Technol. 2021, 111, 405–425. [Google Scholar] [CrossRef]
  57. Flores, M.; Mora, L.; Reig, M.; Toldrá, F. Risk assessment of chemical substances of safety concern generated in processed meats. Food Sci. Hum. Wellness 2019, 8, 244–251. [Google Scholar] [CrossRef]
  58. Ma, J.B.; Wang, X.Y.; Li, Q.; Zhang, L.; Wang, Z.; Han, L.; Yu, Q.L. Oxidation of myofibrillar protein and crosslinking behavior during processing of traditional air-dried yak (Bos grunniens) meat in relation to digestibility. LWT-Food Sci. Technol. 2021, 142, 110984. [Google Scholar] [CrossRef]
  59. Guyon, C.; Meynier, A.; De Lamballerie, M. Protein and lipid oxidation in meat: A review with emphasis on high-pressure treatments. Trends Food Sci. Technol. 2016, 50, 131–143. [Google Scholar] [CrossRef]
  60. Liu, L.; Li, S.S.; Zheng, J.X.; Bu, T.T.; He, G.Q.; Wu, J.P. Safety considerations on food protein-derived bioactive peptides. Trends Food Sci. Technol. 2020, 96, 199–207. [Google Scholar] [CrossRef]
  61. Han, Q.; Kong, B.H.; Chen, Q.; Sun, F.D.; Zhang, H. In vitro comparison of probiotic properties of lactic acid bacteria isolated from Harbin dry sausages and selected probiotics. J. Funct. Foods 2017, 32, 391–400. [Google Scholar] [CrossRef]
  62. Wang, J.; Hou, J.N.; Zhang, X.; Hu, J.R.; Yu, Z.H.; Zhu, Y.C. Improving the flavor of fermented sausage by increasing its bacterial quality via inoculation with lactobacillus plantarum MSZ2 and staphylococcus xylosus YCC3. Foods 2022, 11, 736. [Google Scholar] [CrossRef] [PubMed]
  63. Arnau, J.; Guerrero, L.; Sárraga, C. The effect of green ham pH and NaCl concentration on cathepsin activities and the sensory characteristics of dry-cured hams. J. Sci. Food Agric. 1998, 77, 387–392. [Google Scholar] [CrossRef]
  64. Zhao, G.M.; Zhou, G.H.; Wang, Y.L.; Xu, X.L.; Huan, Y.J.; Wu, J.Q. Time-related changes in cathepsin B and L activities during processing of Jinhua ham as a function of pH, salt and temperature. Meat Sci. 2005, 70, 381–388. [Google Scholar] [CrossRef]
  65. Berardo, A.; Devreese, B.; Maere, H.D.; Stavropoulou, D.A.; Royen, G.V.; Leroy, F.; Smet, S.D. Actin proteolysis during ripening of dry fermented sausages at different pH values. Food Chem. 2017, 221, 1322–1332. [Google Scholar] [CrossRef]
  66. Hu, Y.Y.; Li, Y.J.; Zhu, J.M.; Kong, B.H.; Liu, Q.; Chen, Q. Improving the taste profile of reduced-salt dry sausage by inoculating different lactic acid bacteria. Food Res. Int. 2021, 145, 110391. [Google Scholar] [CrossRef] [PubMed]
  67. Fadda, S.; Vildoza, M.J.; Vignolo, G. The acidogenic metabolism of lactobacillus plantarum crl 681 improves sarcoplasmic protein hydrolysis during meat fermentation. J. Muscle Foods 2010, 21, 545–556. [Google Scholar] [CrossRef]
  68. Casaburi, A.; Monaco, R.D.; Cavella, S.; Toldrá, F.; Ercolini, D.; Villani, F. Proteolytic and lipolytic starter cultures and their effect on traditional fermented sausages ripening and sensory traits. Food Microbiol. 2008, 25, 335–347. [Google Scholar] [CrossRef]
  69. Siedler, S.; Balti, R.; Neves, A.R. Bioprotective mechanisms of lactic acid bacteria against fungal spoilage of food. Curr. Opin. Biotechnol. 2019, 56, 138–146. [Google Scholar] [CrossRef]
  70. Yang, F.; Xia, W.-S.; Zhang, X.-W.; Xu, Y.-S.; Jiang, Q.-X. A comparison of endogenous and microbial proteolytic activities during fast fermentation of silver carp inoculated with Lactobacillus plantarum. Food Chem. 2016, 207, 86–92. [Google Scholar] [CrossRef]
  71. Sun, F.D.; Hu, Y.Y.; Chen, Q.; Kong, B.H.; Liu, Q. Purification and biochemical characteristics of the extracellular protease from Pediococcus pentosaceus isolated from Harbin dry sausages. Meat Sci. 2019, 156, 156–165. [Google Scholar] [CrossRef] [PubMed]
  72. Sun, F.D.; Li, Q.X.; Liu, H.T.; Kong, B.H.; Liu, Q. Purification and biochemical characteristics of the protease from Lactobacillus brevis R4 isolated from Harbin dry sausages. LWT-Food Sci. Technol. 2019, 113, 108287. [Google Scholar] [CrossRef]
  73. Sun, F.D.; Sun, Q.X.; Zhang, H.; Kong, B.H.; Xia, X.F. Purification and biochemical characteristics of the microbial extracellular protease from Lactobacillus curvatus isolated from Harbin dry sausages. Int. J. Biol. Macromol. 2019, 133, 987–997. [Google Scholar] [CrossRef] [PubMed]
  74. Sun, F.D.; Tao, R.; Liu, Q.; Wang, H.; Kong, B.H. Effects of temperature and pH on the structure of a metalloprotease from Lactobacillus fermentum R6 isolated from Harbin dry sausages and molecular docking between protease and meat protein. J. Sci. Food Agric. 2021, 101, 5016–5027. [Google Scholar] [CrossRef] [PubMed]
  75. Sun, F.D.; Hu, Y.Y.; Yin, X.Y.; Kong, B.H.; Qin, L.G. Production, purification and biochemical characterization of the microbial protease produced by Lactobacillus fermentum R6 isolated from Harbin dry sausages. Process Biochem. 2020, 89, 37–45. [Google Scholar] [CrossRef]
  76. Wang, Y.; Wu, Y.P.; Wang, Y.Y.; Xu, H.; Mei, X.Q.; Yu, D.Y.; Wang, Y.B.; Li, W.F. Antioxidant properties of probiotic bacteria. Nutrients 2017, 9, 521. [Google Scholar] [CrossRef]
  77. Lee, J.; Hwang, K.T.; Chung, M.Y.; Cho, D.H.; Park, C.S. Resistance of lactobacillus casei KCTC 3260 to Reactive Oxygen Species (ROS): Role for a metal ion chelating effect. J. Food Sci. 2005, 70, 388–391. [Google Scholar] [CrossRef]
  78. Liu, R.; Li, S.Y.; Yang, B.; Chen, L.; Ge, Q.F.; Xiong, G.Y.; Yu, H.; Wu, M.A.; Zhang, W.A. Investigation of the antioxidant capacity of cell-free extracts from Lactobacillus plantarum NJAU-01 obtained by different cell disruption methods. LWT-Food Sci. Technol. 2021, 152, 112393. [Google Scholar] [CrossRef]
  79. Amaretti, A.; Di Nunzio, M.; Pompei, A.; Raimondi, S.; Rossi, M.; Bordoni, A. Antioxidant properties of potentially probiotic bacteria: In vitro and in vivo activities. Appl. Microbiol. Biotechnol. 2013, 97, 809–817. [Google Scholar] [CrossRef]
  80. Talwalkar, A.; Kailasapathy, K. Metabolic and biochemical responses of probiotic bacteria to oxygen. J. Dairy Sci. 2003, 86, 2537–2546. [Google Scholar] [CrossRef]
  81. Landis, G.N.; Tower, J. Superoxide dismutase evolution and life span regulation. Mech. Ageing Dev. 2005, 126, 365–379. [Google Scholar] [CrossRef] [PubMed]
  82. Gómez-Guzmán, M.; Toral, M.; Romero, M.; Jiménez, R.; Galindo, P.; Sánchez, M.; Zarzuelo, M.J.; Olivares, M.; Gálvez, J.; Duarte, J. Antihypertensive effects of probiotics Lactobacillus strains in spontaneously hypertensive rats. Mol. Nutr. Food Res. 2015, 59, 2326–2336. [Google Scholar] [CrossRef] [PubMed]
  83. Carmel-Harel, O.; Storz, G. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 2000, 54, 439–461. [Google Scholar] [CrossRef]
  84. Arner, E.; Holmgren, A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 2000, 267, 6102–6109. [Google Scholar] [CrossRef] [PubMed]
  85. Aguilar-Toalá, J.E.; Estrada-Montoya, M.C.; Liceaga, A.M.; Garcia, H.S.; González-Aguilar, G.A.; Vallejo-Cordoba, B.; González-Córdova, A.F.; Hernández-Mendoza, A. An insight on antioxidant properties of the intracellular content of Lactobacillus casei CRL-431. LWT-Food Sci. Technol. 2019, 102, 58–63. [Google Scholar] [CrossRef]
  86. Li, S.Y.; Zhao, Y.J.; Zhang, L.; Zhang, X.; Huang, L.; Li, D.; Niu, C.H.; Yang, Z.N.; Wang, Q. Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem. 2012, 135, 1914–1919. [Google Scholar] [CrossRef]
  87. Bleau, C.; Monges, A.; Rashidan, K.; Laverdure, J.-P.; Lacroix, M.; Van Calsteren, M.-R.; Millette, M.; Savard, R.; Lamontagne, L. Intermediate chains of exopolysaccharides from Lactobacillus rhamnosus RW-9595M increase IL-10 production by macrophages. J. Appl. Microbiol. 2010, 108, 666–675. [Google Scholar] [CrossRef]
  88. Aarti, C.; Khusro, A. Functional and technological properties of exopolysaccharide producing autochthonous Lactobacillus plantarum strain AAS3 from dry fish based fermented food. LWT-Food Sci. Technol. 2019, 114, 108387. [Google Scholar] [CrossRef]
  89. Lee, Y.G.; Cho, J.Y.; Moon, J.H. Isolation and antioxidative activity of amino acid derivatives produced by Leuconostoc mesenteroides. Food Sci. Biotechnol. 2016, 25, 329–334. [Google Scholar] [CrossRef]
  90. Zhang, H.; Zhang, C.; Liu, H.T.; Chen, Q.; Kong, B.H. Proteomic response strategies of Pediococcus pentosaceus R1 isolated from Harbin dry sausages to oxidative stress. Food Biosci. 2021, 44, 101364. [Google Scholar] [CrossRef]
  91. Huang, L.; Zeng, X.Q.; Sun, Z.; Wu, A.J.; He, J.; Dang, Y.L.; Pan, D.D. Production of a safe cured meat with low residual nitrite using nitrite substitutes. Meat Sci. 2020, 162, 108027. [Google Scholar] [CrossRef] [PubMed]
  92. Lian, Z.Y.; Li, Y.Q. Isolation of antibacterial, nitrosylmyoglobin forming lactic acid bacteria and their potential use in meat processing. Front. Microbiol. 2020, 11, 1315. [Google Scholar] [CrossRef]
  93. Cao, K.H.; Zhang, K.P.; Ma, M.R.; Ma, J.J.; Tian, J.J.; Jin, Y. Lactobacillus mediates the expression of NPC1L1, CYP7A1, and ABCG5 genes to regulate cholesterol. Food Sci. Nutr. 2021, 9, 6882–6891. [Google Scholar] [CrossRef]
  94. Li, J.Z.; Li, Q.K.; Gao, N.; Wang, Z.H.; Li, F.; Li, J.P.; Shan, A.S. Exopolysaccharides produced by Lactobacillus rhamnosus GG alleviate hydrogen peroxide-induced intestinal oxidative damage and apoptosis through the Keap1/Nrf2 and Bax/Bcl-2 pathways in vitro. Food Funct. 2021, 12, 9632–9641. [Google Scholar] [CrossRef] [PubMed]
  95. Wong, W.Y.; Chan, B.D.; Sham, T.T.; Lee, M.M.L.; Chan, C.O.; Chau, C.T.; Mok, D.K.W.; Kwan, Y.W.; Tai, W.C.S. Lactobacillus casei strain shirota ameliorates dextran sulfate sodium-induced colitis in mice by increasing taurine-conjugated bile acids and inhibiting NF-κB signaling via stabilization of Iκ B α. Front. Nutr. 2022, 9, 816836. [Google Scholar] [CrossRef] [PubMed]
  96. You, Y.; Liu, Y.L.; Ai, Z.Y.; Wang, Y.S.; Liu, J.M.; Piao, C.H.; Wang, Y.H. Lactobacillus fermentum KP-3-fermented ginseng ameliorates alcohol-induced liver disease in C57BL/6N mice through the AMPK and MAPK pathways. Food Funct. 2020, 11, 9801–9809. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Mechanism of Protein Oxidation in Fermented Meats [7,25]. Notes: P = protein; L = lipid. The blue color represents the metal ion-catalyzed protein oxidation mechanism, and the green color represents the lipid peroxidation-induced protein oxidation.
Figure 1. Mechanism of Protein Oxidation in Fermented Meats [7,25]. Notes: P = protein; L = lipid. The blue color represents the metal ion-catalyzed protein oxidation mechanism, and the green color represents the lipid peroxidation-induced protein oxidation.
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Figure 2. Effects of Protein Changes on the Quality of Fermented Meat Products.
Figure 2. Effects of Protein Changes on the Quality of Fermented Meat Products.
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Figure 3. Effects of Protein Degradation on the Flavor of Fermented Meats [48,49].
Figure 3. Effects of Protein Degradation on the Flavor of Fermented Meats [48,49].
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Figure 4. Antioxidant regulation mechanism of LAB. Note: SOD: superoxide dismutase; CAT: catalase; NADH: nicotinamide adenine dinucleotide; Trx: thioredoxin; TrxR: thioredoxin reductase; NADPH: nicotinamide adenine dinucleotide phosphate; GR: glutathione reductase; GSH: glutathione; GPx: glutathione peroxidase.
Figure 4. Antioxidant regulation mechanism of LAB. Note: SOD: superoxide dismutase; CAT: catalase; NADH: nicotinamide adenine dinucleotide; Trx: thioredoxin; TrxR: thioredoxin reductase; NADPH: nicotinamide adenine dinucleotide phosphate; GR: glutathione reductase; GSH: glutathione; GPx: glutathione peroxidase.
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Table 1. Composition of Crude Peptide in Fermented Meat.
Table 1. Composition of Crude Peptide in Fermented Meat.
SamplePeptide SequenceLengthMass (Da)Protein of OriginReferences
Fermented sausageLPVKY 5618.3741 Phosphatidylinositol 3-kinase catalytic subunit type 3[22]
PFGDTH 6672.2867 CDP-6-deoxy-delta-3,4-glucoseen reductase
QPSLVH6679.3653Aminoglycoside transferase
LPVTVR 6683.433 Rho guanine nucleotide exchange factor 2
LPSLKF 6703.4268 Phosphoglycerate kinase
HKLPVK 6720.4646 Myoglobin
YGLDEK 6723.3439 Serine/threonine-protein kinase A
LDRKDL 6758.4286 Lipid A biosynthesis lauroyltransferase
LDLRDK 6758.4286 Tetratricopeptide repeat protein 27
EGGLSKLTLDKLDVKGK 171800.036 Phosphoglycerate kinas
EARSKLTLDKLDVKGK 161800.047 Phosphoglycerate kinase
ESDLLAAFR 91020.524 Adenosine kinase
EVSHGSDQVKAHGQK 151605.786 Hemoglobin subunit alpha
ELSNKLTLDK 101159.645 Phosphoglycerate kinase
VDLNGGSHAGNK 121167.563 Beta-enolase isoform X1
EGADSEMALFGEAAPYLRKSEKEVGKN 272925.418 Myosin-1 isoform X1
NPPKF 5601.3224Myosin
KGGSLELTLDKLDVKGK 171800.036 Phosphoglycerate kinase
MWTD4551.61Uncharacterized protein[23]
SAGNPN6558.20Uncharacterized protein
APYMM5611.76Uncharacterized protein
FWIIE5706.84Spectrin alpha chain-like protein
GVDNPGHP8791.81Creatine Kinase M-type
MVHMASK7803.00Glyceraldehyde-3-phosphate dehydrogenase
FGNTHNK7816.87Creatine Kinase M-type
IPPKIPEGE9887.01Troponin T
ERFSKDE7909.93Uncharacterized protein
ERSFKDE7909.93Troponin T
PFGNTHNK8913.99Creatine Kinase M-type
NVINGGSHAG10924.97Glyceraldehyde-3-phosphate dehydrogenase
HIITHGEE8935.02Myosin regulatory light chain 2
DVAGHGQEVL101024.10Myosin regulatory light chain 2
IDDMIPAQK91030.20Creatine Kinase M-type
GKKFNV6565.28Transcription activator BRGl[23]
LVVDGVK7728.88Uncharacterized protein
VDIINAK7772.45Uncharacterized protein
VHMASKE7801.39Glyceraldehyde-3-phosphate dehydrogenase
LVVDGVKL8841.53Creatine Kinase M-type
IPPKIPEGE9887.01Troponin T
KAGTTPKGK9887.04Maturase K
YGEKLKR7893.04Binding protein
PFGNTHNK8913.99Creatine Kinase M-type
VKQKGPDF8918.50Pyruvate kinase
AGQAFRKF8924.05Uncharacterized protein
MVHMASKE8932.43Glyceraldehyde-3-phosphate dehydrogenase
VITHGDAKD9955.48Myosin regulatory light chain 2
LQNHPEHS8960.99Glyceraldehyde-3-phosphate dehydrogenase
LRDKAKEL8972.12Binding protein
DVGDWRKN8989.05Troponin T
KKAGTTPKGK101015.21Troponin T
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MDPI and ACS Style

Wang, D.; Cheng, F.; Wang, Y.; Han, J.; Gao, F.; Tian, J.; Zhang, K.; Jin, Y. The Changes Occurring in Proteins during Processing and Storage of Fermented Meat Products and Their Regulation by Lactic Acid Bacteria. Foods 2022, 11, 2427.

AMA Style

Wang D, Cheng F, Wang Y, Han J, Gao F, Tian J, Zhang K, Jin Y. The Changes Occurring in Proteins during Processing and Storage of Fermented Meat Products and Their Regulation by Lactic Acid Bacteria. Foods. 2022; 11(16):2427.

Chicago/Turabian Style

Wang, Daixun, Feng Cheng, Yi Wang, Jun Han, Fang Gao, Jianjun Tian, Kaiping Zhang, and Ye Jin. 2022. "The Changes Occurring in Proteins during Processing and Storage of Fermented Meat Products and Their Regulation by Lactic Acid Bacteria" Foods 11, no. 16: 2427.

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