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Utility of dairy microbiome as a tool for authentication and traceability

  • Maria V. Alvanou , Dimitrios Loukovitis , Katerina Melfou and Ioannis A. Giantsis EMAIL logo
Published/Copyright: October 30, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

Milk microbiome contributes substantially to the formation of specific organoleptic and physicochemical characteristics of dairy products. The assessment of the composition and abundance of milk microbiota is a challenging task strongly influenced by many environmental factors. Specific dairy products may be designated by the Protected Designation of Origin (PDO) and Protected Geographical Indication (PGI) labeling, which however, occasionally fail to differentiate them according to specific quality characteristics, which are defined by different microbiota-driven reactions. Combining the above limitations, the scope of the present study, was to summarize the existing information toward three main issues. First, to assess the influence level of the diet type and grazing to rumen–GI tract, mammary gland, and udder microbiome formation in ruminants. Second, to discuss the factors affecting milk microbiota, as well as the effect of the endo-mammary route on milk microbial taxa. Lastly, to evaluate “milk microbiome” as a tool for product differentiation, according to origin, which will contribute to a more robust PDO and PGI labeling. Although the limitations are still a matter of fact (especially considering the sample collection, process, evaluation, and avoidance of its contamination), significant progress has been made, regarding the identification of the factors affecting dairy products’ microbiota and its core composition. In conclusion, although so far not totally efficient in dairy products molecular identification, with the progress in soil, water, plant, and animal host’s microbiota assembly’s characterization, microbiomics could provide a powerful tool for authentication and traceability of dairy products.

Keywords: sheep; goat; microbiome; authentication; PDO; PGI; fraud

1 Introduction

Ruminants represent an important part of global agrifood sector, contributing greatly to agroecology [1]. They are unique in their ability to convert inedible feed (plant cell wall carbohydrates) into high-valued protein such as meat and dairy products. Food by-products [2], forages [3], and non-protein nitrogen [4] can be efficiently included in their diet. It is estimated that the increase in livestock products demand will double by 2050, in line with the global population increase [5,6]. The livestock sector provides employment for more than one billion people while at the same time contributes to 40% of agricultural gross domestic product [7].

Ruminants, as mammalian herbivores are unable to produce cellulolytic or hemi-cellulolytic enzymes for degradation of ingested plant material. Their adaptation toward the degradation is based on the development of a symbiotic relationship with microbial communities (such as bacterial, fungi, and protozoa) for performing digestion [8]. Generally, diet and nutrition of ruminants has been proposed as the main driving force toward microbial community composition in rumen [9], affecting nutritional value of products [10]. Nevertheless, apart from the positive effects of rumen fermentation toward food production, it has also a negative impact toward environment as it is associated with emissions of greenhouse gases [11,12] and nitrogen [13]. As a result, many scientific papers focus on the understanding of rumen microbial composition, both for production improvement and reduction of environmental impact [14].

Recent evidence proposes that microorganisms inhabiting gut, namely “gut microbiome,” exhibit a main role toward host physiology [15]. Rumen forms an anaerobic environment, where a complex microbial community, consisting of bacteria, archaea, protozoa, and fungi, grow, with bacteria being the most abundant [9]. This complex rumen microbiota structure has been described as “the most elegant and highly evolved cellulose-digesting system in nature” [16]. For instance, 7,416 ruminal microbial taxa have been identified in lactating Holstein cows, with rumen microbiome being dominated by Bacteroidetes, Firmicutes, and Proteobacteria phyla, while the most abundant genera were Prevotella, Succiniclasticum, and Prevotellaceae UCG-001 [17]. Furthermore, a strong correlation has been demonstrated between abundance of various bacterial members of the rumen microbiome and physiological parameters of the host, such as milk yield and composition [18]. The organism welfare significantly influences the production rates as it modulates microbiological composition of the rumen [19].

Rumen–gut microbiome seems to be affected by many factors including age, diet, welfare, physiological condition, and surrounding environment. In addition, common mistakes, such as inadequate living conditions and improper diet, often take place during the intensified breeding of ruminants with possible negative impacts toward digestive tract microbiota leading to health status deprivation [20,21]. Apart from their substantial contribution toward health status, the proper composition and quantity of microbiota ensures homeostasis of organism, while in parallel influences the level of methane production [22,23]. Despite the fact that the two-way communication between the microflora of the gastrointestinal tract and the central nervous system is known [24], questions still remain regarding the existence of microbiota transfer through an entero-mammary route [25,26].

Apart from its multiple roles for the organism, microbiome is suggested to be responsible for the final quality characteristics of many agrifood products such as dairy and wine, on account of main microbiota-driven reactions. Recently, the microbiome has been used as a tool/marker for studying the geographic origin of various food products, including shellfish, such as mussels, oysters, and clams [27], Vitis vinifera through the investigation of soil and root-associated microbiome [28], while it has also revealed associations among different terroirs and wine varieties in Cyprus, from the stages of pre- until post-fermentation [29].

Contrariwise, for the dairy sector, microbiome investigation represents a more complex task. For instance, in cheese and especially for rennet-coagulated ones, the rennet, starter, and adjunct microbial cultures are added to accelerate ripening process. The majority of cheeses consist of four main ingredients: milk, rennet, microorganisms (usually starter cultures of lactic acid bacteria [LAB)]), and salt [30]. In dairy LAB two main biotechnological groups are included: starter LAB (SLAB) and non-starter LAB (NSLAB) [30]. The SLAB usually originates from natural starter cultures (NSC) and commercial starter cultures. These bacteria cultures are added in the beginning of the cheese making process and contribute to the pH reduction which helps in milk coagulation before proceeding to the next step where the addition of rennet or another coagulating agent takes place. Apart from that, SLAB also participates in the development of desirable flavor compounds in cheese [31]. NSCs are retained from back slopping, a technique where the whey from the successfully manufactured cheese batch can be retained for future use as the inoculum or starter culture for the next batch [32,33]. One of the main goals of NSC is to keep the genetic variability and the biodiversity of the microorganisms existing in cheese [34]. These actions affect nutritional, technological, and sensory properties of cheese, whereas they modify the final cheese microbiota profile as well [35]. Regarding milk, there are many factors that may affect its microbial composition, including host and environment, as well as the type of strategies followed for sampling, sequencing, and statistical analysis (i.e., various databases available), which may add bias and lead to distortion in milk microbiota analysis [25]. Therefore, from the limited so far existing studies, one interesting point inferred, is the effect of NSC on the final cheese’s microbiota, which in turns influence the flavor profile and can provide some information regarding its origin.

The development of powerful sequencing tools allows the successful investigation of the key factors affecting ruminant’s microflora and the role of microbiome toward health and production of the animal [19]. More specifically, the methods that are culture independent (i.e., 16S RNA sequencing ribosomal RNA, shotgun DNA-seq or RNA-seq which targets entire nucleotide sequence, and metatranscriptomics which enables the detection of changes in gene expression) are gaining more and more attention [19]. Additionally, microbiome has gained more attention recently as a tool for deep analysis, potential characterization, and authentication of several products [36]. Nevertheless, there is still no coherence in information regarding the influence of the ruminal, gut and mammary gland, and udder microbiota in the milk microbiota. Keeping this in mind, the present study attempts to summarize the current information toward three main components:

  1. to evaluate how the diet-type and grazing affect ruminant’s ruminal-intestinal microbiome,

  2. to explore if and how the ruminal-intestinal, mammary gland, and udder microflora affect milk, and lastly

  3. to examine if the produced milk can provide information regarding its origin by investigating its microbiota.

Hence, the main scope of the study is to connect the aforementioned components into a simpler question: Can the milk and/or cheese microbiome synthesis provide information regarding the origin of the dairy products and at what extent the animal’s diet type and composition affects it?

2 Influence of animal diet, grazing, and “freedom of choice” on rumen–GI tract and udder microbiota

The crucial role of diet in rumen and gut microbiota formation and activity is well documented [10,37] and may shift microbial community composition [38–42]. Alterations in the composition of rumen microbiota which regulate animal’s metabolism, impact host’s phenotype as well [43]. Feeding regimes and feed additives may influence the composition and functions of rumen’s microbiome. As a result, the impact of diet on the microbiome and hence to the product quality characteristics is of high interest. As reported by Wang et al. [44] artificial pasture grazing (an artificial grassland with Medicago sativa, Poa pratensis, and Bromus riparius was prepared) influenced muscle metabolites by modulating rumen microflora. Furthermore, high-energy diets are found to alter rumen microbiota composition, by increasing the abundance of Quinella, Ruminococcus 2, Eubacterium, Coprostanoligenes, and Succinivibrionaceae UCG-001, which are associated with carbohydrate metabolism in rumen [43], whereas indoor feeding regimes alter the abundance of rumen bacteria (Christensenellaceae R-7 group, [Eubacterium] Coprostanoligenes group, Methanobrevibacter, Ruminococcus 2, and Quinella) which influence muscle metabolism [45]. It can thus be concluded that host phenotype and metabolism can be altered according to different feeding regimes and dietary supplements. Based on the aforementioned studies, it is suggested that diet can affect rumen microbiota and product quality.

As the influence of diet on ruminal and intestinal microbiota is widely known, the dietary diversity in ruminants is receiving more and more attention [46–49]. In the context of dietary diversity, the “freedom of choice” regarding their diet and how this component can affect animal production is also included. It was observed that by choosing and mixing their diets, animals can reciprocate toward their needs, while at the same time they can self-medicate by consuming and digest plants with specific secondary compounds (PSC) that are associated with nutraceuticals, pharmaceuticals, and prophylactic benefits [50]. Dietary diversity in contrast to dietary monotony can improve ruminant’s welfare by enhancing hedonism and eudaimonism, while at the same time reduces stress levels [51]. Furthermore, diversity in dietary sources can influence the microbial-rumen–gut–brain axis, which is related with alterations in mood, emotions, cognition, and behavior both in humans [52] and farm animals [53]. Hence, dietary monotony can impact dietary preference and eating behavior in ruminants, whereas, on the other hand, grazing can lead to higher dietary diversity by providing animals the freedom of choice. In addition, grazing has a positive effect toward sustainable livestock production and animal welfare [54]. Although there are several studies on diet influence on ruminants’ microbiota [55] and microbial alterations over the transition from forage to concentrate diets [38,56], gaps still exist regarding the effect of the dietary diversity, achieved by grazing, on the microbiome. Belanche et al. [57] revealed that grazing may lead to an increase in the concentration, diversity, network, and abundance of key microbes involved in cellulolysis, lactate production, and methylotrophic archaea populations. Additionally, a core microbiota composition was observed which consisted of 34, 9, and 13 genera for bacteria, methanogens, and fungi, respectively, which were common among sheep independent of grazing or non-grazing [57].

Considering the strong effect of diet on rumen microbiome, it is not surprising that there are plenty of studies investigating the addition of many additives in order to control the gut–rumen axis complex composition. Under this prism, one of the main targeting actions that can cause manipulation of rumen microbiome is the improvement of the animal’s overall health. Animal health is in line with the better nutritional composition of animal products, regarding the lipid and fatty acid content/composition, as well as with the prevention of pathogen transfer in the food supply chain [15]. Regarding additives, plant-derived essential oils (EOs) obtained from the secondary metabolism of plants associated with the odor and spices of plants, often exhibit antimicrobial activity [58]. Depending on the dose and type of administration, EOs may alter gut microbiome, improve rumen fermentation efficiency, and support small ruminant-derived products. The impact on the abundance and composition of rumen’s microorganisms can in turn alter rumen function and green house gases production, by increasing ruminal absorption of total volatile fatty acid (VFA) concentration, better feed conversion ratios and improvement of gut immune responses, integrity of intestinal barrier, and growth performance rates [59].

Udder homeostasis is influenced by many management practices including housing conditions, nutritional status, and antimicrobial usage [60]. Among the nutritional factors, it was observed that feeding conditions, mainly indoor and grazing, pose a pivotal role toward the formation of the microbiome in mammary glands of dairy cows. More specifically, microbial diversity of udder skin tissues was higher during grazing compared to feeding period [61]. Furthermore, dietary supplementation with bamboo leaf extract was found to affect udder and milk microbiome in dairy cows, highlighting the important role of diet in udder microbiome [62].

Based on all the above information, it can be concluded that dietary interventions influence rumen and gut microbiota and may have an impact on dairy products. However, the influence of pasture grazing on milk microbiota and, subsequently, to the microbiota associated with the milk processed and final products, nutritional value, and consumer health represents a very challenging task [61]. These difficulties mostly concern environmental conditions, management practices, animal genetics, seasonality, hygiene, and feedstuffs [63].

3 Impact of rumen, gut, mammary gland, and udder microbiota on milk production and quality

Contrarily to the negative impacts of methane production, rumen and gut microbiomes contribute toward the break down and digestion of the feed consumed by the animal, controlling the production efficiency [64]. More specifically, the complex rumen microbiome facilitates the digestion of complex feed substrates that are high in fiber concentration, into VFA and microbial proteins. These microbial proteins are essential for animal growth, maintenance, and lactation processes [65]. Within the context of lactation, microbiota composition of rumen affects the variation of milk fatty acids in dairy cows [66]. Moreover, high-yielding Holstein cows possess significantly enriched ruminal microbiome, being associated with effective cellulose degradation and increased milk production, compared to low-yielding animals [67].

Apart from milk quality characteristics, the influence of the rumen–gut axis microbiome on milk microbiome still remains unexplored. Although occasional “core” microbiome patterns have been observed in rumen [10], efforts have been also carried out to characterize the potential core microbiota patterns in the mammary glands [25]. Despite the significant progress conducted, the assessment of the composition and abundance of microbial communities in milk still remains a challenging task, as there are many difficulties in the collection of a non-contaminated representative milk sample. Regarding human milk for instance, obstacles still exist in the collection of a sample with low bacterial biomass, non-contaminated with reagent DNA [68], while a standardized method is missing [69], leading to a wide variation in the results of microbiota estimation [68]. The main identified problems in human milk, which has been studied more extensively, may also be applicable to the study of the microbiome of ruminant milk. Indeed, based on previously published studies, similar issues have been reported in ruminant’s milk microbiota analysis [70–72].

Previous studies additionally indicated the significant influence of farming system on special bacterial traits observed in bovine milk, between indoor housing and pasture [61,73,74]. More specifically, grazing is proposed to increase counts of all bacterial categories [73] and the relative abundances of lactic acid and other probiotic bacteria (Propionibacteria and Bifidobacteria), while decreasing at the same time the abundances of spoilage bacteria [75]. Moreover, differences in farming systems and dairy facilities seem to influence the process of cheesemaking and final product quality, which can serve as an index of the origin of dairy products authentication [76]. However, considering that the investigation of milk microbiome represents a very complex task, apart from the farming system, it may be affected by the season and the lactation stage [75], environmental exposure [77], and contamination [78] making the authentication process even more difficult.

Among the environmental factors that seem to affect microbiota composition in milk is the geography. Kumar et al. [79] observed distinct microbiota patterns in human milk in women from different countries. Regarding bovine milk, factors associated with management practices and environment of the farm are proposed to affect milk microbiota patterns [80,81], whereas in other studies a core microbiome in bovine milk failed to be confirmed [82].

There are some hypotheses regarding the existence of an endogenous entero-mammary pathway by which some bacterial species may be transferred from gut to mammary gland and finally to the produced bovine milk [82,83]. This transfer can be possible considering the ability of some microbiomes to leave the intestinal environment, move through the lymph nodes and reach the mammary gland as a final destination. This endogenous route is supported by a plethora of studies regarding human [84–88], sows [89], cows [83], and mice, while more recent studies confirm this specific route with well-established evidence as reviewed by Selvamani et al. [90]. Nevertheless, the aforementioned route is still considered a theory with other studies expressing opposite opinions [26,60], claiming that the presence of gut-associated bacteria in milk microbiome does not necessarily confirm the endo-mammary route hypothesis, since these microorganisms are also present in the dairy environment [60].

Rumen–gut axis microbiome is strongly associated with productive performance and health status of animals (Figure 1). Based on evidence mentioned previously, there is a connection of gut and mammary gland microbiota through an endo-mammary route, which seems to have an influence on milk microbiome as well. Recently, dietary probiotics and other feed additives are gaining more and more attention toward the development of a rumen–gut favorable for the animals. By providing the animals with high-quality feedstuffs and by finding alternative solutions to avoid antibiotic administration, disruption of the normal microbiota in ruminant’s rumen and gut, and microbiota “dysbiosis” can be avoided [91].

Figure 1 The rumen–gut axis microbiome effect on animal health status. Pasture-grazing practices provide the animals with the “free of choice” option, while it may lead to microbiota “dysbiosis” reduction, by eliminating spoilage bacteria in the gut. Together with the inclusion of other feed additives such as probiotics the above components can contribute to improve of animal’s health.
Figure 1

The rumen–gut axis microbiome effect on animal health status. Pasture-grazing practices provide the animals with the “free of choice” option, while it may lead to microbiota “dysbiosis” reduction, by eliminating spoilage bacteria in the gut. Together with the inclusion of other feed additives such as probiotics the above components can contribute to improve of animal’s health.

4 From raw milk microbiome to cheese microbiome and its characteristics

Protected Designation of Origin (PDO) and Protected Geographical Indication (PGI) are quality labels established by the European Union for traditional products’ protection, which secure their economic benefits and origin by preventing commercial fraud (European Commission, 2013) [92]. Plenty of methodologies have been developed for dairy products characterization such as infrared spectroscopy [93], nuclear magnetic resonance spectroscopy [94], high-performance liquid chromatography [95], gas chromatography [96], solid phase microextraction, purge and trap [97], and more recently high throughput sequencing technologies [36].

Raw milk, by definition, is “the milk produced by animals (such as cows, sheep, goats, and buffaloes) which has not been heated above 40°C and subjected to any other treatment processes that have an equivalent effect on the milk-associated microbial community” [98]. There is strict E.U. regulation regarding PDO products for raw milk cheesemaking, as the unique microbial communities that exist in raw milk, provide special organoleptic characteristics in the fermented product in close association with the geographical area [99].

Microbiome has been used as a tool to distinguish geographical regions by giving different properties to various agricultural products, such as the final wine product, suggesting it as a potential biomarker [28,29]. Similarly, microbiome has been proposed as a marker for geographical origin identification of fresh seafood [27]. Similarly, it is of high interest to investigate the potential role of microbiome toward the traceability of dairy products.

In raw milk, there are many factors affecting resident microbial community (Section 3) (e.g., diet) [100]. For instance, dietary supplementation with omega-3 fatty acid has been proposed to reduce the pathogenic microbiota in the bovine milk [101]. Furthermore, the use of back-slopping is also beneficial for the raw milk cheeses. Back-slopping refers to the use of natural whey cultures (NWCs) that consist of fermented milk with a complex microbial community from the raw milk. Owing to their nature, NWCs are characterized of high variability according to different production sites and specific environmental factors [102]. Quality characteristics of dairy products, such as aroma, texture, and flavor are closely related to microbiome diversity and abundance, comprising the result of the substances produced from the chemical reactions of carbohydrates, proteins, and lipids [103–105].

Surprisingly, based on a comprehensive analysis of Italian raw milk cheese microbiota, organoleptic qualities of cheeses with the same PDO label differed between manufacturers. Resident microbial populations constitute a more robust factor that controls the final product’s quality characteristics. In line with this, it has been suggested that the PDO label should be revisited for a deeper understanding of the factors leading to final organoleptic characteristics of dairy products [99]. However, the above study received strict criticism regarding the experimental approach, the interpretation of results, and for citation of biased literature [106]. A recent study revealed that production origin can be correlated with the presence of specific metabolites in buffalo’s milk from PDO and non-PDO regions in Italy, with some specific metabolites detected in both the metabolome of unprocessed milk and corresponding mozzarella cheese in buffalo (i.e., talopyranose and N-acetyl glucosamine) [107]. These metabolites may also be the result of microbiome-driven chemical reactions, which however might need further investigation. An assay of the core microbiome and bacterial diversity in buffalo milk suggested a high farm management effect on the microbiome [108]. Farming conditions were also found to be the main driving force for the overall microbiome richness in cow’s milk [109]. In addition, when PDO feta cheeses from two geographic regions of Greece were analyzed, two distinctive microbiota fingerprints were observed. The starter culture bacteria species had, however, a strong influence on the final microbial composition [110]. Overall, the main factors responsible for cheese microbiota formation are secondary structuring factors, such as dairy product type, geographical area, and ripening practices, highlighting the contribution of biogeography and PDO-specific know-how of the final product [111].

By combining the strong influence of NWCs on cheesemaking and organoleptic characteristics of the final product with the unique characteristics of each NWCs, which is in strong association with a complex microbial community of raw milk from each region, it would be of great interest to evaluate if this could operate as a tool for origin identification. Toward this direction, starter cultures are pivotal for the final dairy product and the use of the selected starter/non-starter LAB cultures are occasionally proved to successfully stabilize PDO cheese production [112]. A very recent study proposed that PDO artisanal blue-veined cheeses are characterized by dominant components of the cheese microbiome that can provide very useful information for its authentication [113]. A summarization of the above applications is presented in Table 1.

Table 1

Scopes of the present study, supported by the corresponding findings

Applications Findings References
Application – factor 1
Diet-type and grazing influence on ruminant’s ruminal-intestinal microbiome

  • Feeding regimes and feed additives may influence the composition and functions of rumen’s microbiome

  • Artificial pasture grazing influenced muscle metabolites by modulating rumen microflora

  • High-energy diets are found to alter rumen microbiota composition associated with carbohydrate metabolism in rumen

  • Indoor feeding regimes can alter the abundance of rumen bacteria and influence muscle metabolism

  • Dietary diversity in contrast to dietary monotony can improve ruminant’s welfare by enhancing hedonism and eudaimonism, while at the same time reduces stress levels

  • EOs may alter gut microbiome, improve rumen fermentation efficiency, and support small ruminant-derived products

 [43]
[44]
[43]
[45]
[51]
[59]
Application – factor 2
Influence of the ruminal-intestinal, mammary gland and udder microflora on milk microbiota

  • There are some hypotheses regarding the existence of an endogenous entero-mammary pathway by which some bacterial species may be transferred from gut to mammary gland and finally to the produced bovine milk

  • Some microbiomes leave the intestinal environment, move through the lymph nodes and reach mammary gland as a final destination

  • Opposing opinions claim that the presence of gut-associated bacteria in milk microbiome does not necessarily confirm the endo-mammary route hypothesis, as these microorganisms are also present in the dairy environment

 [82]
[83]
[60]
Application – factor 3
Milk and dairy microbiota as a tool for authentication and traceability

  • NWCs are characterized of high variability according to different production sites and specific environmental factors

  • Farming conditions were also found to be the main driving force for the overall microbiome richness in cow’s milk

  • The starter culture bacteria species had, however, a strong influence on the final microbial composition

 [102]
[109]
[110]

5 Limitations and future perspectives

Loss in abundance and diversity of microbiome species is a common finding under several stressful conditions including diseases. Dietary substances provide different substrates for each microbial species enhancing its growth. A greater composition diversity diet may lead to a more diverse microbiome [114]. Furthermore, the diet type, apart from rumen–gut microbiome, also affects udder and mammary gland microbiota in ruminants. However, farming conditions seem to drastically affect raw milk composition [109]. In particular, individual farms [115,116] and different dairy plants lead to different production and quality efficiency of cheesemaking [117].

High-throughput sequencing technologies enhance the ability to track and understand the complex ecosystem of microorganisms in dairy products and thus improve their stability and quality through precision fermentation [118]. However, so far, there is a gap in identification of a core milk microbiome due to many existing difficulties. More specifically, there is a lack of standardized methods for collection, process, and evaluation of milk samples [26].

Pasteurization can influence autochthonous raw milk microbiota while inactivate microbial-produced antimicrobial compounds, by modestly affecting richness and significantly affecting composition [119]. The use of NWCs will provide characteristics that are unique for each region and are expected to further support the traceability of the final product by producing natural adjunct cultures [120], which is already found to be the most important factor for microbiome composition in the case of mozzarella PDO cheese [121].

Along with microclimate, native microbiota fauna in specific geographic regions, included in animals’ diet by grazing, constitute factors that also contribute to the unique characteristics of the final product with PDO and PGI labeling. However, regarding dairy products, there are also other significant components affecting the special organoleptic properties (Section 4). Thus, microbiome investigation, as a potential tool for identifying the product origin and to keep the quality and stability of the final product, will be beneficial for both consumers and producers. A deep understanding of all the aforementioned factors is expected to shed light on the milk microbiome composition and, in a more general sense, on cheese microbiota that give dairy products their uniqueness. More specifically, the investigation of the native fauna effect on mammary gland microbiome through the endo-mammary route, as well as to udder microbiome, which is in contact with native fauna via soil of each region is of great interest. This is especially important in regions characterized by high biodiversity, contributing to rumen–GI tract microbiome, often influenced by the farming conditions as well. In this context, the “free of choice” diet accomplished by grazing can provide access to animals in plants with secondary metabolites such as EO. For this reason, there are two possible advantages toward microbiome with the “free of choice” diet: (a) improvement of overall well-being and (b) self-medicate by consuming and digest plants with PSC that are associated with nutraceuticals, pharmaceuticals, and prophylactic properties. Thus, the potential elimination of the effect from other environmental factors such as the farming conditions, which also have an effect on the typicity of the final product, might lead to a more stable core microbiome of the dairy products for a specific geographical region. At the same time, common NWCs in each specific region that highly affect the fermentation for cheesemaking provide both higher quality and stability.

6 Conclusions

Although PDO and PGI products are characterized by high quality, they are non-standardized, while their organoleptic characteristics are influenced from many factors during milk production and processing. According to the proposed model of Figure 2, microbial populations existing in raw milk constitute one of the main driving factors for the chemical reactions leading to the formation of specific compounds responsible for the unique organoleptic characteristic of the final product. Among the factors contributing to the formation of milk microbiota the farming conditions, the udder microbiome of the animal, the rumen–GI tract microbiome, the animal’s physiological state, and diet are included. Regarding the rumen–GI tract microbiome contribution to the milk microbiota abundance and composition, it is mainly accomplished by an endo-mammary route, though the extent of the above contribution is still under investigation. Foraging and “free of choice” diet types, through increasing the overall wellbeing and eudemonic of the ruminants, have a substantial contribution to the complexity of animal’s microbiota regarding diversity and abundance microbiome increase (Figure 2). Furthermore, the type of grazing system affects the udder and teat microbiota which in turn, affect the microbiome in raw milk.

Figure 2 Proposed model factors affecting microbiome in small ruminants and its potential use in authentication. Implementation of pasture-grazing techniques provides the animals a “free of choice” option, and access to unique flora of each region. Apart from the specific unique characteristic of plants from each region, animals are also consuming the secondary metabolites of these plants. The above factors have been shown to influence the rumen and GI tract microbiome, as diet is one of the main driving factors shaping the formation and composition of the microbiome in these organs. Further, the rumen and GI tract microbiome can possibly influence udder and mammary gland microbiome through the endo-mammary route. The milk microbiome included in the milk from these animals will be influenced from all the previous components. Finally, with the addition of NWC – which has been found to be a major factor contributing to final cheese organoleptic characteristic – the dairy products will be characterized by specific microbiota diversity and composition operating as an additional tool for the PDO and PGI products identification.
Figure 2

Proposed model factors affecting microbiome in small ruminants and its potential use in authentication. Implementation of pasture-grazing techniques provides the animals a “free of choice” option, and access to unique flora of each region. Apart from the specific unique characteristic of plants from each region, animals are also consuming the secondary metabolites of these plants. The above factors have been shown to influence the rumen and GI tract microbiome, as diet is one of the main driving factors shaping the formation and composition of the microbiome in these organs. Further, the rumen and GI tract microbiome can possibly influence udder and mammary gland microbiome through the endo-mammary route. The milk microbiome included in the milk from these animals will be influenced from all the previous components. Finally, with the addition of NWC – which has been found to be a major factor contributing to final cheese organoleptic characteristic – the dairy products will be characterized by specific microbiota diversity and composition operating as an additional tool for the PDO and PGI products identification.

Thus, in conclusion, there are three key steps toward the precise geographic characterization of a dairy product. First, the diet type which leads to the formation of the unique microorganism populations in rumen–GI tract and in the udder of the ruminants. Second, the effect of this unique microbiota complex both from rumen–GI tract and from udder on the milk microbiome (considering the existence of the entero-mammary route). Lastly, the contribution of the above two components toward characterization of a raw milk that has been produced from animals having the same diet type from the same geographical region. The combination of the above three steps will lead to final products with specific characteristics that can be traced by investigating the microbiota pattern in the final product, giving information for the origin and avoiding food frauds. Generally, authentication of the origin of the dairy products is crucial, as sometimes the food labeling can be substituted or misrepresented, for achieving an economic gain. The above methodologies may contribute to the detection of possible food frauds by developing anti-fraud services [36,122]. Under this prism, particularly for dairy products under the PDO and the PGI nomination, molecular microbiome is suggested to be further investigated as a tool, in order to better characterize the products according to their organoleptic characteristics and origin.

  1. Funding information: The research is supported by the Administrative Region of Western Macedonia, Greece (Special Account for Research and Funds Project Number: 45291).

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and consented to its submission to the journal, reviewed all the results and approved the final version of the manuscript. M.V.A. conducted the literature research; M.V.A. and I.A.G. collected the information included in the study; M.V.A. wrote the first draft of the manuscript and prepared the figures; I.A.G. designed the study; I.A.G. and D.L. contributed to the interpretation of the finding; K.M. and M.V.A. guided the writing, D.L. and K.M. critically revised the manuscript; K.M. conceptualized the study; I.A.G. supervised the study and participated in figure preparation; K.M. and D.L. approved the final version; all authors reviewed the manuscript; M.V.A. formatted the study according to journal criteria.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

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Received: 2024-07-24
Revised: 2024-09-06
Accepted: 2024-09-16
Published Online: 2024-10-30

© 2024 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  208. Retraction
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https://doi.org/10.1515/biol-2022-0983
Keywords for this article
sheep; goat; microbiome; authentication; PDO; PGI; fraud
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Constitutive and evoked release of ATP in adult mouse olfactory epithelium
  3. LARP1 knockdown inhibits cultured gastric carcinoma cell cycle progression and metastatic behavior
  4. PEGylated porcine–human recombinant uricase: A novel fusion protein with improved efficacy and safety for the treatment of hyperuricemia and renal complications
  5. Research progress on ocular complications caused by type 2 diabetes mellitus and the function of tears and blepharons
  6. The role and mechanism of esketamine in preventing and treating remifentanil-induced hyperalgesia based on the NMDA receptor–CaMKII pathway
  7. Brucella infection combined with Nocardia infection: A case report and literature review
  8. Detection of serum interleukin-18 level and neutrophil/lymphocyte ratio in patients with antineutrophil cytoplasmic antibody-associated vasculitis and its clinical significance
  9. Ang-1, Ang-2, and Tie2 are diagnostic biomarkers for Henoch-Schönlein purpura and pediatric-onset systemic lupus erythematous
  10. PTTG1 induces pancreatic cancer cell proliferation and promotes aerobic glycolysis by regulating c-myc
  11. Role of serum B-cell-activating factor and interleukin-17 as biomarkers in the classification of interstitial pneumonia with autoimmune features
  12. Effectiveness and safety of a mumps containing vaccine in preventing laboratory-confirmed mumps cases from 2002 to 2017: A meta-analysis
  13. Low levels of sex hormone-binding globulin predict an increased breast cancer risk and its underlying molecular mechanisms
  14. A case of Trousseau syndrome: Screening, detection and complication
  15. Application of the integrated airway humidification device enhances the humidification effect of the rabbit tracheotomy model
  16. Preparation of Cu2+/TA/HAP composite coating with anti-bacterial and osteogenic potential on 3D-printed porous Ti alloy scaffolds for orthopedic applications
  17. Aquaporin-8 promotes human dermal fibroblasts to counteract hydrogen peroxide-induced oxidative damage: A novel target for management of skin aging
  18. Current research and evidence gaps on placental development in iron deficiency anemia
  19. Single-nucleotide polymorphism rs2910829 in PDE4D is related to stroke susceptibility in Chinese populations: The results of a meta-analysis
  20. Pheochromocytoma-induced myocardial infarction: A case report
  21. Kaempferol regulates apoptosis and migration of neural stem cells to attenuate cerebral infarction by O‐GlcNAcylation of β-catenin
  22. Sirtuin 5 regulates acute myeloid leukemia cell viability and apoptosis by succinylation modification of glycine decarboxylase
  23. Apigenin 7-glucoside impedes hypoxia-induced malignant phenotypes of cervical cancer cells in a p16-dependent manner
  24. KAT2A changes the function of endometrial stromal cells via regulating the succinylation of ENO1
  25. Current state of research on copper complexes in the treatment of breast cancer
  26. Exploring antioxidant strategies in the pathogenesis of ALS
  27. Helicobacter pylori causes gastric dysbacteriosis in chronic gastritis patients
  28. IL-33/soluble ST2 axis is associated with radiation-induced cardiac injury
  29. The predictive value of serum NLR, SII, and OPNI for lymph node metastasis in breast cancer patients with internal mammary lymph nodes after thoracoscopic surgery
  30. Carrying SNP rs17506395 (T > G) in TP63 gene and CCR5Δ32 mutation associated with the occurrence of breast cancer in Burkina Faso
  31. P2X7 receptor: A receptor closely linked with sepsis-associated encephalopathy
  32. Probiotics for inflammatory bowel disease: Is there sufficient evidence?
  33. Identification of KDM4C as a gene conferring drug resistance in multiple myeloma
  34. Microbial perspective on the skin–gut axis and atopic dermatitis
  35. Thymosin α1 combined with XELOX improves immune function and reduces serum tumor markers in colorectal cancer patients after radical surgery
  36. Highly specific vaginal microbiome signature for gynecological cancers
  37. Sample size estimation for AQP4-IgG seropositive optic neuritis: Retinal damage detection by optical coherence tomography
  38. The effects of SDF-1 combined application with VEGF on femoral distraction osteogenesis in rats
  39. Fabrication and characterization of gold nanoparticles using alginate: In vitro and in vivo assessment of its administration effects with swimming exercise on diabetic rats
  40. Mitigating digestive disorders: Action mechanisms of Mediterranean herbal active compounds
  41. Distribution of CYP2D6 and CYP2C19 gene polymorphisms in Han and Uygur populations with breast cancer in Xinjiang, China
  42. VSP-2 attenuates secretion of inflammatory cytokines induced by LPS in BV2 cells by mediating the PPARγ/NF-κB signaling pathway
  43. Factors influencing spontaneous hypothermia after emergency trauma and the construction of a predictive model
  44. Long-term administration of morphine specifically alters the level of protein expression in different brain regions and affects the redox state
  45. Application of metagenomic next-generation sequencing technology in the etiological diagnosis of peritoneal dialysis-associated peritonitis
  46. Clinical diagnosis, prevention, and treatment of neurodyspepsia syndrome using intelligent medicine
  47. Case report: Successful bronchoscopic interventional treatment of endobronchial leiomyomas
  48. Preliminary investigation into the genetic etiology of short stature in children through whole exon sequencing of the core family
  49. Cystic adenomyoma of the uterus: Case report and literature review
  50. Mesoporous silica nanoparticles as a drug delivery mechanism
  51. Dynamic changes in autophagy activity in different degrees of pulmonary fibrosis in mice
  52. Vitamin D deficiency and inflammatory markers in type 2 diabetes: Big data insights
  53. Lactate-induced IGF1R protein lactylation promotes proliferation and metabolic reprogramming of lung cancer cells
  54. Meta-analysis on the efficacy of allogeneic hematopoietic stem cell transplantation to treat malignant lymphoma
  55. Mitochondrial DNA drives neuroinflammation through the cGAS-IFN signaling pathway in the spinal cord of neuropathic pain mice
  56. Application value of artificial intelligence algorithm-based magnetic resonance multi-sequence imaging in staging diagnosis of cervical cancer
  57. Embedded monitoring system and teaching of artificial intelligence online drug component recognition
  58. Investigation into the association of FNDC1 and ADAMTS12 gene expression with plumage coloration in Muscovy ducks
  59. Yak meat content in feed and its impact on the growth of rats
  60. A rare case of Richter transformation with breast involvement: A case report and literature review
  61. First report of Nocardia wallacei infection in an immunocompetent patient in Zhejiang province
  62. Rhodococcus equi and Brucella pulmonary mass in immunocompetent: A case report and literature review
  63. Downregulation of RIP3 ameliorates the left ventricular mechanics and function after myocardial infarction via modulating NF-κB/NLRP3 pathway
  64. Evaluation of the role of some non-enzymatic antioxidants among Iraqi patients with non-alcoholic fatty liver disease
  65. The role of Phafin proteins in cell signaling pathways and diseases
  66. Ten-year anemia as initial manifestation of Castleman disease in the abdominal cavity: A case report
  67. Coexistence of hereditary spherocytosis with SPTB P.Trp1150 gene variant and Gilbert syndrome: A case report and literature review
  68. Utilization of convolutional neural networks to analyze microscopic images for high-throughput screening of mesenchymal stem cells
  69. Exploratory evaluation supported by experimental and modeling approaches of Inula viscosa root extract as a potent corrosion inhibitor for mild steel in a 1 M HCl solution
  70. Imaging manifestations of ductal adenoma of the breast: A case report
  71. Gut microbiota and sleep: Interaction mechanisms and therapeutic prospects
  72. Isomangiferin promotes the migration and osteogenic differentiation of rat bone marrow mesenchymal stem cells
  73. Prognostic value and microenvironmental crosstalk of exosome-related signatures in human epidermal growth factor receptor 2 positive breast cancer
  74. Circular RNAs as potential biomarkers for male severe sepsis
  75. Knockdown of Stanniocalcin-1 inhibits growth and glycolysis in oral squamous cell carcinoma cells
  76. The expression and biological role of complement C1s in esophageal squamous cell carcinoma
  77. A novel GNAS mutation in pseudohypoparathyroidism type 1a with articular flexion deformity: A case report
  78. Predictive value of serum magnesium levels for prognosis in patients with non-small cell lung cancer undergoing EGFR-TKI therapy
  79. HSPB1 alleviates acute-on-chronic liver failure via the P53/Bax pathway
  80. IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
  81. Baculovirus-mediated endostatin and angiostatin activation of autophagy through the AMPK/AKT/mTOR pathway inhibits angiogenesis in hepatocellular carcinoma
  82. Metformin mitigates osteoarthritis progression by modulating the PI3K/AKT/mTOR signaling pathway and enhancing chondrocyte autophagy
  83. Evaluation of the activity of antimicrobial peptides against bacterial vaginosis
  84. Atypical presentation of γ/δ mycosis fungoides with an unusual phenotype and SOCS1 mutation
  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
  86. Omega-3 fatty acids prevent gestational diabetes mellitus via modulation of lipid metabolism
  87. Refractory hypertension complicated with Turner syndrome: A case report
  88. Interaction of ncRNAs and the PI3K/AKT/mTOR pathway: Implications for osteosarcoma
  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
  96. Chemical composition’s effect on Solanum nigrum Linn.’s antioxidant capacity and erythrocyte protection: Bioactive components and molecular docking analysis
  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
  99. Laryngeal non-Hodgkin lymphoma: Report of four cases and review of the literature
  100. Clinical value of macrogenome next-generation sequencing on infections
  101. Overview of dendritic cells and related pathways in autoimmune uveitis
  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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