A Review: Microbial Diversity and Function of Fermented Meat Products in China

Fermented meat products have a long history in China. These products exhibit a characteristic unique flavor, compact meat quality, clear color, long shelf life and wide variety and are easy to transport. During the processing and storage of fermented meat products, microorganisms are present and exhibit diverse characteristics. Microorganisms can accelerate the degradation of proteins and fats to produce flavor compounds, inhibit the growth and reproduction of heterozygous bacteria, and reduce the content of chemical pollutants. This paper reviews the microbial diversity of Chinese ham, sausage, preserved meat, pressed salted duck, preserved fish and air-dried meat and provides analyses of the microbial compositions of various products. Due to the differences in raw materials, technology, auxiliary materials, and fermentation technology, the microbial species found in various fermented meat products in China are different. However, most fermented meat products in China are subjected to pickling and fermentation, so their microbial compositions also have similarities. Microorganisms in fermented meat products mainly include staphylococci, lactobacilli, micrococci, yeasts, and molds. The study of microbial diversity is of great significance for the formation of quality flavor and the safety control of fermented meat products, and it provides some theoretical reference for the study of fermented meat products in China.


INTRODUCTION
Fermented meat products are meat products with longer shelf lives and special flavors, textures and colors that are made of raw meat under specific temperature and humidity conditions by fermentation via microorganisms or enzymes . Fermentation methods include natural fermentation and the artificial addition of a starter to regulate fermentation (Sivamaruthi et al., 2020). The microorganisms involved in the natural fermentation process are primarily derived from raw materials and the environment. Under specific curing and maturing process conditions, typical local microbial communities are formed through competition, thus significantly affecting the product quality and safety (Frédéric et al., 2006). In the 1990s, with the transformation of Chinese people's demand for meat from quantity to quality, fermented meat products with artificially added microbial starters were gradually introduced into the Chinese market (Yu et al., 2010).
Many traditional meat products, such as Sichuan preserved meat, Hunan preserved meat, Nanjing pressed salted duck, Cantonese sausage, Sichuan sausage, Jinhua ham, Xuanwei ham, and Rugao ham, are all fermented. In recent years, with the improvement of production technology and equipment, research on the flavor, sensory perception, nutritional characteristics and safety of fermented meat products has become a hot topic (Douglas et al., 2020). Microorganisms play an important role during the fermentation of meat products. Flavor formation in fermented meat products is a complex biochemical process that has not been completely understood to date. The microbial diversity of the primary fermented meat products in China is summarized in this paper, and the characteristics of their microbial compositions were analyzed to provide a theoretical basis for further study on fermented meat products.

THE FUNCTION OF MICROORGANISMS IN FERMENTED MEAT PRODUCTS
Food fermentation is not only an effective method of food preservation but also an economical method of food processing . Microorganisms play an important role in fermented meat products, and their functions are as follows: Promotion of the production of special flavors in meat products (PaPamanoli et al., 2002;Polka et al., 2015). Studies have shown that Staphylococcus carnosus (S. carnosus) and Staphylococcus xylosus (S. xylosus) can significantly promote the hydrolysis of fat and protein in preserved meat, improve the color and promote the rapid formation of flavor (Zhou et al., 2018). The esterases, proteases and catalases produced by microorganisms have synergistic effects with endogenous enzymes, causing biochemical changes in the proteins and fats in raw meat and forming small molecules, such as amino acids, esters, peptides and short-chain volatile fatty acids. The digestive function is greatly improved, and the contents of essential amino acids, vitamins and bifidobacterium are increased, enhancing the effects on nutrition and health (Liang et al., 2010). Chen et al. (2017) inoculated Harbin dried sausage with a mixed starter, and the free fatty acid (FFA) content in the inoculated group was significantly higher than that in the uninoculated group. The peroxide value and thiobarbituric acid contents in the inoculated group were significantly reduced compared with those in the uninoculated group, and the contents of aldehydes, ketones and hydrocarbons, which are related to lipid oxidation, were significantly reduced compared with those in the uninoculated group. The mixed starter promoted the hydrolysis of fat, inhibited lipid peroxidation and improved the fermentation flavor of Harbin dried sausage. Wang et al. (2014) added complex microbial starters to traditional preserved meat, and the contents of free amino acids and the types of volatile flavor substances in the preserved meat increased, which improved its nutritional value, flavor and safety.
Inhibition of the growth and reproduction of heterozygous bacteria (Swetwiwathana and Visessanguan, 2015).
Microorganisms primarily inhibit the growth and reproduction of harmful bacteria through bacterial competition, acid production and bacteriocin production. Studies have shown that S. xylosus can inhibit the growth of Listeria monocytogenes (L. monocytogenes) in sausage (PaPamanoli et al., 2002). Wang et al. (2013) inoculated Latilactobacillus sakei subsp. sakei (L. sakei) as a starter culture into Sichuan sausage, and the results showed that the lactic acid bacteria rapidly controlled the growth of the total bacterial colonies during sausage fermentation and inhibited the growth of foodborne pathogenic bacteria, such as Escherichia coli (E. coli) and enterobacteriaceae. Lactic acid bacteria can decompose carbohydrates in sausages to produce a large number of lactic acid and a small number of acetic acid as well as propionic acid, formic acid, 3-methyl-butyric acid, butyric acid and other organic acids, thus extending the shelf life of sausages . Lactic acid bacteria can reportedly inhibit or kill spoilage microorganisms and pathogenic microorganisms in food . Zhao et al. (2017) isolated and screened a strain of lactic acid bacteria with obvious antibacterial activity against E. coli and Staphylococcus aureus (S. aureus) from five kinds of fermented meat products, which was identified as Weissella hellenica (W. hellenica). Studies have shown that L. sakei C2 can produce broad-spectrum antibacterial bacteriocins and inhibit the growth of harmful microorganisms (Gao et al., 2014).
Reducing the content of biogenic amines (BAs). Sun et al. (2016) found that six types of BAs (cadaverine, putrescine, tryptamine, 2-phenylethylamine, histamine, and tyramine) were inhibited by the presence of L. plantarum and S. xylosus, and a mixture of these bacteria had the highest inhibitory effect. Niu et al. (2019) selected L. plantarum PL-ZL001 from four types of fermented meat products and added it to sausage. PL-ZL001 inhibited the accumulation of six BAs, and its inhibitory effect on the most toxic histamine was significantly greater than that of commercial S. xylosus.
Reducing the nitrite content. Wang et al. (2013) inoculated L. sakei as a starter culture into Sichuan sausage. The results showed that the nitrite content in the sausage containing added L. sakei decreased rapidly from 100 to 9.6 ppm, whereas the nitrite content in the naturally fermented sausage decreased slowly from 100 to 32.1 ppm. You et al. (2015) inoculated lactic acid bacteria into dried salted fish as a starter, and the results showed that the mass fraction of nitrite in the dried salted fish with added lactic acid bacteria was (0.1 ± 0.04) mg·kg −1 , which was significantly lower than that in the group without the addition of lactic acid bacteria at (0.8 ± 0.04) mg/kg −1 . Lactic acid bacteria had an inhibitory effect on the formation of nitrosamines. Gao et al. (2014) inoculated 5 log CFU/g and 7 log CFU/g L. sakei C2 into sausage, and the results showed that the nitrite content decreased with increasing inoculation concentrations.
Microorganisms can improve the quality of fermented meat products to a certain extent. They can not only promote the degradation of protein and fat and accelerate the formation of flavor substances but can also improve the nutritional value of fermented meat products. At the same time, they can inhibit the growth and reproduction of harmful bacteria, reduce the use of salt in fermented meat products, improve the taste, reduce the content of nitrite and BAs, and improve the safety of fermented meat products.

MICROBIAL DIVERSITY IN FERMENTED MEAT PRODUCTS Ham
Ham is a non-ready-to-eat meat product made from fresh (frozen) pig hind legs as the primary raw material with other auxiliary materials add after finishing, curing, washing, desalting, air-drying and fermentation, and other processes. The most famous Chinese-style hams are Jinhua, Rugao, and Xuanwei hams. Alcohols, ketones, aldehydes, esters, alkanes, and acids are considered the primary volatile compounds in hams (Radovčić et al., 2016;Liu D. Y. et al., 2020;Wu et al., 2020). There is a close relationship between the staphylococci and the aldehyde compounds produced as hexanal, nonanal, benzaldehyde, and phenylacetaldehyde, indicating their contributions to the formation of characteristic flavor substances in Jinhua dry-cured ham . Yeasts and molds were primarily present on the surface of Anfu ham, and cocci and yeasts were primarily present inside the ham (Huang et al., 2003). During the dehydration of Jinhua ham, the number of microorganisms inside the ham reached 1.39 × 10 6 CFU/g, and during the maturation stage, the number of microorganisms inside decreased to 2.0 × 10 3 CFU/g. Lactic acid bacteria and staphylococci are the dominant bacteria in Jinhua ham. The lactic acid bacteria have primarily been identified as Pediococcus urinaeequi (P. urinaeequi), Pediococcus pentosaceus (P. pentosaceus), and Lactiplantibacillus pentosus (L. pentosus). The staphylococci species primarily include S. xylosus, Staphylococcus equus (S. equus) and Staphylococcus gallinarum (S. gallinarum) (He et al., 2007). The dominant microorganisms in Xuanwei ham were micrococci, staphylococci and molds, the number of which reached greater than 10 6 CFU/g on the surface and greater than 10 2 CFU/g inside (Li et al., 2003). Twenty-seven fungi were detected in Xuanwei ham using PCR-DGGE technology. The primary species were Aspergillus pseudoglaucus (A. pseudoglaucus), Phialosimplex caninus (P. caninus), Aspergillus penicillioides (A. penicillioides), Yamadazyma triangularis (Y. triangularis), Wallemia sebi (W. sebi), and Candida glucosophila (C. glucosophila), among which the dominant fungus was A. pseudoglaucus (Zou et al., 2020). The diversity and abundance of bacteria in Panxian ham were higher than those of fungi. Ten bacterial phyla were detected at the phylum level, of which Firmicutes and Proteobacteria were dominant. Firmicutes and Proteobacteria were the dominant phyla in the curing process, while Proteobacteria was the dominant phylum in the maturing process. A total of 154 bacterial genera was detected at the genus level, and the dominant genera were Psychrobacter, Acinetobacter, Ochrobactrum, Staphylococcus, and Micrococcus. Four fungal phyla were detected at the phylum level, and the dominant fungus was Ascomycota. Fifty-one fungal genera were detected at the genus level, and the dominant fungi were Debaryomyces, Aspergillus, Yamadazyma, Candida, and Penicillium (Mu et al., 2019). After isolation and purification of the dominant microorganisms in Weining ham, a total of 10 strains was obtained, including 4 strains of Staphylococcus equinosus (S. equinosus), 2 strains of S. xylosus, 2 strains of Lactococcus lactis, 1 strain of Candida metapsilosis (C. metapsilosis), and 1 strain of Candida parapsilosis (C. parapsilosis) . Among the different processing procedures of Nuodeng ham, the bacterial diversity at the salting stage was the highest, and the dominant bacteria at the phylum level were Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes. At the genus level, the dominant bacteria included Psychrobacter, Aeromonas, Shewanella, Pseudomonas, and Acinetobacter (Wang X. R. et al., 2021). The primary species of microorganisms in different hams are presented in Table 1.

Sausage
Sausage is a type of non-ready-to-eat meat product made from fresh (frozen) livestock and poultry meat and other auxiliary materials by cutting (or mincing), stirring, curing, filling (or shaping), drying by baking (or drying in the sun, air-drying in the shade), smoking (or not smoking) and other processes. Sausage is primarily produced in Sichuan, Guangdong, Guangxi, Hunan, and Shanghai. The most famous sausages are Cantoneseand Sichuan-style sausages. Sichuan-style sausage is spicy and hot, whereas Cantonese-style sausage is salty and sweet. Among the different styles, Sichuan sausage is distinguished by its high processing and consumption, multiflavored nature and excellent flavor. The flavor components of mature sausage primarily include acetic acid, 3-hydroxy-2-butanone, 2-butanone, esters, volatile phenols, aldehydes and small amounts of alkene, and nitrogen compounds (Hu et al., 2020). Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes were detected at the phylum level in Sichuan sausage. Firmicutes  (Hu et al., 2020). The primary species of microorganisms in different sausages are presented in Table 2.

Pressed Salted Duck
Pressed salted duck is a non-ready-to-eat meat product made from duck as the raw material processed by slaughter, hair removal, evisceration, cleaning and curing, shaping, and air drying. Pressed salted duck is a specialty of the southwest region, and famous products include Chongqing Baishiyi pressed salted duck, Nanan pressed salted duck, and Jianchang pressed salted duck. Benzaldehyde and (E, E)-2,4-nonadienal are the key flavor compounds of pressed salted duck. Hexanal, nonanal, naphthalene, (Z)-2-heptenal, (E)-2-octenal, (E)-2kunienal, 1-octene-3-ol, 2-n-pentylfuran and linalool were the primary compounds affecting the flavor differences in pressed salted ducks from different regions (Tong et al., 2018). The total number of microbial colonies in Sichuan air-dried ducks was 4.692 × 10 3 CFU/g, and Neisseria, Micrococcus, and Staphylococcus were the primary dominant genera (Liu et al., 2007). The beneficial microorganisms in Jianchang pressed salted duck primarily include staphylococci, lactic acid bacteria,  (Lin, 2017). The predominant spoilage bacteria in water-cooked salted duck at the end of the shelf life were Brochothrix thermosphacta (B. thermosphacta) and lactic acid bacteria, and minor components were enterobacteriaceae, micrococci, yeasts and molds (Li et al., 2010). The primary species of microorganisms in different pressed salted ducks are presented in Table 4.

Air-Dried Meat
Air-dried meat is stored at temperatures below zero. The meat is cut into small strips and treated with spices, pickled and hung  in the shade, and it is naturally air-dried for approximately 3 months to form a directly edible product. After drying, the meat is crispy, and this product is commonly found in Xizang and northwestern Inner Mongolia. The volatile flavor compounds in air-dried meat include acids, aldehydes, ketones, alcohols, alkenes, sulfur-containing compounds and heterocyclic compounds, among which heptanal, 1octene-3-ol, cyclopentanol, 3-hydroxy-2-heptanone, and 6-methyl-5-heptene-2-ketone are the primary contributors (Ma et al., 2021). The dominant microorganisms during the air-drying process of Xinjiang air-dried beef were lactic acid bacteria, staphylococci and micrococci. The total number of microorganisms was 8.0 × 10 8 CFU/g, the number of lactic acid bacteria was 1.48 × 10 7 CFU/g, the number of staphylococci and micrococci was approximately 4.40 × 10 8 CFU/g, the number of enterobacteria was approximately 10 2 CFU/g, the number of enterococci was less than 10 5 CFU/g, and the number of yeasts and molds was approximately 1.50 × 10 4 CFU/g (Wang et al., 2016). Lei et al. (2017) found 36% enterobacteria, 33% yeasts, 16% pseudomonades, 10% cocci, and 5% lactic acid bacteria in Xinjiang air-dried beef.

CONCLUSION AND PROSPECT
Due to differences in raw materials, technology, auxiliary materials and fermentation time, the microbial species in fermented meat products in China are different. However, most fermented meat products in China are subjected to salting and fermentation, so the microbial compositions share some similarities. Microorganisms in fermented meat products mainly include staphylococci, lactobacilli, micrococci, yeasts, and molds. At present, research on fermented meat products largely focuses on the microbial diversity of fermented meat products, the mechanisms by which specific microbes influence the quality of fermented meat products, the characteristic flavor of fermented meat products and their production pathway. A large number of studies have shown that microorganisms can promote the formation flavor of fermented meat products and inhibit the generation of BAs, nitrosamines and other harmful chemicals in fermented meat products, but the specific mechanisms have not been fully reported. In the future, research on these mechanisms will provide effective theoretical support for improving the production process and the modernization and standardization of production of fermented meat products.

AUTHOR CONTRIBUTIONS
ZLW and ZXW conducted the literature collection and literature research. ZLW drafted the original manuscript. ZLW, ZXW, and LC modified the manuscript. All authors critically reviewed, contributed to, and approved the final manuscript.