Fermentation in Traditional Foods: History
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Fermentation counts among the oldest food-processing technologies and is applied historically in almost every culture to prepare a wide variety of staple foods that play an important role in human diets.

  • fermentation
  • lactic acid bacteria
  • Fermented cereal and legume
  • Traditional foods

1. Introduction

Fermentation counts among the oldest food-processing technologies and is applied historically in almost every culture to prepare a wide variety of staple foods that play an important role in human diets. Fermented beverages, such as Mahewu (South Africa), or cereal puddings, such as Ogi (Nigeria), are prepared from raw cereal grains and consumed throughout the day or used as infant food. Spontaneous fermentation takes place during the preparation as a result of undefined mixed cultures with plant- and environmental origin and can be defined as controlled microbial growth that affects major and minor food components through enzymatic conversion [1]. As a result, starchy raw materials are preserved and rendered more palatable through the production of organic acids and the pre-digestion of plant material. Popular non-alcoholic fermented products are found across the African, Eastern-European, and Asian continents and are summarised in Table 1 with associated LAB microbiota.
Table 1. Overview of popular traditionally fermented beverage and gel-type foods from various cultures worldwide including dominating microbiota, food type, and preparation methods.

2. Undefined Mixed Cultures of Traditional Foods

The fermentation by lactic acid bacteria (LAB) belonging to the family Lactobacillaceae is predominant in liquid and semiliquid traditional foods [23]. The production of organic acids by metabolising carbohydrate material to lactic acid, acetic acid, and, to a lesser extent, propionic acid, succinate, and acetoin leads to a pH reduction and characteristic flavours. Additionally, the accumulation of exopolysaccharides (EPSs) is a desired effect and contributes to texture development by impacting viscosity and water retention [24]. Additional fermentative processes take place and have to be acknowledged, which also includes the activity of yeast (Saccharomyces sp., Candida sp.). In boza, a fermented Bulgarian beverage, the presence of LAB and yeast was reported at a ratio of 2.2–2.6 [4]. Synergistic behaviour exists between LAB and yeast, but their presence in non-alcoholic foods is generally undesired based on sensory studies [25]. Fungi, spore-forming bacteria (Bacillus sp.), and additional alkaline fermenting species (Micrococcus sp.) have been attributed to protein fermentation in legume-based condiments, such as natto (Japan) or kinema (India) [26][27]. In liquid foods rich in carbohydrates, their role is however limited by the antagonistic effects of LAB fermentation. Dominating LAB from boza and other cereal-based products have shown the capacity to produce a wide range of antimicrobial substances, including bacteriocin, hydrogen peroxide, fatty acids, and diacetyl, which have attracted interest in them as probiotics [28][29][30]. Microbiota of traditional fermented foods are established from dispersed naturally occurring species found on the grain and depend on the ecological fitness of the individual organism, fermentation conditions, and availability of nutrients.
An inoculation step is often included in traditional preparations and uses small amounts of previous successful batches as a starter culture (Table 1). Remarkably, by using this so called “back-slopping” approach, undefined mixed cultures were found to remain stable, down to the strain level, over decades if substrates and fermentation conditions are maintained [31]. This phenomenon has been explored mainly in fermented dairy products so far. In such environments, mixed cultures have shown superior resilience against phage attack and contaminants when compared to defined single-strain starter cultures [32][33]. This increased stability is economically advantageous to the food producer as it reduces the risk of failed batches and limits the need to monitor phages during the fermentation. Additionally, the continuous sub-culturing process in fermented food produced using back-slopping has been shown to allow for metabolic adaptations to the food environment in dairy-associated species, such as L. delbrueckii [34]. Such adaptations can permit the emergence of cultures with superior performance without the need for gene manipulation. Model mixed cultures of cereal-fermented foods remain poorly explored to this date but continue to attract attention as a valuable source of LAB strains with beneficial technological and probiotic properties [29][30][35].

3. Metabolic Processes during Fermentation

Cereals, such as maize, millet and sorghum, but also tubers (cassava) or legumes (faba bean), are among plant materials that are widely used as substrates for fermentation. Typically, the type of fermentation ingredient will depend on the country or region and availability. These plant materials are often pre-processed through mashing, grinding, and soaking to promote access by microorganisms to the fermentable compounds. Across this diversity of raw materials, starches are the most abundant (i.e., 35–90%) fermentable macromolecule and serve as an important carbon source. Pre-processing steps, such as mashing, grinding, and soaking, result in the release and stimulation of endogenous enzymes (α-amylase, maltase, glucoamylase) in the early stages, allowing for starch hydrolysis into fermentable sugar (glucose, maltose, maltodextrin) [26]. Additionally, amylolytic LAB (ALAB) that show the expression of extracellular α-amylase have been isolated from fermented cereals [36]. ALAB are capable of metabolising starches directly and form synergies with other LAB species. In Nigerian Ogi, ALAB make up 14% of isolated bacteria and were found to be essential for its biodiversity [37]. Genomic markers for the responsible enzymes (α-amylase, α-glucosidase, glycosyltransferase) can be found across most LAB species; however, their expression is rare and specific to certain strains [38]. Lp. plantarum is recognised as the dominant ALAB, while few other examples exist for L. acidophilus, Lm. Fermentum, and Lm. reuteri [36]. B. amyloliquefaciens, as one of the most amylolytic species, can also be found in fermented foods [7][39], but a poor pH tolerance limits the activity of such spore-forming bacteria.
Species that are considered “nomadic”, Lp. plantarum, Lc. Casei, and Lv. brevis, dominate microbial communities in traditional fermented food and possess broad carbohydrate-metabolic capabilities, whereas host-adapted species (L. delbrueckii, Lm. reuteri) have lost their ability to metabolise diverse carbohydrates due to niche adaptation and often rely on the presence of glucose, lactose, and sucrose in the substrate [34]. The separation of LAB into two main groups based on evolutionary history is useful. Homofermentative LAB (L. delbrueckii, L. acidophilus) convert glucose to lactic acid following the Emden–Meyerhof–Parnaz Pathway and are used as starter cultures in modern food fermentation, while heterofermentative LAB (Lv. brevis, Lm. fermentum, Lm. reuteri) are abundant in traditional fermentation and convert glucose to lactic acid and CO2 using variations of the phosphoketolase pathway. Ethanol can collect as a side product but normally only at low quantities due to a rate-limiting effect, which leads to the accumulation of flavour active alternatives, such as the fruity acetate [24]. Lp. Plantarum, Lc. Rhamnosus, and L. paracasei are examples of facultative heterofermenters that possess the ability to switch between the two metabolic pathways depending on environmental factors [31]. The diversity of carbohydrates present in cereals is beneficial for such organisms and allows for the formation of complex mixtures of metabolites [36]. Hexose (fructose, mannose), pentose (xylose, ribose), and organic acids (citrate, malate, or pyruvate) for instance were shown to support the growth of heterofermenters and are involved in the production of EPS [40].
Species-dependant auxotrophy for essential amino acids is a characteristic of LAB. To sustain growth, a variety of proteolytic systems (cell-wall bound protease, transporter, and intracellular peptidase) are expressed once free amino acids are depleted [41]. The ability to metabolise peptides is widely found among LAB, unlike protease-type enzymes, which are found on plasmids and can be lost during prolonged propagation [42][43]. Substrate specificity of the expressed enzymes differs between species and combined with the limited proteolytic activity of species, such as Lp. plantarum and Leuconostoc sp., encourages a symbiotic lifestyle of LAB, where required metabolites (amino acids, glucose, vitamins) are exchanged. As such, the effect on protein materials and the release of amino acids/peptides depends on the combined proteolytic capabilities and metabolic demand of the present mixed culture. In the context of food, the fermentative breakdown of protein has been shown to contribute to the flavour, generation of bioactivities, and improvement of digestive properties [42][44].

This entry is adapted from the peer-reviewed paper 10.3390/fermentation9050452

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