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Opinion

Preserving Microbial Biodiversity: The Case of Food-Associated Microorganisms

by
Spiros Paramithiotis
1,* and
Maria Dimopoulou
2,*
1
Laboratory of Food Process Engineering, Department of Food Science and Human Nutrition, Agricultural University of Athens, 75 Iera Odos St., 11855 Athens, Greece
2
Department of Wine, Vine and Beverage Sciences, School of Food Science, University of West Attica, 28 Ag. Spyridonos St., 12243 Athens, Greece
*
Authors to whom correspondence should be addressed.
Ecologies 2023, 4(3), 521-534; https://doi.org/10.3390/ecologies4030034
Submission received: 12 June 2023 / Revised: 29 July 2023 / Accepted: 7 August 2023 / Published: 8 August 2023
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Abstract

:
The preservation of microbial diversity is an issue not properly addressed, considering their role in shaping Earth into a habitable planet and their contribution to human well-being. The disturbance of their natural habitats triggers responses, which are reflected in the modification of microecosystem composition and metabolic activities. This is also the case with food-related microecosystems; changes in the growing environment, recorded as agricultural practices and manufacturing or storage conditions, result in similar alterations in the residing microcommunity. In fact, the principle aim of food microbiology is to favor the growth of health-promoting microorganisms and restrict the development of the ones that may negatively affect the quality of food or even cause infection or intoxication. Therefore, the current perspective is one-sided, disregarding issues of general interest, such as the preservation of actual biodiversity. The aim of the present article is to present the current food microbiology perspective, which is based on the different roles of food-related microbiota and highlight the need to move from an anthropocentric to a microbe-centric perception.

1. Introduction

Microbial biomass constitutes an important part of the total biomass of the organisms living on Earth and the largest source of biodiversity, whether this is considered using taxonomic or functional criteria [1]. Microorganisms hold very important roles: a. they participate in natural biogeochemical processes contributing to maintaining the functionality of ecosystems [2], b. through the colonization of the skin and the intestinal tract of humans and animals, they affect their homeostasis [3,4,5], c. the microbiome of the under- and above-ground parts of plants affects their growth and productivity [6], and d. their biotechnological exploitation, aiming to produce a wide range of value-added products, including food, has had a decisive role in increasing human well-being and life expectancy [7]. Despite their multiple important roles, conservation of their biodiversity is absent from the relevant discussions. The reason is the belief that microbial communities do not face the risk of limiting their biodiversity due to the absence of biogeographical restrictions on their distribution, the plasticity of their genomes, and their very short doubling time. However, this belief is based on doubtful generalizations. In fact, there is still no clear estimation of the true microbial biodiversity, nor is there a link between this biodiversity and the functionality of microorganisms within an ecosystem [8,9]. In addition, not all microorganisms have the same ability to adapt to changes in the environmental conditions they live in, with the risk of extinction of species as a result of disturbances in their natural environment being present [10]. The above demonstrates the importance of maintaining microbial biodiversity.
Food-related microorganisms are of particular interest. This interest is based on their ability to grow in commodities considered for human consumption and either participate in the production process or cause unwanted biotransformations. In addition, there are microorganisms that can cause foodborne infections or intoxications. The questions that arise are the following: is there a correlation between microbial biodiversity and food production, and would it be possible for a disturbance in the former to affect the latter, both in terms of security and quality? The aim of the present article is to briefly present the role of microorganisms in the food production chain and argue on the preservation of their biodiversity.

2. Food-Associated Microorganisms

Food-associated microorganisms can be distinguished into three categories, on the basis of their effect on food: a. beneficial microorganisms, which are those that either contribute to the production of food (e.g., fermented foods) or the dietary intake of their cells or metabolites may have a positive effect on consumer health (e.g., probiotic bacteria); b. spoilage microorganisms, the growth of which is likely to cause unwanted modifications in the physicochemical and/or organoleptic characteristics of food, to an extent that makes it no longer marketable; and c. pathogenic microorganisms, the dietary intake of which, or in some cases their metabolites, may cause significant health problems or even death. In the following paragraphs, a short description of the most important types of the above microorganisms is offered.

2.1. Beneficial Microorganisms

The production of fermented foods necessarily includes some type of microbial biotransformation. In this way, the raw materials, which are also suitable for human consumption, are transformed into another form with modified organoleptic characteristics, improved shelf-life and, in the majority of cases, nutritional value. Traditionally, such biotransformation is carried out by a microbial consortium, some members of which are present in a larger population and their metabolic activities have a determinative role in shaping the physicochemical and organoleptic properties of the final product. Three parameters determine the development of the microecosystem that carries out the desired bioconversion: the type and microbiological quality of the raw materials, the components added or released during the whole process and the environmental conditions during fermentation (e.g., temperature). The control of these parameters is a prerequisite for the effective control of the fermentation process [11,12,13].
Depending on the main metabolic end product, fermentation can be distinguished into three types: a. Acidic, when the final product is an organic acid (in the majority of cases lactic, acetic, or propionic acid); their accumulation leads to a decrease in the pH value and an increase in titratable acidity. b. Alkaline, when the end product is ammonia, the accumulation of which leads to an increase in the pH value, and c. alcoholic, when the final product is ethanol [14].
In Table 1, renowned products of lactic acid fermentation and the corresponding lactic acid bacteria that contribute to their production are shown. What is immediately noticeable is the multitude of genera and species that have been reported to participate in each microecosystem. For example, in the microbial community of wheat sourdoughs, the presence of 67 species of lactic acid bacteria, belonging to 18 genera, has been reported. Some of them seem to be adapted to the specific microenvironment, since they have the ability to use the available carbon and energy sources and are resistant to acidic environments, e.g., several strains of the species Fructilactobacillus sanfranciscensis.
Some others are distinguished only by their ability to resist an acidic environment, e.g., strains of the species Pediococcus pentosaceus. It is therefore understood that the capabilities that microorganisms have at the strain level determine their role in the developing microecosystem. Therefore, strains of Fr. sanfranciscensis are more likely to be used as a starter culture, as they are more likely to meet the technological requirements for such a product, while strains of other species (or even the same) are likely to be used as a secondary or adjunct culture to confer a specific characteristic (e.g., the production of a metabolite or an enzyme of technological or functional interest) [101]. The same applies to products whose production has been reported to involve the participation of acetic acid bacteria and yeasts [14].

2.2. Spoilage Microorganisms

Any deviation from the desired physicochemical and/or organoleptic properties of a food can be defined as ‘spoilage’. This deviation may be due to the growth of microorganisms and/or chemical reactions, which, in the majority of the cases, takes place during its storage. Especially regarding microbial spoilage, this can result from the growth of fungi, yeasts and/or bacteria, depending on the treatment the food has undergone (e.g., heat treatment, fermentation, etc.), the properties of the food (e.g., pH, water activity, the type and concentration of carbon and nitrogen sources, the presence of antimicrobial compounds, etc.) as well as the storage conditions (e.g., temperature, relative humidity, atmosphere, etc.). In the following paragraphs, some examples are briefly presented to facilitate an understanding of the diversity of the microorganisms that can cause such deviations.

2.2.1. Spoilage of Meat and Meat Products

Meat and its products are very rich in nutrients, such as glucose, proteins, amino acids, nucleotides, and fatty acids. The factors that determine the growth of microorganisms and, consequently, the extent of deviations from the desired organoleptic qualities are the characteristics of the product (e.g., pH value, water activity, and the concentration of sodium chloride and nitrite salts), the storage conditions (mainly temperature and atmosphere), as well as the initial microbial load. The latter is determined by the microbiological quality of the meat and other ingredients (e.g., spices and seasoning materials), the facilities, as well as the utensils used. Thus, meat kept at 4 °C under aerobic conditions may show surface exudation and mucus formation as well as off-odor development due to the growth of species of the genus Pseudomonas, most commonly P. fragi, P. fluorescens, and P. lundensis, if their population reaches 107–108 CFU/cm2. Meat preserved in modified-atmosphere packaging may undergo acidification and also develop off-odors due to the growth of lactic acid bacteria and/or Brochothrix thermosphacta. When storage takes place under vacuum, swelling of the package may be observed due to the production of CO2 by species of the genus Clostridium, such as Cl. algidicarnis, Cl. estertheticum, Cl. gasigenes, and Cl. putrefaciens. The development of off-odors may result from the growth of the above microorganisms as well as lactic acid bacteria and enterobacteria, such as Hafnia alvei, Serratia spp., Enterobacter spp., etc. [102,103,104]. Regarding cured meat products, i.e., products that have been treated with sodium chloride, nitrites, and a number of other ingredients and may be sold raw (e.g., bacon) or after heat treatment (e.g., sausages), their microbiological stability is ensured by the use of the above ingredients, a vacuum or modified-atmosphere packaging, as well as low storage temperature (4 °C). If the above conditions are fulfilled, physicochemical and/or organoleptic deviations, such as discoloration and acidification, which are accompanied by the expulsion of serum, may be observed due to the growth of lactic acid bacteria. If any of the above conditions are not met, the growth of yeasts, fungi, and bacteria may be observed [105,106]. Finally, in the case of fermented meat products, i.e., products made by using lactic acid bacteria, members of the family Micrococcaceae, and even yeasts and fungi, accurate control of their growth is required to avoid the possibility of deviations from the desired organoleptic characteristics. During storage, microbiological stability is ensured as already described. If the product is not packaged under vacuum, there is the possibility of surface growth of yeasts, fungi, and pseudomonads, resulting in numerous physicochemical and organoleptic deviations and even the production of mycotoxins. If the product is not acidified enough by lactic acid fermentation, enterobacteria can grow, which can cause discoloration and the development of off-odors [106].

2.2.2. Spoilage of Milk and Dairy Products

Milk is very rich in nutrients (such as lactose, proteins, fatty acids, minerals, and vitamins) and characterized by a slightly acidic pH. Thus, it is an ideal substrate for the growth of microorganisms. When the animal is healthy, the milk inside the udder is considered practically sterile. It is contaminated by microorganisms that settle on the external surface of the udder and come from the living environment of the animal, the utensils used, and the personnel. The most important spoilage microorganisms are psychrotrophic bacteria, which can grow at a storage temperature of less than 6 °C; heat-resistant bacteria, which can survive pasteurization; sporulating bacteria, whose spores are heat-resistant; as well as yeasts and fungi. The storage temperature of the product and the treatment it has undergone determine the types of microorganisms that can cause organoleptic and/or physicochemical deviations. Thus, raw milk kept at room temperature can support the growth of many microorganisms (such as lactic acid bacteria, coliforms, pseudomonads, species of the genera Clostridium, Bacillus, etc.), resulting in the appearance of many organoleptic deviations due to the production of proteolytic and lipolytic enzymes as well as organic acids. If the storage temperature is 3–7 °C, organoleptic deviations are usually due to the growth of species of the genus Pseudomonas. Pasteurization can reduce the population of bacteria, but not the heat-resistant ones (e.g., Bacillus, Clostridium, Corynebacterium, Enterococcus, Lactobacillus, and Streptococcus). In addition, it activates the germination of spores produced by sporulating bacteria (Bacillus and Clostridium). Thus, if there is no contamination of the milk after pasteurization, all the above microorganisms can grow, causing acidification, and through their proteolytic and lipolytic enzymes, a multitude of organoleptic deviations. If contamination occurs after pasteurization, other bacteria such as Pseudomonas, coliforms, etc., can be added to the above species. As far as cheeses are concerned, the factors that affect microbiological stability are cheese-making conditions, water activity, pH value, sodium chloride content, the characteristics of the starter culture, as well as the storage conditions. Depending on the above, the growth of Gram-negative psychrotrophic bacteria, lactic acid bacteria, as well as yeasts and fungi may result in a series of deviations such as mucus production, discoloration, putrid smell and taste, etc. [107,108].

2.2.3. Spoilage of Fruits and Vegetables

The surface microbiome of plant material depends upon many factors, such as the produce type, the farming practices, the soil and its amendments, the irrigation water, as well as the occurrence of domestic or wild animals [109,110,111]. Generally, the surface of fresh fruits and vegetables is covered by the cuticle, a surface layer of cells that protects the internal tissues from microbial attack. Thus, when the surface is not injured, the microorganisms that may reside on it lack the nutrients that are essential for their growth, since it is not possible for them to diffuse from the cells of the internal tissues. The microbiota of intact plant surfaces may consist of molds and yeasts, such as members of the genera Aspergillus, Eurotium, Penicillium, Rhizopus, Candida, Debaryomyces, and Pichia as well as bacteria (mostly Gram-negative, such as pseudomonads). This microecosystem may be enriched by human pathogenic microorganisms upon improper agricultural practices [110]. Injury can be caused by factors that are not easy to control, such as birds, insects, sand carried by the wind, friction between plant surfaces, etc. In places where plant tissue has been injured, there is a diffusion of nutrients to the outside, and the proliferation of microorganisms, including phytopathogenic fungi and bacteria, is possible. The latter, in turn, produce a number of enzymes such as pectinases and cellulases that degrade the main structural components of plant cells, namely pectins and celluloses, and ultimately, the local availability of nutrients increases. Injuries can also occur during harvesting or processing as a result of poor handling. Based on the above, the alteration of plant tissues can result from the following: a. phytopathogenic fungi and bacteria, the growth of which is accompanied by symptoms characteristic of the type of microorganism that is developed, e.g., soft rot can be caused in green beans by species of the genus Rhizopus, and in vegetables by species of the genera Pseudomonas, Bacillus, Clostridium, and Erwinia, while black rot can be caused in cabbage by Xanthomonas campestris, onions by Aspergillus niger, and potatoes by Erwinia carotovora; b. non-phytopathogenic microorganisms, which multiply occasionally depending on the availability of nutrients [112].

2.3. Pathogenic Microorganisms

Pathogenic microorganisms are the ones that can cause infection or poisoning upon ingestion of their cells or some of their toxic metabolites, respectively. These microorganisms contaminate food at some stage of its preparation and have the ability to multiply, depending on the food’s properties (e.g., pH, nutrients, water activity, etc.) and storage conditions (e.g., temperature, atmosphere, etc.). In the European Union, 98.8% of foodborne infections reported in 2019 were confirmed to be caused by Campylobacter spp. (220,682 cases), Salmonella spp. (87,923 cases), shiga-toxin-producing Escherichia coli (STEC) (7775 cases), Yersinia spp. (6961 cases), and Listeria monocytogenes (2621 cases) [113]. The most frequent foodborne infection in the European Union since 2005 is the one caused by the microorganism Campylobacter spp. The most frequent sources of infection are products made with unpasteurized milk and poultry meat (mainly chicken). The mortality of the infection caused by this microorganism is low at only 0.03%. Salmonellosis is the second-most-common foodborne infection. The majority of infections are caused by strains of the Salmonella Enteritidis serotype. The most frequent sources of infection are eggs and their products, bakery products, as well as pork and its products. The mortality of Salmonellosis amounts to 0.22%. Listeriosis is the most important foodborne infection in the European Union due to the very high mortality rate, which, in 2019, amounted to 17.6%. The most common source of infection was meat products. Infection caused by strains of STEC has most frequently been caused by the consumption of beef and beef products, milk, and water (both from water supply networks and from wells). The mortality rate of the infection is 0.21% [113].

3. The Concept of Native Food Microbiota

The concept of native food microbiota is synonymous with the concept of microbiome [114]. Both terms define the microbial community that lives in a clearly defined habitat, which has distinct physicochemical properties. This definition indicates that all microorganisms that make up this community interact both with each other and with the environment. A consequence of these interactions is the dynamic nature of the microecosystem that is created. Due to this dynamic nature, the microbial species that make up a microbiome are not always the same but can be classified into two categories: those that form the core of the microbiome in question and those that are occasionally found in it. The core members justify their persistence in the capability of using the available nutrients and energy sources, under the specific conditions, as well as in their ability to adapt to changes in physicochemical parameters, which usually result from microbial metabolism. In contrast, the microorganisms that occasionally participate in the microbiome are usually distinguished only by their ability to adapt to the adverse conditions created by microbial metabolism. To better understand this difference, Figure 1 and Figure 2 are listed. Figure 1 shows the lactic acid bacteria microbiome of 439 traditional wheat sourdough samples from European countries, the USA, China, and Japan [26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61]. Despite the differences in the raw materials used (in the sense of wheat variety and related cultivation conditions) and in the production process, the core of the microbiome consists of strains of the species Fr. sanfranciscensis, Lactiplantibacillus plantarum, and Levilactobacillus brevis. Additionally, a variety of lactic acid bacteria (64 different species) have been found to occasionally inhabit this particular microecosystem. Figure 2 shows the lactic acid bacteria microbiome of 38 samples of traditional rye sourdoughs from European countries and the USA [45,46,47,57,58,59,60,61,62,63,64,65,66,67,68,69]. In this case, the species Fr. sanfranciscensis, Lp. plantarum, Limosilactobacillus pontis, and Lv. brevis appear to form the core of the microbiome. An abundance of lactic acid bacteria (39 different species) can also occasionally live in this particular microecosystem. In both cases, the existence of the members of the core microbiome, individually or in combination, has been reported in the majority of the samples. However, their absence has also been reported [28,45,59,69], indicating that these products can be made without their contribution. This seems also to be the case with dairy products [115,116,117].
The concept of the microbiome and the distinction between the microorganisms that participate in core and occasional ones also exist in the case of the spoilage microbiota. Thus, the composition of the spoiling microbiome depends on the type of food, the processing it has undergone, and the storage conditions. For example, hundreds of bacterial species can grow in fresh meat kept at a temperature of 0–8 °C, but only a small percentage (less than 10%) can be considered responsible for the creation of the phenotype (off-odors, discoloration, etc.), which is considered by humans as spoilage. These species can multiply to such an extent that the effect of their metabolism is perceived by humans [102]. Thus, the species Pseudomonas spp., Acinetobacter spp., Brochothrix spp., Shewanella spp., and Aeromonas spp. are considered the main spoilage microorganisms of fresh meat kept aerobically at a temperature of 0–8 °C, while the species Weissella spp., Leuconostoc spp., Bacillus spp., and Clostridium spp. are considered those of fresh meat preserved anaerobically. In the case of fish, the microorganisms Shewanella putrefaciens and Pseudomonas spp. are considered the main spoilage microorganisms of fresh catches from temperate climates preserved aerobically on ice, while the microorganism Photobacterium phosphoreum is considered the main spoilage microorganism of the same catches if they are preserved in a modified atmosphere [118].
The above demonstrates that the food microbiome is more influenced by the types of raw materials and the conditions of production and/or storage and less by their geographical origin. Therefore, any restriction in the biodiversity of the related microorganisms seems highly unlikely to affect food production and storage.
However, there are strong indications that the disturbance of microbial natural habitats triggers a response, at least as far as terrestrial, oceanic, and urban ecosystems are concerned [119]. This response may also affect microbial physiology and biodiversity [120,121]. In the case of food-associated microorganisms, modification of the native microbiota composition as a response to the modification of their natural habitats has also been experienced. An example is the study by Lhomme et al. [122], according to which the use of organically grown wheat and rye flour resulted in sourdoughs dominated by Kazachstania yeasts and not Saccharomyces cerevisiae, which has been reported to dominate sourdoughs from around the world. In contrast, no change was observed in the prevailing bacterial species, and the bacterium Fr. sanfranciscensis was reported to form the core of the associated microbiome. However, this change did not seem to affect the technological properties of these products and their use in bakeries, while there was no mention of a change in their nutritional value or functional properties related to this change. In addition, the modification of the dominant populations rather than a loss of biodiversity was reported in this study. Another example, with significant economic implications, comes from the field of viticulture/enology. There are many regions with a cold climate where viticulture is practiced, e.g., the regions of Mosel and Baden in Germany, Innsbruck in Austria, Champagne in France, Christchurch in New Zealand, Hobart in Australia, Michigan and Oregon in the USA, Okanagan in Canada, etc. [123,124]. In these areas, the average temperature during the growing season (April to October) varies between 13 and 15 °C, while the average temperature during the winter is around −18 °C. Under these conditions, viticulture is based on the use of suitable varieties (e.g., Riesling, Chardonnay, Pinot Noir, Sauvignon Blanc, etc.), in which the ripening of the grapes can take place in a comparatively shorter period of time and at lower temperatures. The climate change that the planet is experiencing has significant implications for viticulture. The increase in temperature (0.85 °C from 1880 to 2012), which is more intense in regions with a cold climate (1.7 °C from 1948 to 2016 in Canada), as well as the change in the intensity and frequency of precipitation, results in the earlier ripening of grapes, which contain more sugars and fewer organic acids, and thus higher pH value [125]. The consequence of this is a change in the typical characteristics of the wines produced in these regions. From a cultivation perspective, these can be addressed through viticultural practices and the use of other varieties. From a microbiological point of view, these changes are very likely to affect the composition of the microbial community, both the one that resides on the surface of the fruits and the one that grows during winemaking. Unfortunately, there are no studies that investigate the changes in the microbiome and relate them to climate change. Due to its great economic importance, research has mainly focused on addressing the problem through the use of appropriate strains of microorganisms, aiming to restore the typical characteristics of the wines produced [126].
Regarding pathogenic microorganisms, several studies have correlated the environmental changes triggered by global warming with the occurrence and virulence of foodborne pathogens [127]. However, no such correlations have been made so far regarding their biodiversity. Another issue that deserves special attention is the fact that specific microorganisms have been isolated from specific habitats. Such is the case of the species belonging to the newly designated genus Bombilactobacillus, which have been isolated from the stomach and the hindgut of honeybees and bumblebees [128] and seem to promote their intestinal health [129], with possible effects on the quality of honey. In this case, it is very likely that a loss of biodiversity will be evident, following the reduction in the honeybee population [130].
The lack of data regarding the fluctuation of biodiversity of food-associated microorganisms resulting from the disturbance of their natural habitats is evident. The conceptual and technological advances of recent years, especially in the field of molecular biology, have allowed the fast and accurate estimation of biodiversity, either measured as alpha, beta, and gamma or as type-one, -two, -three, and -four diversity [131]. Therefore, verification of the notion that a possible biodiversity reduction is unlikely to affect food production and storage is feasible. Such studies should address all steps of the food production chain and include data referring to environmental conditions, such as temperature, humidity, environmental pollutants, etc. The study by Cibrario et al. [132] could serve as an example. In that study, the increase in triploid Brettanomyces bruxellensis groups during recent decades was reported and attributed to the attempt of the yeast to adapt to winemaking conditions, possibly including climate change. Ultimately, an accumulation of such data would facilitate the development of meaningful correlations as well as the adoption of preventive or remediating strategies [133].

4. Conclusions

The anthropocentric character of the above view is clear: microorganisms are classified according to their usefulness in food preparation and according to the effects that their ingestion can have on human health. Therefore, there is a constant effort to eliminate spoilage and pathogenic microorganisms and facilitate the development of beneficial ones, through processing and preservation methods. The risk of a loss of biodiversity of food-associated microorganisms upon the disturbance of their natural habitat seems to exist. However, the current food-microbiological perspective is one-sided and focuses only on issues that may have a direct effect on food production and quality, directing our attention to the tip of the iceberg and ignoring the big picture. The possibility of a biodiversity loss of food-related microorganisms should trigger studies assessing the possible effects throughout the food production chain. Therefore, the need to adopt a holistic perspective in future studies is imperative in order to effectively address this issue.

Author Contributions

Conceptualization, S.P.; investigation, S.P. and M.D.; resources, S.P. and M.D.; data curation, S.P. and M.D.; writing—original draft preparation, S.P. and M.D.; writing—review and editing, S.P. and M.D.; visualization, S.P. and M.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Escalas, A.; Hale, L.; Coordeckers, J.W.; Yang, Y.; Firestone, M.K.; Alvarez-Cohen, L.; Zhou, J. Microbial functional diversity: From concepts to applications. Ecol. Evol. 2019, 9, 12000–12016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Basu, S.; Kumar, G.; Chhabra, S.; Prasad, R. Role of soil microbes in biogeochemical cycle for enhancing soil fertility. In New and Future Developments in Microbial Biotechnology and Bioengineering. Phytomicrobiome for Sustainable Agriculture; Verma, J.P., Macdonald, C.A., Gupta, V.K., Podile, A.R., Eds.; Elsevier B.V.: Amsterdam, The Netherlands, 2021; pp. 149–157. [Google Scholar]
  3. McKenney, E.A.; Koelle, K.; Dunn, R.R.; Yoder, A.D. The ecosystem services of animal microbiomes. Mol. Ecol. 2018, 27, 2164–2172. [Google Scholar] [CrossRef] [PubMed]
  4. Byrd, A.L.; Belkaid, Y.; Serge, J.A. The human skin microbiome. Nat. Rev. Microbiol. 2018, 16, 143–155. [Google Scholar] [CrossRef] [PubMed]
  5. Lloyd-Price, J.; Abu-Ali, G.; Huttenhower, C. The healthy human microbiome. Genome Med. 2016, 8, 51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Trivedi, P.; Leach, J.E.; Tringe, S.G.; Sa, T.; Singh, B.K. Plant-microbiome interactions: From community assembly to plant health. Nat. Rev. Microbiol. 2020, 18, 607–621. [Google Scholar] [CrossRef] [PubMed]
  7. Bull, A.T.; Goodfellow, M.; Slater, J.H. Biodiversity as a source of innovation in biotechnology. Annu. Rev. Microbiol. 1992, 46, 219–252. [Google Scholar] [CrossRef]
  8. Bodelier, P.L.E. Towards understanding, managing, and protecting microbial ecosystems. Front. Microbiol. 2011, 2, 80. [Google Scholar] [CrossRef] [Green Version]
  9. Vuong, P.; Chong, S.; Kaur, P. The little things that matter: How bioprospecting microbial biodiversity can build towards the realization of United Nations Sustainable Development Goals. npj Biodivers. 2020, 1, 4. [Google Scholar] [CrossRef]
  10. Colwell, R.R. Microbial diversity: The importance of exploration and conservation. J. Ind. Microbiol. Biotechnol. 1997, 18, 302–307. [Google Scholar] [CrossRef]
  11. Drosinos, E.H.; Paramithiotis, S. Trends in lactic acid fermentation. In Food Microbiology Research Trends; Palino, M.V., Ed.; Nova Publishers: Hauppauge, NY, USA, 2007; pp. 39–92. [Google Scholar]
  12. Paramithiotis, S.; Drosinos, E.H.; Sofos, J.; Nychas, G.J.E. Fermentation: Microbiology and biochemistry. In Handbook of Meat Processing; Toldra, F., Ed.; Springer: New York, NY, USA, 2010; pp. 185–198. [Google Scholar]
  13. Paramithiotis, S.; Papoutsis, G.; Drosinos, E.H. Lactic acid fermentation of fruits and vegetables; an overview. In Lactic Acid Fermentation of Fruits and Vegetables; Paramithiotis, S., Ed.; CRC Science: Cleveland, OH, USA, 2017; pp. 1–18. [Google Scholar]
  14. Paramithiotis, S. Microorganisms associated with food fermentation. In Bioactive Compounds in Fermented Foods: Health Aspects; Rai, A.K., Anu Appaiah, K.A., Eds.; CRC Press: Cleveland, OH, USA, 2021; pp. 3–47. [Google Scholar]
  15. Lee, J.S.; Heo, G.Y.; Lee, J.W.; Oh, Y.J.; Park, J.A.; Park, Y.H.; Pyun, Y.R.; Ahn, J.S. Analysis of kimchi microflora using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 2005, 102, 143–150. [Google Scholar] [CrossRef]
  16. Cho, J.; Lee, D.; Yang, C.; Jeon, J.; Kim, J.; Han, H. Microbial population dynamics of kimchi, a fermented cabbage product. FEMS Microbiol. Lett. 2006, 257, 262–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Chang, H.W.; Kim, K.H.; Nam, Y.D.; Roh, S.W.; Kim, M.S.; Jeon, C.O.; Oh, H.M.; Bae, J.W. Analysis of yeast and archaeal population dynamics in kimchi using denaturing gradient gel electrophoresis. Int. J. Food Microbiol. 2008, 126, 159–166. [Google Scholar] [CrossRef] [PubMed]
  18. Jung, J.Y.; Lee, S.H.; Jin, H.M.; Hahn, Y.; Madsen, E.L.; Jeon, C.O. Metatranscriptomic analysis of lactic acid bacterial gene expression during kimchi fermentation. Int. J. Food Microbiol. 2013, 163, 171–179. [Google Scholar] [CrossRef] [PubMed]
  19. Jeong, S.H.; Jung, J.Y.; Lee, S.H.; Jin, H.M.; Jeon, C.O. Microbial succession and metabolite changes during fermentation of dongchimi, traditional Korean watery kimchi. Int. J. Food Microbiol. 2013, 164, 46–53. [Google Scholar] [CrossRef] [PubMed]
  20. Jeong, S.H.; Lee, S.H.; Jung, J.Y.; Choi, E.J.; Jeon, C.O. Microbial succession and metabolite changes during long-term storage of kimchi. J. Food Sci. 2013, 78, M763–M769. [Google Scholar] [CrossRef] [PubMed]
  21. Hong, Y.; Yang, H.S.; Chang, H.C.; Kim, H.Y. Comparison of bacterial community changes in fermenting kimchi at two different temperatures using a denaturing gradient gel electrophoresis analysis. J. Microbiol. Biotechnol. 2013, 23, 76–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Chang, H.C. Healthy and safe Korean traditional fermented foods: Kimchi and chongkukjang. J. Ethn. Foods 2018, 5, 161–166. [Google Scholar] [CrossRef]
  23. Harris, L.J. The Microbiology of vegetable fermentations. In Microbiology of Fermented Foods; Wood, B.J.B., Ed.; Blackie Academic and Professional: London, UK, 1998; pp. 45–72. [Google Scholar]
  24. Barrangou, R.; Yoon, S.S.; Breidt, F., Jr.; Fleming, H.P.; Klaenhammer, T.R. Identification and characterization of Leuconostoc fallax strains isolated from an industrial sauerkraut fermentation. Appl. Environ. Microbiol. 2002, 68, 2877–2884. [Google Scholar] [CrossRef] [Green Version]
  25. Beganovic, J.; Kos, B.; Lebos Pavunc, A.; Uroic, K.; Jokic, M.; Suskovi, J. Traditionally produced sauerkraut as source of autochthonous functional starter cultures. Microbiol. Res. 2014, 169, 623–632. [Google Scholar] [CrossRef]
  26. Gobbetti, M.; Corsetti, A.; Rossi, J.; La Rosa, F.; De Vincenzi, S. Identification and clustering of lactic acid bacteria and yeasts from wheat sourdoughs of central Italy. Ital. J. Food Sci. 1994, 6, 85–94. [Google Scholar]
  27. Garofalo, C.; Silvestri, G.; Aquilanti, L.; Clementi, F. PCR-DGGE analysis of lactic acid bacteria and yeast dynamics during the production processes of three varieties of Panettone. J. Appl. Microbiol. 2008, 105, 243–254. [Google Scholar] [CrossRef] [PubMed]
  28. Corsetti, A.; Lavermicocca, P.; Morea, M.; Baruzzi, F.; Tosti, N.; Gobbetti, M. Phenotypic and molecular identification and clustering of lactic acid bacteria and yeasts from wheat (species Triticum durum and Triticum aestivum) sourdoughs of southern Italy. Int. J. Food Microbiol. 2001, 64, 95–104. [Google Scholar] [CrossRef] [PubMed]
  29. Randazzo, C.L.; Heilig, H.; Restuccia, C.; Giudici, P.; Caggia, C. Bacterial population in traditional sourdough evaluated by molecular methods. J. Appl. Microbiol. 2005, 99, 251–258. [Google Scholar] [CrossRef] [PubMed]
  30. Zotta, T.; Piraino, P.; Parente, E.; Salzano, G.; Ricciardi, A. Characterization of lactic acid bacteria isolated from sourdoughs for Cornetto, a traditional bread produced in Basilicata (Southern Italy). World J. Microbiol. Biotechnol. 2008, 24, 1785–1795. [Google Scholar] [CrossRef]
  31. Iacumin, L.; Cecchini, F.; Manzano, M.; Osualdini, M.; Boscolo, D.; Orlic, S.; Comi, G. Description of the microflora of sourdoughs by culture-dependent and culture independent methods. Food Microbiol. 2009, 26, 128–135. [Google Scholar] [CrossRef]
  32. Osimani, A.; Zannini, E.; Aquilanti, L.; Mannazzu, I.; Comitini, F.; Clementi, F. Lactic acid bacteria and yeasts from wheat sourdoughs of the Marche Region. Ital. J. Food Sci. 2009, 21, 269–286. [Google Scholar]
  33. Minervini, F.; Di Cagno, R.; Lattanzi, A.; De Angelis, M.; Antonielli, L.; Cardinali, G.; Cappelle, S.; Gobbetti, M. Lactic acid bacterium and yeast microbiotas of 19 sourdoughs used for traditional/typical Italian breads: Interactions between ingredients and microbial species diversity. Appl. Environ. Microbiol. 2012, 78, 1251–1264. [Google Scholar] [CrossRef] [Green Version]
  34. Reale, A.; Tremonte, P.; Succi, M.; Sorrentino, E.; Coppola, R. Exploration of lactic acid bacteria ecosystem of sourdoughs from the Molise region. Ann. Microbiol. 2005, 55, 17–22. [Google Scholar]
  35. Ricciardi, A.; Parente, E.; Piraino, P.; Paraggio, M.; Romano, P. Phenotypic characterization of lactic acid bacteria from sourdoughs for Altamura bread produced in Apulia (Southern Italy). Int. J. Food Microbiol. 2005, 98, 63–72. [Google Scholar] [CrossRef]
  36. Reale, A.; Di Renzo, T.; Succi, M.; Tremonte, P.; Coppola, R.; Sorrentino, E. Identification of lactobacilli isolated in traditional ripe wheat sourdoughs by using molecular methods. World J. Microbiol. Biotechnol. 2011, 27, 237–244. [Google Scholar] [CrossRef]
  37. Yagmur, G.; Tanguler, H.; Leventdurur, S.; Elmaci, E.U.; Francesca, N.; Settanni, L.; Moschetti, G.; Erten, H. Identification of predominant lactic acid bacteria and yeasts of Turkish sourdoughs and selection of starter cultures for liquid sourdough production using different flours and dough yields. Pol. J. Food Nutr. Sci. 2016, 66, 99–107. [Google Scholar] [CrossRef] [Green Version]
  38. Arena, M.P.; Russo, P.; Spano, G.; Capozzi, V. Exploration of the microbial biodiversity associated with north Apulian sourdoughs and the effect of the increasing number of inoculated lactic acid bacteria strains on the biocontrol against fungal spoilage. Fermentation 2019, 5, 97. [Google Scholar] [CrossRef] [Green Version]
  39. Sevgili, A.; Erkmen, O.; Koçaslan, S. Identification of lactic acid bacteria and yeasts from traditional sourdoughs and sourdough production by enrichment. Czech J. Food Sci. 2021, 39, 312–318. [Google Scholar] [CrossRef]
  40. Valmorri, S.; Settanni, L.; Suzzi, G.; Gardini, F.; Vernocchi, P.; Corsetti, A. Application of a novel polyphasic approach to study the lactobacilli composition of sourdoughs from the Abruzzo region (central Italy). Lett. Appl. Microbiol. 2006, 43, 343–349. [Google Scholar] [CrossRef]
  41. Palomba, S.; Blaiotta, G.; Ventorino, V.; Saccone, A.; Pepe, O. Microbial characterization of sourdough for sweet baked products in the Campania region (southern Italy) by a polyphasic approach. Ann. Microbiol. 2011, 61, 307–314. [Google Scholar] [CrossRef]
  42. Zhang, J.; Liu, W.; Sun, Z.; Bao, Q.; Wang, F.; Yu, J.; Chen, W.; Zhang, H. Diversity of lactic acid bacteria and yeasts in traditional sourdoughs collected from western region in Inner Mongolia of China. Food Control 2011, 22, 767–774. [Google Scholar] [CrossRef]
  43. Palla, M.; Cristani, C.; Giovannetti, M.; Agnolucci, M. Identification and characterization of lactic acid bacteria and yeasts of PDO Tuscan bread sourdough by culture dependent and independent methods. Int. J. Food Microbiol. 2017, 250, 19–26. [Google Scholar] [CrossRef]
  44. Reale, A.; Di Renzo, T.; Boscaino, F.; Nazzaro, F.; Fratianni, F.; Aponte, M. Lactic acid bacteria biota and aroma profile of Italian traditional sourdoughs from the Irpinian area in Italy. Front. Microbiol. 2019, 10, 1621. [Google Scholar] [CrossRef] [Green Version]
  45. Scheirlinck, I.; Van der Meulen, R.; Van Schoor, A.; Vancanneyt, M.; De Vuyst, L.; Vandamme, P.; Huys, G. Influence of geographical origin and flour type on diversity of lactic acid bacteria in traditional Belgian sourdoughs. Appl. Environ. Microbiol. 2007, 73, 6262–6269. [Google Scholar] [CrossRef] [Green Version]
  46. Scheirlinck, I.; Van der Meulen, R.; Van Schoor, A.; Vancanneyt, M.; De Vuyst, L.; Vandamme, P.; Huys, G. Taxonomic structure and stability of the bacterial community in Belgian sourdough ecosystems as assessed by culture and population fingerprinting. Appl. Environ. Microbiol. 2008, 74, 2414–2423. [Google Scholar] [CrossRef] [Green Version]
  47. Lhomme, E.; Lattanzi, A.; Xavier, D.; Minervini, F.; De Angelis, M.; Lacaze, G.; Onno, B.; Gobbetti, M. Lactic acid bacterium and yeast microbiotas of sixteen French traditional sourdoughs. Int. J. Food Microbiol. 2015, 215, 161–170. [Google Scholar] [CrossRef] [PubMed]
  48. Pino, A.; Russo, N.; Solieri, L.; Sola, L.; Caggia, C.; Randazzo, C.L. Microbial consortia involved in traditional Sicilian sourdough: Characterization of lactic acid bacteria and yeast populations. Microorganisms 2022, 10, 283. [Google Scholar] [CrossRef]
  49. Ferchichi, M.; Valcheva, R.; Oheix, N.; Kabadjova, P.; Prevost, H.; Onno, B.; Dousset, X. Rapid investigation of French sourdough microbiota by restriction fragment length polymorphism of the 16S-23S rRNA gene intergenic spacer region. World J. Microbiol. Biotechnol. 2008, 24, 2425–2434. [Google Scholar] [CrossRef]
  50. Fu, W.; Rao, H.; Tian, Y.; Xue, W. Bacterial composition in sourdoughs from different regions in China and the microbial potential to reduce wheat allergens. LWT-Food Sci. Technol. 2020, 117, 108669. [Google Scholar] [CrossRef]
  51. De Vuyst, L.; Schrijvers, V.; Paramithiotis, S.; Hoste, B.; Vancanneyt, M.; Swings, J.; Kalantzopoulos, G.; Tsakalidou, E.; Messens, W. The biodiversity of Lactic Acid Bacteria in Greek traditional wheat sourdough is reflected in both composition and metabolite formation. Appl. Environ. Microbiol. 2002, 68, 6059–6069. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Paramithiotis, S.; Tsiasiotou, S.; Drosinos, E.H. Comparative study of spontaneously fermented sourdoughs originating from two regions of Greece: Peloponnesus and Thessaly. Eur. Food Res. Technol. 2010, 231, 883–890. [Google Scholar] [CrossRef]
  53. Syrokou, M.K.; Themeli, C.; Paramithiotis, S.; Mataragas, M.; Bosnea, L.; Argyri, A.; Chorianopoulos, N.G.; Skandamis, P.N.; Drosinos, E.H. Microbial ecology of Greek wheat sourdoughs identified by culture-dependent and culture-independent approach. Foods 2020, 9, 1603. [Google Scholar] [CrossRef]
  54. Lattanzi, A.; Minervini, F.; Di Cagno, R.; Diviccaro, A.; Antonielli, L.; Cardinali, G.; Cappelle, S.; De Angelis, M.; Gobbetti, M. The lactic acid bacteria and yeast microbiota of eighteen sourdoughs used for the manufacture of traditional Italian sweet leavened baked goods. Int. J. Food Microbiol. 2013, 15, 71–79. [Google Scholar] [CrossRef]
  55. Michel, E.; Monfort, C.; Deffrasnes, M.; Guezenec, S.; Lhomme, E.; Barret, M.; Sicard, D.; Dousset, X.; Onno, B. Characterization of relative abundance of lactic acid bacteria species in French organic sourdough by cultural, qPCR and MiSeq high-throughput sequencing methods. Int. J. Food Microbiol. 2016, 239, 35–43. [Google Scholar] [CrossRef] [Green Version]
  56. Nionelli, L.; Curri, N.; Curiel, J.A.; Di Cagno, R.; Pontonio, E.; Cavoski, I.; Gobbetti, M.; Rizzello, C.G. Exploitation of Albanian wheat cultivars: Characterization of the flours and lactic acid bacteria microbiota, and selection of starters for sourdough fermentation. Food Microbiol. 2014, 44, 96–107. [Google Scholar] [CrossRef]
  57. Comasio, A.; Verce, M.; Van Kerrebroeck, S.; De Vuyst, L. Diverse microbial composition of sourdoughs from different origins. Front. Microbiol. 2020, 11, 1212. [Google Scholar] [CrossRef]
  58. Kitahara, M.; Sakata, S.; Benno, Y. Biodiversity of Lactobacillus sanfranciscensis strains isolated from five sourdoughs. Lett. Appl. Microbiol. 2005, 40, 353–357. [Google Scholar] [CrossRef] [PubMed]
  59. Fraberger, V.; Unger, C.; Kummer, C.; Domig, K.J. Insights into microbial diversity of traditional Austrian sourdough. LWT-Food Sci. Technol. 2020, 127, 109358. [Google Scholar] [CrossRef]
  60. Petkova, M.; Stefanova, P.; Gotcheva, V.; Angelov, A. Isolation and characterisation of lactic acid bacteria and yeasts from typical Bulgarian sourdoughs. Microorganisms 2021, 9, 1346. [Google Scholar] [CrossRef] [PubMed]
  61. Boreczek, J.; Litwinek, D.; Zylinska-Urban, J.; Izak, D.; Buksa, K.; Gawor, J.; Gromadka, R.; Bardowski, J.K.; Kowalczyk, M. Bacterial community dynamics in spontaneous sourdoughs made from wheat, spelt, and rye wholemeal flour. MicrobiologyOpen 2020, 9, e1009. [Google Scholar] [CrossRef]
  62. Ganchev, I.; Koleva, Z.; Kizheva, Y.; Moncheva, P.; Hristova, P. Lactic acid bacteria from spontaneously fermented rye sourdough. Bulg. J. Agric. Sci. 2014, 20, 69–73. [Google Scholar]
  63. Rosenquist, H.; Hansen, A. The microbial stability of two bakery sourdoughs made from conventionally and organically grown rye. Food Microbiol. 2000, 17, 241–250. [Google Scholar] [CrossRef]
  64. Mueller, M.R.A.; Wolfrum, G.; Stolz, P.; Ehrmann, M.A.; Vogel, R.F. Monitoring the growth of Lactobacillus species during a rye flour fermentation. Food Microbiol. 2001, 18, 217–227. [Google Scholar] [CrossRef]
  65. Rocha, J.M.; Malcata, F.X. On the microbiological profile of traditional Portuguese sourdough. J. Food Prot. 1999, 62, 1416–1429. [Google Scholar] [CrossRef]
  66. Ispirli, H.; Demirbaş, F.; Yüzer, M.O.; Dertli, E. Identification of lactic acid bacteria from spontaneous rye sourdough and determination of their functional characteristics. Food Biotechnol. 2018, 32, 222–235. [Google Scholar] [CrossRef]
  67. Bartkiene, E.; Lele, V.; Ruzauskas, M.; Domig, K.; Starkute, V.; Zavistanaviciute, P.; Bartkevics, V.; Pugajeva, I.; Klupsaite, D.; Juodeikiene, G.; et al. Lactic acid bacteria isolation from spontaneous sourdough and their characterization including antimicrobial and antifungal proper-ties evaluation. Microorganisms 2020, 8, 64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Meroth, C.B.; Walter, J.; Hertel, C.; Brandt, M.J.; Hammes, W.P. Monitoring the bacterial population dynamics in sourdough fermentation processes by using PCR denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 2003, 69, 475–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Viiard, E.; Mihhalevski, A.; Rühka, T.; Paalme, T.; Sarand, I. Evaluation of the microbial community in industrial rye sourdough upon continuous back-slopping propagation revealed Lactobacillus helveticus as the dominant species. J. Appl. Microbiol. 2013, 114, 404–442. [Google Scholar] [CrossRef] [PubMed]
  70. Albano, H.; Henriques, I.; Correia, A.; Hogg, T.; Teixeira, P. Characterization of microbial population of ‘Alheira’ (a traditional Portuguese fermented sausage) by PCR-DGGE and traditional cultural microbiological methods. J. Appl. Microbiol. 2008, 105, 2187–2194. [Google Scholar] [CrossRef]
  71. Ammor, S.; Rachman, C.; Chaillou, S.; Prévost, H.; Dousset, X.; Zagorec, M.; Dufour, E.; Chevallier, I. Phenotypic and genotypic identification of lactic acid bacteria isolated from a small-scale facility producing traditional dry sausages. Food Microbiol. 2005, 22, 373–382. [Google Scholar] [CrossRef]
  72. Aquilanti, L.; Santarelli, S.; Silvestri, G.; Osimani, A.; Petruzzelli, A.; Clementi, F. The microbial ecology of a typical Italian salami during its natural fermentation. Int. J. Food Microbiol. 2007, 120, 136–145. [Google Scholar] [CrossRef]
  73. Aymerich, T.; Martin, B.; Garriga, M.; Vidal-Carou, M.C.; Bover-Cid, S.; Hugas, M. Safety properties and molecular strain typing of lactic acid bacteria from slightly fermented sausages. J. Appl. Microbiol. 2006, 100, 40–49. [Google Scholar] [CrossRef]
  74. Benito, M.J.; Martin, A.; Aranda, E.; Perez-Nevado, F.; Ruiz-Moyano, S.; Cordoba, M.G. Characterization and selection of autochthonous lactic acid bacteria isolated from traditional Iberian dry-fermented Salchichon and Chorizo sausages. J. Food Sci. 2007, 72, M193–M201. [Google Scholar] [CrossRef]
  75. Bonomo, M.G.; Ricciardi, A.; Zotta, T.; Parente, E.; Salzano, G. Molecular and technological characterization of lactic acid bacteria from traditional fermented sausages of Basilicata region (Southern Italy). Meat Sci. 2008, 80, 1238–1248. [Google Scholar] [CrossRef]
  76. Comi, G.; Urso, R.; Iacumin, L.; Rantsiou, K.; Cattaneo, P.; Cantoni, C.; Cocolin, L. Characterisation of naturally fermented sausages produced in the North East of Italy. Meat Sci. 2005, 69, 381–392. [Google Scholar] [CrossRef]
  77. Coppola, R.; Giagnacovo, B.; Iorizzo, M.; Grazia, L. Characterization of lactobacilli involved in the ripening of soppressata molisana, a typical southern Italy fermented sausage. Food Microbiol. 1998, 15, 47–353. [Google Scholar] [CrossRef]
  78. Di Cagno, R.; Chaves Lopez, C.; Tofalo, R.; Gallo, G.; De Angelis, M.; Paparella, A.; Hammes, W.; Gobbetti, M. Comparison of the compositional, microbiological, biochemical and volatile profile characteristics of three Italian PDO fermented sausages. Meat Sci. 2008, 79, 224–235. [Google Scholar] [CrossRef] [PubMed]
  79. Drosinos, E.H.; Mataragas, M.; Xiraphi, N.; Moschonas, G.; Gaitis, F.; Metaxopoulos, J. Characterization of the microbial flora from a traditional Greek fermented sausage. Meat Sci. 2005, 69, 307–317. [Google Scholar] [CrossRef]
  80. Drosinos, E.H.; Paramithiotis, S.; Kolovos, G.; Tsikouras, I.; Metaxopoulos, I. Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in Southern Greece. Food Microbiol. 2007, 24, 260–270. [Google Scholar] [CrossRef]
  81. Federici, S.; Ciarrocchi, F.; Campana, R.; Ciandrini, E.; Blasi, G.; Baffone, W. Identification and functional traits of lactic acid bacteria isolated from Ciauscolo salami produced in Central Italy. Meat Sci. 2014, 98, 575–584. [Google Scholar] [CrossRef]
  82. Fonseca, S.; Cachaldora, A.; Gómez, M.; Franco, I.; Carballo, J. Monitoring the bacterial population dynamics during the ripening of Galician chorizo, a traditional dry fermented Spanish sausage. Food Microbiol. 2013, 33, 77–84. [Google Scholar] [CrossRef] [PubMed]
  83. Fontana, C.; Cocconcelli, P.S.; Vignolo, G. Monitoring the bacterial population dynamics during fermentation of artisanal Argentinean sausages. Int. J. Food Microbiol. 2005, 103, 131–142. [Google Scholar] [CrossRef] [PubMed]
  84. Garcia Fontan, M.C.; Lorenzo, J.M.; Parada, A.; Franco, I.; Carballo, J. Microbiological characteristics of “androlla”, a Spanish traditional pork sausage. Food Microbiol. 2007, 24, 52–58. [Google Scholar] [CrossRef]
  85. Garcia Fontan, M.C.; Lorenzo, J.M.; Martinez, S.; Franco, I.; Carballo, J. Microbiological characteristics of Botillo, a Spanish traditional pork sausage. LWT-Food Sci. Technol. 2007, 40, 610–1622. [Google Scholar] [CrossRef]
  86. Greppi, A.; Ferrocino, I.; La Storia, A.; Rantsiou, K.; Ercolini, D.; Cocolin, L. Monitoring of the microbiota of fermented sausages by culture independent rRNA-based approaches. Int. J. Food Microbiol. 2015, 212, 67–75. [Google Scholar] [CrossRef]
  87. Martin, B.; Garriga, M.; Hugas, M.; Bover-Cid, S.; Veciana-Nogués, M.T.; Aymerich, T. Molecular, technological and safety characterization of Gram-positive catalase-positive cocci from slightly fermented sausages. Int. J. Food Microbiol. 2006, 107, 148–158. [Google Scholar] [CrossRef] [PubMed]
  88. Papamanoli, E.; Tzanetakis, N.; Litopoulou-Tzanetaki, E.; Kotzekidou, P. Characterization of lactic acid bacteria isolated from a Greek dry-fermented sausage in respect of their technological and probiotic properties. Meat Sci. 2003, 65, 859–867. [Google Scholar] [CrossRef] [PubMed]
  89. Parente, E.; Grieco, S.; Crudele, M.A. Phenotypic diversity of lactic acid bacteria isolated from fermented sausages produced in Basilicata (Southern Italy). J. Appl. Microbiol. 2001, 90, 943–952. [Google Scholar] [CrossRef] [PubMed]
  90. Pini, F.; Aquilani, C.; Giovannetti, L.; Viti, C.; Pugliese, C. Characterization of the microbial community composition in Italian Cinta Senese sausages dry-fermented with natural extracts as alternatives to sodium nitrite. Food Microbiol. 2020, 89, 103417. [Google Scholar] [CrossRef] [PubMed]
  91. Pisacane, V.; Callegari, M.L.; Puglisi, E.; Dallolio, G.; Rebecchi, A. Microbial analyses of traditional Italian salami reveal microorganisms transfer from the natural casing to the meat matrix. Int. J. Food Microbiol. 2015, 207, 57–65. [Google Scholar] [CrossRef]
  92. Polka, J.; Rebecchi, A.; Pisacane, V.; Morelli, L. Bacterial diversity in typical Italian salami at different ripening stages as revealed by high-throughput sequencing of 16s rRNA amplicons. Food Microbiol. 2015, 46, 342–356. [Google Scholar] [CrossRef]
  93. Prado, N.; Sampayo, M.; González, P.; Lombó, F.; Díaz, J. Physicochemical, sensory and microbiological characterization of Asturian Chorizo, a traditional fermented sausage manufactured in Northern Spain. Meat Sci. 2019, 156, 118–124. [Google Scholar] [CrossRef]
  94. Rantsiou, K.; Drosinos, E.H.; Gialitaki, M.; Metaxopoulos, I.; Comi, G.; Cocolin, L. Use of molecular tools to characterize Lactobacillus spp. isolated from Greek traditional fermented sausages. Int. J. Food Microbiol. 2006, 112, 215–222. [Google Scholar] [CrossRef]
  95. Rantsiou, K.; Drosinos, E.H.; Gialitaki, M.; Urso, R.; Krommer, J.; Gasparik-Reichardt, J.; Toth, S.; Metaxopoulos, I.; Comi, G.; Cocolin, L. Molecular characterization of Lactobacillus species isolated from naturally fermented sausages produced in Greece, Hungary and Italy. Food Microbiol. 2005, 22, 19–28. [Google Scholar] [CrossRef]
  96. Rebecchi, A.; Crivori, S.; Sarra, P.G.; Cocconcelli, P.S. Physiological and molecular techniques for the study of bacterial community development in sausage fermentation. J. Appl. Microbiol. 1998, 84, 1043–1049. [Google Scholar] [CrossRef]
  97. Samelis, J.; Maurogenakis, F.; Metaxopoulos, J. Characterisation of lactic acid bacteria isolated from naturally fermented Greek dry salami. Int. J. Food Microbiol. 1994, 23, 179–196. [Google Scholar] [CrossRef] [PubMed]
  98. Samelis, J.; Metaxopoulos, J.; Vlassi, M.; Pappa, A. Stability and safety of traditional Greek salami—A microbiological ecology study. Int. J. Food Microbiol. 1998, 44, 69–82. [Google Scholar] [CrossRef] [PubMed]
  99. Silvestri, G.; Santarelli, S.; Aquilanti, L.; Beccaceci, A.; Osimani, A.; Tonucci, F.; Clementi, F. Investigation of the microbial ecology of Ciauscolo, a traditional Italian salami, by culture–dependent techniques and PCR-DGGE. Meat Sci. 2007, 77, 413–423. [Google Scholar] [CrossRef] [PubMed]
  100. Urso, R.; Comi, G.; Cocolin, L. Ecology of lactic acid bacteria in Italian fermented sausages: Isolation, identification and molecular characterization. Syst. Appl. Microbiol. 2006, 29, 671–680. [Google Scholar] [CrossRef]
  101. Paramithiotis, S.; Drosinos, E.H. The sourdough micro-ecosystem: An update. In Fermented Foods, Part II: Technological Interventions; Ray, R.C., Montet, D., Eds.; CRC Science: Cleveland, OH, USA, 2017; pp. 263–283. [Google Scholar]
  102. Shao, L.; Chen, S.; Wang, H.; Zhang, J.; Xu, X.; Wang, H. Advances in understanding the predominance, phenotypes, and mechanisms of bacteria related to meat spoilage. Trends Food Sci. Technol. 2021, 118, 822–832. [Google Scholar] [CrossRef]
  103. Paramithiotis, S.; Skandamis, P.N.; Nychas, G.J.E. Insights into fresh meat spoilage. In Safety of Meat and Processed Meat; Toldra, F., Ed.; Springer: New York, NY, USA, 2009; pp. 55–82. [Google Scholar]
  104. Lorenzo, J.M.; Munekata, P.E.; Dominguez, R.; Pateiro, M.; Saraiva, J.A.; Franco, D. Main groups of microorganisms of relevance for food safety and stability: General aspects and overall description. In Innovative Technologies for Food Preservation. Inactivation of Spoilage and Pathogenic Microorganisms; Barba, G.J., Sant’Ana, A.S., Orlien, V., Koubaa, M., Eds.; Academic Press: Amsterdam, The Netherlands, 2018; pp. 53–107. [Google Scholar]
  105. Borch, E.; Kant-Muermans, M.-L.; Blixt, Y. Bacterial spoilage of meat and cured meat products. Int. J. Food Microbiol. 1996, 33, 103–120. [Google Scholar] [CrossRef]
  106. Paramithiotis, S.; Drosinos, E.H. Foodborne pathogens of fermented meat products In Fermented Meat Products: Health Aspects; Zdolec, N., Ed.; CRC Science: Cleveland, OH, USA, 2016; pp. 196–227. [Google Scholar]
  107. Moschopoulou, E.; Moatsou, G.; Syrokou, M.K.; Paramithiotis, S.; Drosinos, E.H. Food quality changes during shelf life. In Food Quality and Shelf Life; Galanakis, C.M., Ed.; Academic Press: London, UK, 2019; pp. 1–32. [Google Scholar]
  108. Erkmen, O.; Bozoglu, T.F. Spoilage of milk and milk products. In Food Microbiology: Principles into Practice; Erkmen, O., Bozoglu, T.F., Eds.; J. Wiley & Sons: Hoboken, NJ, USA, 2016; pp. 307–336. [Google Scholar]
  109. Leff, J.W.; Fierer, N. Bacterial communities associated with the surfaces of fresh fruits and vegetables. PLoS ONE 2013, 8, e59310. [Google Scholar] [CrossRef] [Green Version]
  110. Paramithiotis, S.; Drosinos, E.H.; Skandamis, P. Microbial ecology of fruits and fruit-based products. In Quantitative Microbiology in Food Processing—Modeling the Microbial Ecology; de Souza Sant’Ana, A., Ed.; J. Wiley & Sons: Hoboken, NJ, USA, 2017; pp. 358–381. [Google Scholar]
  111. Michl, K.; Berg, G.; Cernava, T. The microbiome of cereal plants: The current state of knowledge and the potential for future applications. Environ. Microbiome 2023, 18, 28. [Google Scholar] [CrossRef]
  112. Erkmen, O.; Bozoglu, T.F. Spoilage of vegetables and fruits. In Food Microbiology: Principles into Practice; Erkmen, O., Bozoglu, T.F., Eds.; J. Wiley & Sons: Hoboken, NJ, USA, 2016; pp. 337–363. [Google Scholar]
  113. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). The European Union One Health 2019 Zoonoses Report. EFSA J. 2021, 19, 6406. [Google Scholar]
  114. Berg, G.; Rybakova, D.; Fischer, D.; Cernava, T.; Champomier Vergès, M.-C.; Charles, T.; Chen, X.; Cocolin, L.; Eversole, K.; Corral, G.H.; et al. Microbiome definition re-visited: Old concepts and new challenges. Microbiome 2020, 8, 103. [Google Scholar] [CrossRef]
  115. Tilocca, B.; Soggiu, A.; Iavarone, F.; Greco, V.; Putignani, L.; Ristori, M.V.; Macari, G.; Spina, A.A.; Morittu, V.M.; Ceniti, C.; et al. The functional characteristics of goat cheese microbiota from the one-health perspective. Int. J. Mol. Sci. 2022, 23, 14131. [Google Scholar] [CrossRef]
  116. Nelli, A.; Venardou, B.; Skoufos, I.; Voidarou, C.; Lagkouvardos, I.; Tzora, A. An insight into goat cheese: The tales of artisanal and industrial Gidotyri microbiota. Microorganisms 2023, 11, 123. [Google Scholar] [CrossRef]
  117. Tsigkrimani, M.; Bakogianni, M.; Paramithiotis, S.; Bosnea, L.; Pappa, E.; Drosinos, E.H.; Skandamis, P.Ν.; Mataragas, M. Microbial ecology of artisanal Feta and Kefalograviera cheeses. Part I: Bacterial community and its functional characteristics with focus on lactic acid bacteria as determined by culture-dependent methods and phenotype microarrays. Microorganisms 2022, 10, 161. [Google Scholar] [CrossRef]
  118. Gram, L.; Huss, H.H. Microbiological spoilage of fish and fish products. Int. J. Food Microbiol. 1996, 33, 121–137. [Google Scholar] [CrossRef]
  119. Tiedje, J.M.; Bruns, M.A.; Casadevall, A.; Criddle, C.S.; Eloe-Fadrosh, E.; Karl, D.M.; Nguyen, N.K.; Zhouh, J. Microbes and climate change: A research prospectus for the future. mBio 2022, 13, 3. [Google Scholar] [CrossRef] [PubMed]
  120. Guo, X.; Zhou, X.; Hale, L.; Yuan, M.; Ning, D.; Feng, J.; Shi, Z.; Li, Z.; Feng, B.; Gao, Q.; et al. Climate warming accelerates temporal scaling of grassland soil microbial biodiversity. Nat. Ecol. Evol. 2019, 3, 612–619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  121. Brubacher, D.; Allen, M.; Déry, S.J.; Parkes, M.W.; Chhetri, B.; Mak, S.; Sobie, S.; Takaro, T.K. Associations of five food- and water-borne diseases with ecological zone, land use and aquifer type in a changing climate. Sci. Total Environ. 2020, 728, 138808. [Google Scholar] [CrossRef] [PubMed]
  122. Lhomme, E.; Urien, C.; Legrand, J.; Dousset, X.; Onno, B.; Sicard, D. Sourdough microbial community dynamics: An analysis during French organic bread-making processes. Food Microbiol. 2016, 53, 41–50. [Google Scholar] [CrossRef]
  123. Schultze, S.R.; Sabbatini, P. Implications of a climate-changed atmosphere on cool-climate viticulture. J. Appl. Meteorol. Climatol. 2019, 58, 1141–1153. [Google Scholar] [CrossRef]
  124. Hewer, M.J.; Gough, W.A. Climate change impact assessment on grape growth and wine production in the Okanagan valley (Canada). Clim. Risk Manag. 2021, 33, 100343. [Google Scholar] [CrossRef]
  125. van Leeuwen, C.; Destrac-Irvine, A. Modified grape composition under climate change conditions requires adaptations in the vineyard. Oeno One 2017, 51, 147–154. [Google Scholar] [CrossRef]
  126. Santos, J.A.; Fraga, H.; Malheiro, A.C.; Moutinho-Pereira, J.; Dinis, L.-T.; Correia, C.; Moriondo, M.; Leolini, L.; Dibari, C.; Costafreda-Aumedes, S.; et al. A Review of the potential climate change impacts and adaptation options for European viticulture. Appl. Sci. 2020, 10, 3092. [Google Scholar] [CrossRef]
  127. Duchenne-Moutien, R.A.; Neetoo, H. Climate change and emerging food safety issues: A review. J. Food Prot. 2021, 84, 1884–1897. [Google Scholar] [CrossRef] [PubMed]
  128. Zheng, J.; Wittouck, S.; Salvetti, E.; Franz, C.M.A.P.; Harris, H.M.B.; Mattarelli, P.; O’Toole, P.W.; Pot, B.; Vandamme, P.; Walter, J.; et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 2020, 70, 2782–2858. [Google Scholar] [CrossRef]
  129. Kang, J.P.; Huo, Y.; Hoang, V.A.; Yang, D.U.; Yang, D.C.; Kang, S.C. Bombilactobacillus apium sp. nov., isolated from the gut of honeybee (Apis cerana). Arch. Microbiol. 2021, 203, 2193–2198. [Google Scholar] [CrossRef]
  130. Panziera, D.; Requier, F.; Chantawannakul, P.; Pirk, C.W.W.; Blacquière, T. The diversity decline in wild and managed honey bee populations urges for an integrated conservation approach. Front. Ecol. Evol. 2022, 10, 767950. [Google Scholar] [CrossRef]
  131. Semeniuk, V.; Cresswell, I.D. A proposed revision of diversity measures. Diversity 2013, 5, 613–626. [Google Scholar] [CrossRef] [Green Version]
  132. Cibario, A.; Avramova, M.; Dimopoulou, M.; Magani, M.; Miot-Sertier, C.; Mas, A.; Portillo, M.C.; Ballestra, P.; Albertin, W.; Masneuf-Pomarede, I.; et al. Brettanomyces bruxellensis wine isolates show high geographical dispersal and long persistence in cellars. PLoS ONE 2019, 14, e0222749. [Google Scholar]
  133. Peixoto, R.S.; Voolstra, C.R.; Sweet, M.; Duarte, C.M.; Carvalho, S.; Villela, H.; Lunshof, J.E.; Gram, L.; Woodhams, D.C.; Walter, J.; et al. Harnessing the microbiome to prevent global biodiversity loss. Nat. Microbiol. 2022, 7, 1726–1735. [Google Scholar] [CrossRef]
Ecologies 04 00034 g001
Figure 1. The lactic acid bacteria microbiota of 439 traditional wheat sourdough samples from European countries, USA, China, and Japan. The word cloud was generated at https://www.freewordcloudgenerator.com/ (accessed on 2 June 2023).
Figure 1. The lactic acid bacteria microbiota of 439 traditional wheat sourdough samples from European countries, USA, China, and Japan. The word cloud was generated at https://www.freewordcloudgenerator.com/ (accessed on 2 June 2023).
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Figure 2. The lactic acid bacteria microbiota of 38 samples of traditional rye sourdoughs from European countries and USA. The word cloud was generated at https://www.freewordcloudgenerator.com/ (accessed on 2 June 2023).
Figure 2. The lactic acid bacteria microbiota of 38 samples of traditional rye sourdoughs from European countries and USA. The word cloud was generated at https://www.freewordcloudgenerator.com/ (accessed on 2 June 2023).
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Table 1. Lactic acid bacteria involved in the development of renowned products made by spontaneous lactic acid fermentation.
Table 1. Lactic acid bacteria involved in the development of renowned products made by spontaneous lactic acid fermentation.
ProductLactic Acid BacteriaReferences
KimchiLc. gelidum, Ln. carnosum, Ln. citreum, Ln. gasicomitatum, Ln. gelidum, Ln. holzapfelii, Ln. inhae, Ln. kimchii, Ln. lactis, Ln. mesenteroides, Lp. pentosus, Lp. plantarum, Lt. curvatus, Lt. sakei, Lv. brevis, Lv. parabrevis, Lv. spicheri, W. cibaria, W. confusa, W. kandleri, W. koreensis, and W. soli[15,16,17,18,19,20,21,22]
SauerkrautE. faecalis, Lc. lactis subsp. lactis, Ln. fallax, Ln. mesenteroides, Lp. plantarum, Lt. curvatus, Lt. sakei, Lv. brevis, P. pentosaceus, and W. confusa[23,24,25]
Wheat sourdoughsC. alimentarius, C. crustorum, C. farciminis, C. heilongjiangensis, C. kimchii, C. mindensis, C. nantensis, C. paralimentarius, E. durans, E. faecalis, E. faecium, E. hirae, Fr. fructivorans, Fr. sanfranciscensis, Fu. rossiae, La. casei, La. paracasei, La. rhamnosus, Lb. acetotolerans, Lb. acidophilus, Lb. delbrueckii, Lb. gallinarum, Lb. guizhouensis, Lb. helveticus, Lc. lactis, Le. buchneri, Le. diolivorans, Le. farraginis, Le. hilgardii, Le. kisonensis, Le. parabuchneri, Lm. fermentum, Lm. frumenti, Lm. panis, Lm. pontis, Ln. citreum, Ln. mesenteroides, Ln. pseudomesenteroides, Lo. coryniformis, Lp. paraplantarum, Lp. pentosus, Lp. plantarum, Lp. xiangfangensis, Lt. curvatus, Lt. graminis, Lt. sakei, Lt. sunkii, Lv. brevis, Lv. hammesii, Lv. koreensis, Lv. namurensis, Lv. parabrevis, Lv. senmaizukei, Lv. spicheri, Lv. zymae, P. acidilactici, P. argentinicus, P. inopinatus, P. parvulus, P. pentosaceus, Pa. vaccinostercus; Sc. harbinensis, Sc. perolens, W. cibaria, W. confusa, W. paramesenteroides, and W. viridescens[26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61]
Rye sourdoughsC. kimchii, C. paralimentarius, C. mindensis, C. nantensis, E. pseudoavium, Fr. sanfranciscensis, Fu. rossiae, La. casei, La. paracasei, Lb. acidophilus, Lb. amylovorus, Lb. crispatus, Lb. delbrueckii, Lb. gallinarum, Lb. helveticus, Lb. johnsonii, Lc. lactis, Le. diolivorans, Le. farraginis, Le. kisonensis, Le. otakiensis, Lm. fermentum, Lm. frumenti, Lm. panis, Lm. pontis, Lm. reuteri, Ln. citreum, Ln. mesenteroides, Lo. coryniformis, Lp. plantarum, Lp. xiangfangensis, Lq. uvarum, Lt. curvatus, Lt. graminis, Lv. brevis, Lv. hammesii, Lv. parabrevis, Lv. senmaizukei, Lv. spicheri, P. acidilactici, P. pentosaceus, W. cibaria, W. confusa, and W. viridescens[45,46,47,57,58,59,60,61,62,63,64,65,66,67,68,69]
Fermented meat productsC. alimentarius, C. farciminis, C. futsai, C. paralimentarius, C. versmoldensis, Ca. divergens, E. faecalis, E. faecium, E. gallinarum, E. pseudoavium, La. casei, La. paracasei, La. rhamnosus, La. zeae, Lb. acidophilus, Lb. helveticus, Lb. johnsonii, Lc. garveae, Lc. lactis, Le. buchneri, Li. salivarius, Lm. antri, Lm. fermentum, Lm. frumenti, Lm. oris, Lm. panis, Lm. reuteri, Lm. vaginalis, Ln. carnosum, Ln. citreum, Ln. gelidum, Ln. lactis, Ln. mesenteroides, Ln. pseudomesenteroides, Lo. coryniformis, Lp. paraplantarum, Lp. pentosus, Lp. plantarum, Lt. curvatus, Lt. graminis, Lt. sakei, Lv. brevis, P. acidilactici, P. pentosaceus, W. hellenica, W. minor, W. paramesenteroides, and W. viridescens[70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100]
C.: Companilactobacillus; Ca.: Carnobacterium; E.: Enterococcus; Fr.: Fructilactobacillus; Fu.: Furfurilactobacillus; La.: Lacticaseibacillus; Lb.: Lactobacillus; Lc.: Lactococcus; Le.: Lentilactobacillus; Li.: Ligilactobacillus; Lm.: Limosilactobacillus; Ln.: Leuconostoc; Lo.: Loigolactobacillus; Lp.: Lactiplantibacillus; Lq.: Liquorilactobacillus; Lt.: Latilactobacillus; Lv.: Levilactobacillus; P.: Pediococcus; Pa.: Paucilactobacillus; Sc.: Schleiferilactobacillus; W.: Weissella.
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Paramithiotis, S.; Dimopoulou, M. Preserving Microbial Biodiversity: The Case of Food-Associated Microorganisms. Ecologies 2023, 4, 521-534. https://doi.org/10.3390/ecologies4030034

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Paramithiotis S, Dimopoulou M. Preserving Microbial Biodiversity: The Case of Food-Associated Microorganisms. Ecologies. 2023; 4(3):521-534. https://doi.org/10.3390/ecologies4030034

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Paramithiotis, Spiros, and Maria Dimopoulou. 2023. "Preserving Microbial Biodiversity: The Case of Food-Associated Microorganisms" Ecologies 4, no. 3: 521-534. https://doi.org/10.3390/ecologies4030034

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