Edited by: Xucong Lv, Fuzhou University, China
Reviewed by: Yongqiang Zhao, Chinese Academy of Fishery Sciences (CAFS), China; Aly Farag El Sheikha, Jiangxi Agricultural University, China
This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Cheese has a long history and this naturally fermented dairy product contains a range of distinctive flavors. Microorganisms in variety cheeses are an essential component and play important roles during both cheese production and ripening. However, cheeses from different countries are still handmade, the processing technology is diverse, the microbial community structure is complex and the cheese flavor fluctuates greatly. Therefore, studying the general processing technology and relationship between microbial structure and flavor formation in cheese is the key to solving the unstable quality and standardized production of cheese flavor on basis of maintaining the flavor of cheese. This paper reviews the research progress on the general processing technology and key control points of natural cheese, the biochemical pathways for production of flavor compounds in cheeses, the diversity and the role of yeasts in cheese. Combined with the development of modern detection technology, the evolution of microbial structure, population evolution and flavor correlation in cheese from different countries was analyzed, which is of great significance for the search for core functional yeast microorganisms and the industrialization prospect of traditional fermented cheese.
Cheese is an ancient traditional fresh or fermented dairy product with a long history of production. Cheese making originated in various West Asian countries about 8,000 years ago (
Fermented dairy products with high nutritional value are considered “the pearls in the crown of the dairy industry” (
Globally, there is a lack of an authoritative cheese-making process, which can be used for cheese production followed in any country – China or abroad. This is due to differences in regions, production methods, and available raw materials. The earliest method of producing cheese in the world was to carry the milk to the animal’s internal and the milk was fermented into cheese by constant oscillation during the migration. Cheese is made differently in different regions. For instance, for making cheddar cheese in southwest England, the raw material is sterilized and cooled; then, the fermenting agent, calcium chloride, and rennet are added to ferment the curd (
The acceptability of cheese to the final consumer largely depends on specific sensory characteristics, including flavor and aroma. The unique characteristics and special quality of cheese all depend on the various compounds and molecules that constitute it, including fatty acids, amines, ketones, free amino acids, alcohols, aldehydes, lactones, and sulfur compounds (
Traditionally fermented cheeses have complex microbial communities, multi-strain co-fermentation, complex metabolic mechanisms, and different flavor profiles. Therefore, microbes play a pivotal role in cheese flavor formation. The current review aims to provide a comprehensive overview of dynamics of the cheese microbiota in various cheese-making processes and technologies as well as understand the main biochemical pathways of cheese flavor formation, with a specific focus on the role of yeasts in cheese. Furthermore, this review provides important advances in understanding the effects of different cheese-making techniques and microbial diversity on cheese flavor and quality.
More than 2,000 different cheese varieties exist in the world, of which more than 400 are more famous (
Classification and main varieties of cheese.
Form facture | Moisture content/% | Mature microorganisms | Main cheese variety | Cheese flavor | Country of origin |
---|---|---|---|---|---|
Extra hard cheese | Bacterial | Parmesan | Fruit flavor and salt | Italy ( |
|
Romano | Strong flavor | ||||
Hard cheese | Bacterial: atmospheric hole | Emmanuel | Fruity aroma and taste stimulation | Switzerland ( |
|
Gruyere | Aromatic, rich, and smooth smell | ||||
Bacterial: no air holes | Cheddar | Walnut flavor | United Kingdom ( |
||
Semi-hard cheese | Bacterial: small air hole | Gouda | Caramel and creamy candy | Netherlands ( |
|
Bacterial: no air holes | Edam | Sweet and nutty | |||
Semi-soft cheese | Bacterial | Brick | Spicy | German ( |
|
Limburg | Spicy | ||||
Mold | Roquefort | Strong salt aroma | France, Denmark ( |
||
Blue | Strong spicy | ||||
Soft cheese | Mold | Camembert | Mild | France ( |
|
Not mature | Cottage | Mild | America ( |
||
Cream | Slightly sour |
Bold values indicate the values of the header and moisture content.
Milk high in bacterial numbers may contain lactose-fermenting bacteria, which may interfere with milk acidification during cheese making. A cheese maker would not have strict control over the rate and extent of acidification during cheese making, which is one of the key components of successful cheese making. Pasteurization kills most bacteria capable of fermenting lactose, so it is sometimes necessary to use added starter for proper fermentation. Pasteurization kills most lactose fermenters and enables more stringent acidification control during the cheese-making process more stringent, in turn facilitating cheese quality control. Therefore, adding a starter is necessary for proper fermentation here. For some cheese varieties, especially cheddar, Parmesan, and aged Gouda, it is a common practice to add adjunct bacteria (mostly
For centuries, the milk used to make many cheese varieties in the world has not pretreated in anyway before curdling. That is, raw milk, especially artisanal cheese, is conventionally used for making these cheeses (
The general processing process of natural cheeses.
Cheese is generally produced from cow’s milk, but several cheeses, such as Roquefort, feta, and Manchego, are produced using the sheep or goat milk (
Extra-hard cheeses have very low water and fat contents. The key components of their production include low-fat milk, thermophilic LABs, high blanching temperature, long salt water–soaking period, and long-term slow ripening (
The carbon dioxide produced by propionic acid bacteria (PAB) leads to formation of holes (also called “eyes”) in hard cheeses, such as Swiss and Emmental (
Semi-hard cheeses have a wide range of flavor profiles and structures because of the various LABs used and their effects. For Caerphilly and Lancashire cheeses, the growth of strains is promoted during the clot production stage: the low acidity (pH 5.0–5.2) of fresh cheese produces acidic clots that cause the cheese to have a crumbly texture (
Limburger is called “smelly cheese” because of its strong aroma, mainly originating from the rind, rather than the cheese itself. Limburger is first stored for 2 weeks under higher temperature and humidity and then matured for 2–3 months under refrigerated conditions. During this time, it is soaked in brine several times to stimulate the growth of bacteria and the formation of a light brown crust and a unique taste. For storage, Limburger is wrapped in packaging made of breathable material such as aluminum foil or paper to ensure that the cheese remains ripe. Blue cheeses, including Roquefort and Danish blue cheese, are produced from high-acid, semi-soft curds, involving slow acid production over a long period of whey removal. The clots are not heated during processing, and the cheese is not mechanically pressed like pasta filata cheeses. The typical process of producing blue cheese includes puncturing the cheese for aeration to promote the growth of
Mozzarella cheese is a semi-hard, fresh pasta filata family cheese. Its most unique processing technique includes hot stretching, which gives the cheese its distinctive texture. Mozzarella requires rapid acid production, but high acidity can also lead to low-quality cheese production. High-fat cheeses are sour curd cheeses. For these cheeses, whey is traditionally drained by hanging the clots in bags – similar to traditional Kazak cheese making (
In contrast, the main forces that drive cheese technology are economics, equipment/engineering, consumer demands, and regulatory standards. In addition, production of consistent and high-quality cheese, while maintaining high-volume throughput is a key challenge in cheese manufacture (
In recent years, new biotechnologies to promote cheese maturation and improve flavor have been explored frequently, including the inoculation of additional cultures and exogenous enzymes, and the impact of temperature and high pressure on the quality of cheese (
The development of dairy technology has allowed for the standardization of industrial production technology for some cheeses, whereas other cheeses are still prepared using with the traditional non-standardized methods. For example, ultrafiltration and concentration technologies are more suitable for feta production, but Kazak cheese is made using the traditional non-standardized manual processes. In addition, use of edible films and coatings in cheese preservation has opportunities and challenges (
Cheese is a product of biochemical dynamics occurring during its production and ripening (
Cheese flavor substances include acids, alcohols, esters, ketones, and lactones – all of which are affected by raw milk quality and fermentation and/or ripening processes (
Lactose and citrate are the main carbohydrates in all mammalian milks, but the lactose content varies widely from mammal to mammal (range, 0–100 g/L;
Biochemical pathways for production of flavor compounds in cheeses.
In mature cheeses such as Camembert and Brie, lactate in the surface layer is metabolized and decomposed into water and oxygen by the mold and yeast on the surface, causing their pH to increase (
In milk, citrate mainly exists in the form of ionized salts at concentrations of ≤1.8 g/L, most of which is lost in the whey during cheese making. This is because nearly 94% of the citrate is in the soluble phase of the milk (
Lipolysis has an important effect on cheese flavor and texture (
The formation of typical flavor of cheese through lipolysis mainly reflects in the following: the ester bonds between triglycerides and fatty acids break under the action of lipase and monoglycerides, diglycerides, and free fatty acids are produced (
Fatty acids produced
Short-chain fatty acids provide strong characteristic flavors, some of which are precursors to flavor and are converted to other aromatic substances, including lactones and alcohols (
Protein hydrolysis, a main biochemical reaction, is crucial to the formation of cheese flavor and has an important influence on the release and taste of cheese flavor during cheese ripening process (
Free amino acid content and metabolism in mature cheese play essential roles in cheese flavor development. Under the action of transaminase, deaminase, decarboxylase, and other enzymes, free amino acids in cheese are transformed into a series of volatile and nonvolatile flavor substances (e.g., ketones, aldehydes, acids, and alcohols)
Branched-chain amino acids – the precursors of aromatic compounds such as isobutyl ester, 3-methylbutanal, and 2-methylbutanal – are found in different cheeses (
In cheese, methionine is converted to volatile sulfur compounds, such as methanethiol (which has a rancid flavor) as well as dimethyl sulfide and dimethyl trisulfide (which have a garlicky flavor); they represent the basic flavor substances in many cheese varieties (
The various cheeses have varied aromas and complex structures, the analysis of which mainly based on volatile component extraction. At present, the main extraction methods include distillation, solvent extraction, headspace capture method (HS), and solid-phase microextraction (SPME). Distillation is a relatively simple extraction technique; however, it is time and labor intensive (
Gas chromatography–mass spectrometry, which plays a significant role in food flavor substance analysis, has been widely used in the detection of volatile and semi-volatile samples (
More than 600 compounds have been identified as food volatile components thus far. Only a few of these compounds have a significant effect on the sensory flavor profile of the analyzed food. Only GC–MS can analyze for a wide range of volatile compounds. However, it cannot determine the flavor active ingredients that contribute the most to the flavor in food. Gas chromatography olfactometry (GC-O) is the most effective for detecting and identifying aroma component identification; the analytical methods that can be used with this technique mainly include the time–intensity method, Charm analysis, and aroma extraction dilution analysis (
The traditional fermented foods, including Chinese liquor, cheese, vinegar, and bread, are enriched with various microorganisms in an open environment. Consequently, cooperative metabolism of multiple microbiotas underlies the fermentation involved in these foods (
The cheese ecosystem is a special habitat that supports the coexistence of yeast, bacteria, and filamentous fungi. The initial dominant yeasts are acid and salt tolerant; they can metabolize lactate produced by the SLAB and produce NH3 from amino acids. Yeast in cheese originates from not only milk but also the processing environment and storage process during the cheese fermentation process (
A study on the diversity of 44 types of cheese fungi found that
Traditional fermented cheeses show complex microbial communities, multispecies cofermentation, complex metabolic mechanism, and varied flavors. The flavors in cheese are mainly produced
Traditional fermented cheeses have a stable core microbiota; however, the yeast species present in this microbiota needs to be further analyzed based on their metamorphic genome and metabolomics. The effects of microbial interactions, environment, and production processes on the microbial community of cheese have demonstrated that the microbes distributed in cheese surfaces are highly reproducible, making cheese an easy-to-handle, constructible microecosystem model. The focus of ongoing relevant research includes the following: (1) a method for effective control of the ripening stage of cheese for ensuring the flavor and quality of the finished cheese; (2) identification of the core microbiota including various yeast species involved and their interactions during cheese production and ripening; (3) exploration of the correlation between the aforementioned interactions or dynamic changes and the flavor changes during cheese production and ripening; and (4) a method to analyze the internal relationship between the ecological and functional characteristics of the cheese microbial community.
Yeasts play an important role in the manufacture of nearly all traditional ripened cheeses, especially some smear ripened cheeses such as Gruyère, Tilsit, and Reblochon (
The development of yeast in cheese depends on many physicochemical conditions, such as low pH, mold content, high salt concentration, refrigerated ripening, and storage conditions (
Most of the yeasts isolated from the surface of mature cheeses are salt tolerant, of which
Traditional fermented cheeses are mostly fermented naturally using multiple microbial strains. Scientific problems such as unclear mechanism underlying flavor substance formation and unstable flavor quality have become a bottleneck for developing standardized cheese production processes – severely restricting the transformation of manual production to industrial processing. In recent years, studies have screened the functional microbial strains that improve the flavor of cheese. A study reported that the contents of ethanol, esterase, and glycol acyltransferase are the main factors limiting the synthesis of ethyl acetate in French Camembert (
With the advancement of science and technology, the use of various traditional methods may decrease. Thus, application and protection of microbial resources used in traditional fermented foods, such as cheese, is urgently needed. Therefore, evaluating the impact of dairy products on human health by using microbial resources in traditional fermented dairy products is essential. The microbial population inhabiting cheese has strong ecological adaptability; it also determines microbial community structural diversity and flavors of the various cheeses from different countries. The regional and climatic differences and diversification of processing technologies have induced considerable changes in the cheeses worldwide in terms of factors, such as appearance and flavor. The metabolic effects of yeast on cheese ripening and quality have long been underestimated, and the metabolic mechanisms of yeast have slowly been elucidated in the recent years. Therefore, studying the relationship of yeast community structure with the formation of yeast microbiota and flavor substances in the process of cheese fermentation is the key to producing cheese with the desired flavor and stable quality by using a cheese-specific standardized process. In summary, cheese has the potential to become a dairy product consumed on a large-scale in the future, and thus, it has very broad market prospects. The current review provided a theoretical basis for the succession and selection of functional yeast strains, and optimization of cheese processing technologies to improve flavor and quality of fermented cheese.
XZ wrote the main text of the manuscript. BW and XS supervised the research activities. All authors contributed to the article and approved the submitted version.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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