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Ziarno, M. Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages. Encyclopedia. Available online: https://encyclopedia.pub/entry/17502 (accessed on 28 November 2023).
Ziarno M. Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages. Encyclopedia. Available at: https://encyclopedia.pub/entry/17502. Accessed November 28, 2023.
Ziarno, Malgorzata. "Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages" Encyclopedia, https://encyclopedia.pub/entry/17502 (accessed November 28, 2023).
Ziarno, M.(2021, December 23). Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages. In Encyclopedia. https://encyclopedia.pub/entry/17502
Ziarno, Malgorzata. "Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages." Encyclopedia. Web. 23 December, 2021.
Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal- Based Beverages
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms9122532

Plant beverages are becoming more popular, and fermented cereal- or pseudocereal-based beverages are increasingly used as alternatives for fermented products made from cow milk. This review aimed to describe the basic components of cereal- or pseudocereal-based beverages and determine the feasibility of fermenting them with lactic acid bacteria (LAB) to obtain products with live and active LAB cells and increased dietary value. The technology used for obtaining cerealor pseudocereal-based milk substitutes primarily involves the extraction of selected plant material, and the obtained beverages differ in their chemical composition and nutritional value (content of proteins, lipids, and carbohydrates, glycemic index, etc.) due to the chemical diversity of the cereal and pseudocereal raw materials and the operations used for their production. Beverages made from cereals or pseudocereals are an excellent matrix for the growth of LAB, and the lactic acid fermentation not only produces desirable changes in the flavor of fermented beverages and the biological availability of nutrients but also contributes to the formation of functional compounds (e.g., B vitamins).

plant-based beverages lactic acid fermentation bioactive metabolites B vitamins

1. Occurrence of LAB in Cereals and Pseudocereals and Their Fermentation Abilities

1.1. Occurrence and Activity of LAB

LAB occur naturally in various environments, including the surface of growing and decaying plant materials. This obviously indicates that LAB can adapt to a specific environment. This property of environmental adaptation of LAB can be related to their ability to use available nutrients by lactic acid fermentation, to tolerate and survive in different environmental conditions, and to produce antimicrobial compounds that can inhibit competing microorganisms [1][2][3][4][5][6][7].
Lactic acid fermentation is defined as the process by which energy-rich organic substances are enzymatically decomposed into simple compounds that are poorer in energy. This process, which takes place under microaerophilic or relatively anaerobic conditions, is carried out by various bacterial species that can convert sugars into lactic acid and other metabolites. Fermented products have been part of the human diet since the beginning of human civilization, which indicates that they were believed to have a positive effect on health [1][2][8][9][10][11][12][13][14][15][16][17][18][19][20][21]. Lactic acid fermentation is of two types: (1) spontaneous fermentation and (2) fermentation with the use of selected starter cultures. Of these, the latter allows for greater control of the process [22][23][24].
Both spontaneous and controlled lactic acid fermentation are applied in the food industry, including the dairy industry for producing fermented milk drinks, cheese, and butter; the meat industry for producing raw-ripening cured meats; the fruit and vegetable industry for producing vegetable silage and fermented food spices; and the feed industry for producing silage [25][23][26][27][28][29][30][31][32]. In general, products resulting from lactic acid fermentation are characterized by a desirable taste, improved digestibility, and increased bioavailability of nutrients (Table 1) [1][2][22][33][34][35][36][37][38][39]. The characteristic taste of fermented plant-based products can be related to their slight but significant proteolytic and lipolytic activity, as was demonstrated for fermented soy beverages [40]. In addition, fermentation has been shown to contribute to the formation of functional compounds such as B vitamins and antioxidants, and scientists have proven that fermented products are valuable for the prevention of diabetes and obesity [41][42][43][44][45][46][47][48][49][50][51]. In the case of plant-based raw materials, fermentation allows for the elimination of plant flavors and changes the content of phytic acid, polyphenols, and tannins [2][22][33][52][34][42][53][54][55][56][57][58][59][60][61][62].
Table 1. Studies employing LAB as starter cultures in fermentation of cereal- and pseudocereal-based beverages (examples).
Matrix Culture Used Topic of Study Ref.
Rice Commercial starters Properties of yogurt-like fermented brown rice product [63]
Rice L. plantarum, L. brevis, L. rhamnosus Characterizatics of yogurt-style snack [64]
Rice L. casei, L. bulgaricus L. acidophilus, S. thermophilus, B. longum, Probiotic rice milk [65]
Rice L. brevis, L. fermentum, L. plantarum, Bifidobacterium longum Properties of fermented rice
Beverages		 [66]
Rice Commercial starter culture (L. acidophilus, S. thermophilus, Bifidobacterium bifidum) Fermented rice milk [67]
Rice Commercial starter cultures of yogurt bacteria Viability of starter culture bacteria [38]
Rice L. plantarum, L. vermiforme, L. paracasei Fermented rice beverage [68]
Oat L. plantarum Properties of oat-based beverage [69]
Oat L. plantarum Properties of fermented oat-based product [70]
Oat P. damnosus Properties of oat-based product, determination of EPS [71]
Oat L. plantarum Properties of flavored oat drink [39]
Oat L. plantarum Properties of synbiotic functional drink from oats [72]
Oat L. plantarum, L. Casei, L. paracasei Properties of oat-based, yogurt-like beverage [34]
Oat L. brevis, P. damnosus Properties of oat-based product [73]
Oat L. delbrueckii
subsp. bulgaricus, L. brevis, S. thermophilus		 Properties of oat-based, yogurt-like beverage, determination of EPS yield [74]
Oat L. reuteri, L. acidophilus, Bifidobacterium bifidum Properties of oat-based product [75]
Oat Commercial yogurt culture (S. thermophilus, L. delbrueckii subsp. bulgaricus) Properties of oat yogurt-type product [76]
Millet Commercial yogurt culture (S. thermophilus, L. delbrueckii subsp. Bulgaricus, Bifidobacterium sp.) Properties of fermented millet beverages [77]
Millet Commercial yogurt culture (S. thermophilus, L. delbrueckii subsp. bulgaricus, Bifidobacterium sp.) Properties of fermented millet beverages [78]
Millet L. brevis, L. fermentum Carbohydrate content of pearl millet flour [79]
Sorghum W. confusa, L. paracasei, L. fermentum, L. brevis, L. plantarum Volatile analysis of fermented cereal beverage [80]
Buckwheat Commercial starter culture (S. thermophilus, L. delbrueckii subsp. bulgaricus, Bifidobacterium sp.) Fermentation of buckwheat beverages [81]
Buckwheat Lb. rhamnosus, Lactococcus lactis spp. lactis, L. lactis spp. cremoris, S. thermophilus Growth and metabolic characteristics of selected LAB in buckwheat substrates [82]
Buckwheat Commercial yogurt culture (S. thermophilus, L. delbrueckii subsp. bulgaricus, Bifidobacterium sp.) Characteristics of fermented buckwheat beverages [83]
Quinoa L. plantarum, L. casei, Lactococcus lactis Characteristics of quinoa-based
fermented beverage		 [84]
Quinoa L. plantarum, L. rhamnosus, W. confusa Microbial, chemical, rheological, and nutritional properties of quinoa yogurt-like beverages [85]
Quinoa W. cibaria Nutritional properties of quinoa-based yogurt [86]
Quinoa L. plantarum Fermentation process, microbiological safety [87]
Quinoa Commercial starter culture (Bifidobacterium sp., L. acidophilus, S. thermophilus) Nutritional properties of quinoa-based beverage fermented [88]
Maize L. paracasei Properties of functional corn-based beverage [89]
Maize L. rhamnosus, S. thermophilus African maize-based fermented food (kwete) [90]
Maize Spontaneous fermentation Fermented cornmeal, digestibility of proteins [91]
Emmer L. plantarum, L. confusa, L. brevis, W cibaria, P. pentosaceus, L. rhamnosus Characterization of fermented emmer,
beverages		 [92]
Malt, barley, and barley mixed with malt L. plantarum, L. acidophilus Functional and organoleptic properties of cereal-based probiotic drinks [93]
Rice (red), barley buckwheat L. casei, L. paracasei, L. parabuchneri, L. buchneri, L. fermentum, L. coryniformis, L. rhamnosus, P. parvulus, W. oryzae, S. thermophilus Properties of cereal (red rice and barley)- and pseudocereal (buckwheat)-based substrates [94]
Mixture of cereals L. rhamnosus Rye, barley, amaranth, buckwheat, oat [1]
Mixture of cereals (rice, barley, emmer, oat) L. plantarum, L. rossiae, W. cibaria, P. pentosaceus Microbiological, textural, nutritional, and sensory properties of vegetable yogurt-like beverages [52]
Rice, millet Commercial starter culture (Bifidobacterium sp., L. acidophilus, S. thermophilus) Bacterial population, color, flavor, texture, and overall acceptability of the beverages, shelf-life [3]
Boza–Balkan drink (from cereals) L. plantarum, L. rhamnosus, L. pentosus. L. paracasei Antimicrobial activity, tolerance to gastric juice, bile salt hydrolase activity, adhesion to HT-29 and Caco-2 cell lines [95]
Currently, cereals and pseudocereals are considered potential raw materials for the production of plant-based nondairy fermented beverages. For experimental and industrial purposes, starter cultures with a known composition are used, which allows for the repeatability of the process [96][22][23][24]. The fermentation of cereal- and pseudocereal-based beverages is mostly carried out with the following LAB: Lactobacillus delbrueckii, Lactobacillus acidophilus, L. plantarum, Lactobacillus gasseri, Lactobacillus johnsonii, Lactobacillus paracasei, L. casei, Lactobacillus rhamnosus (now classified as Lacticaseibacillus rhamnosus), Lactobacillus fermentum (now classified as Limosilactobacillus fermentum), Lactobacillus reuteri (now classified as Limosilactobacillus reuteri), Lactobacillus helveticus, Lactobacillus lactis, Leuconostoc sp. (L. lactis subsp. cremoris, L. lactis subsp. lactis), Lactococcus sp. (L. cremoris, L. diacetylactis, L. intermedius), and Streptococcus thermophilus (Table 1). Most of these bacteria have been acknowledged as “generally recognized as safe”, which suggests that they pose no risk to the health of humans after consumption. Consuming LAB at an amount of 109 cells/day can have beneficial effects on health [97][84][88][21][38][98][99][100][101][102][66][69][87].
One of the issues studied is the production of fermented cereal- or pseudocereal-based beverages without the addition of thickeners or stabilizers. For this purpose, LAB producing exopolysaccharides (EPS) are studied (Table 1) [103][85][104][105][92][71][73]. EPS-synthesis is a strain-dependent metabolic characteristic, affected by the composition of the matrix and fermentation settings [106][86]. LAB can produce different types of EPS through the linking of different monosaccharides (mainly glucose, rhamnose, or galactose in the case of heteropolysaccharides) or the same polymeric unit (mainly glucose or fructose in the case of homopolysaccharides). The synthesis of EPS is correlated to LAB sugar metabolism, linking the anabolic pathway of EPS production, and the catabolic pathway of glycolysis [107]. The synthesis of EPS during the fermentation of cereal or pseudocereal beverages by lactic acid bacteria is crucial for obtaining a final product with proper texture. The advantages of EPS production during fermentation are not limited only to textural properties—they also include the enhancement of mouth-feel properties and water-holding properties [103][105][74].
Fermented plant-based beverages are often enriched with prebiotic oligofructose and inulin, which stimulate the growth of LAB [1][2][33][98][108][109][72]. Thus, some cereal- or pseudocereal-based beverages are advantageous over others due to the natural content of prebiotic substances, which in the case of cereal products include water-soluble fiber (e.g., β-glucan), oligosaccharides (galacto- and fructooligosaccharides), and resistant starch [2][22].

1.2. Changes in Carbohydrates Content

Beverages made from cereals or pseudocereals are an excellent matrix for the growth of LAB. As can be seen in the above discussion, the largest percentage of carbohydrates in cereals, pseudocereals, and their preparations used in the production of plant-based beverages is starch (Table 1). The process of amylolytic starch hydrolysis by enzymatic treatment, malting, or sprouting allows for the partial decomposition of starch and the release of sugars that are more easily fermented by LAB [81][83][110][111]. Starch is a plant polysaccharide formed by the condensation of D-glucose molecules linked by α-glycosidic bonds. It is not chemically homogeneous, and its structure can be divided into two fractions: amylose (essentially unbranched) and amylopectin (branched). The difference in the structure of individual starch fractions is related to the bonds linking the glucose molecules and the plant species. Amylose has only α-1,4-glycosidic bonds, while amylopectin also has α-1,6-glycosidic bonds, which enable branching [112]. During the germination of seeds, α- and β-amylases are released, which partially hydrolyze the α-1,4-glycosidic bonds of starch (but also glycogen), giving rise to maltose [81][83].
Furthermore, carbohydrates are formed as a result of starch hydrolysis, during the lactic acid fermentation of cereal and pseudocereal beverages. The content and type of carbohydrates formed depends on the cereal or pseudocereal used, the amount of water added, the thermal treatment applied during beverage preparation before fermentation, and the bacteria used for the fermentation process and process parameters [81][83][84][85]. However, the differences are mainly attributed to variations in the fermentation ability of LAB, resulting from their different biochemical activities (mainly saccharolytic activity and fermentation) [81][83][113][114].
LAB use carbohydrates as their major carbon source [114][115][116][117]. Glucose is the main energy source for living microorganisms, although some LAB also prefer fructose or lactose [117][118][119]. Glucose is also the primary carbohydrate used as a carbon source in the lactic acid fermentation process. It is a monosaccharide belonging to the group of aldohexoses, contains six carbon atoms, and is commonly found in nature. In turn, fructose is a monosaccharide belonging to the group of ketoses. It is identical in chemical formula to glucose but differs in structure. Fructose and glucose are components of the disaccharide sucrose (both linked by an α-1,4-glycosidic bond). Starch is known to be hydrolyzed by both lactic streptococci and lactobacilli. For example, Minerva et al. [115] reported that an acidophilic enzyme secreted from the cells of the strains from Lactobacillus plantarum (now classified as Lactiplantibacillus plantarum subsp. plantarum) hydrolyzed soluble starch, amylopectin, and to some extent amylose, without any effect on dextran and cyclodextrins. It is also known that the fermentation of starch results in the formation of other metabolites, including short-chain fatty acids (such as acetic, butyric, and propionic acid), which differ in their concentration and distribution based on the microorganisms used and carbohydrate content [116]. However, there are no data in the literature supporting that such LAB are used in industries for the production of plant-based beverages. It can be assumed that the biochemical activity of LAB will cause further changes in the carbohydrate content when the fermented cereal- or pseudocereal-based beverages are refrigerated for storage [81][83].
In general, during fermentation, the levels of carbohydrates and some indigestible poly- and oligosaccharides reduce in cereals and pseudocereals (Table 1). The raffinose group of oligosaccharides (RFO), which includes raffinose, stachyose, and verbascose, is an interesting group of oligosaccharides found in plant material, particularly grains and seeds. These oligosaccharides consist of two or more simple sugars linked together [120][121][122]. Raffinose is a trisaccharide with glucose, fructose, and galactose; stachyose is a tetrasaccharide composed of two galactose molecules, one fructose, and one glucose molecule; and verbascose is a pentasaccharide made up of four galactose and one fructose molecule. Several studies have confirmed the ability of LAB to ferment the oligosaccharides available in the plant matrix [123][114][124][125]. It has also been shown that LAB strains exhibit a high activity of enzymes such as α- and β-galactosidases [126][127][128]. Mital and Steinkraus [120] identified that α-galactosidase in lactobacilli is active at a pH of 4.5–8.0. The enzymatic activity often correlates with the catabolism of α-galactosidase, which is a characteristic of strains from L. plantarum and Lactobacillus casei subsp. casei (now classified as Lacticaseibacillus casei subsp. casei), while β-galactosidase activity is high in strains from species L. plantarum and Leuconostoc mesenteroides. Strains of L. plantarum and L. casei subsp. casei have been characterized with moderate-to-high galactosidase activity. Galactosugars are compounds that are resistant to the activity of enzymes in the digestive tract, but are used by microorganisms, including lactobacilli, during the process of lactic acid fermentation [42][122]. The above-mentioned strains have also been shown to hydrolyze RFO [120][121][122][124][125][126][127][128][129]. In fermented beans, the content of complex carbohydrates (stachyose, raffinose, verbascose) was found to be changed, but the degree of their reduction was determined by the type of microorganisms used in the fermentation process [123][130][60][61][131][132]. On the other hand, Granito et al. [131] demonstrated that, in addition to the bacteria used for fermentation, the parameters of the lactic acid fermentation process played a key role. The enzymatic degradation of stachyose and raffinose results in the formation of sucrose, fructose, and glucose, along with a change in the sweetness of the drink, its flavor, its profile of phenolics and flavonoids, and its antioxidant capacity. Similar effects can be expected in the case of fermented cereal and pseudocereal beverages, although there are no data in the literature regarding this subject.

1.3. Changes in the LAB Population

The number of live LAB is an important indicator of the quality of fermented beverages. A microbial cell count of 7–8 log CFU/mL indicates that the product has probiotic properties [81][83][82]. The primary criterion that ensures the health quality of the products is the viability of microorganisms from the starter culture (Table 1). Thus, the appropriate selection of starter cultures and storage parameters is essential to achieve final products with good organoleptic properties, which are determined by the metabolites formed during the fermentation process as well as during storage [81][83][38][100][133][134][94]. The effective growth of LAB during the fermentation of cereal- or pseudocereal-based beverages is dependent on the presence of significant amounts of mono- and disaccharides in the plant matrix.
Ziarno and Zaręba [38] investigated the viability of yogurt bacteria in rice-based beverages. The authors tested seven commercial freeze-dried yogurt starter cultures and noticed that the survival rate of lactobacilli was worse than streptococci, which may be due to the negative influence of antimicrobial substances derived from the plant matrix, low pH, and inappropriate refrigeration storage conditions [81][83][38][56][133][135][136][137][68][75]. As Němečková et al. [138] indicated, fermented plant-based beverages have a lower content of buffering substances compared to milk fermented with LAB, which is also reflected by the different dynamics of fermentation and the final pH values. Furthermore, the reduction in the number of bacterial cells during cold storage may have been caused by the production of antimicrobial compounds (e.g., hydrogen peroxide, bacteriocins, organic acids) by bacteria [1][81][3][83][84]. Although, the growth and viability of LAB are limited, at the same time this protects the final product against over-acidification during the distribution and refrigerated storage.
Using the L. rhamnosus GG strain, Kocková et al. [1] conducted an analysis on various parameters of fermentation such as pH, the number of bacterial cells, and the concentration of organic acids formed before and after 10 h of fermentation of 10 aqueous extracts obtained from a variety of cereals and pseudocereals (rye flour, rye grain, barley flour, whole grain barley flour, amaranth flour, amaranth grain, buckwheat flour, whole grain buckwheat flour, oat flour, millet grain). The authors noted that the studied strain grew in each of the tested cereal and pseudocereal substrates during the lactic acid fermentation process. In addition, the active metabolism and growth of LAB cells was observed from an initial value of 5.0–6.5 log CFU/g to a final value of 7.4–8.8 log CFU/g. During lactic acid fermentation, L. rhamnosus GG produced organic acids (lactic, acetic, and citric), causing a reduction in the pH value from 4.9–6.1 (initial) to 4.3–5.9 (final) [1]. In turn, during storage at 5 °C for 21 days, the population of L. rhamnosus GG and the pH value were found to be reduced (due to an increase in the concentration of lactic, acetic, and citric acids) [1]. In particular, a visible decrease in the L. rhamnosus GG population was observed in the samples obtained from buckwheat, rye, barley, and amaranth flours. Němečková et al. [138] also highlighted the negative effect of pH on the LAB population. The authors fermented beverages made from rice, rice, barley, and maize flours, supplemented with glucose (1%, w/w), to increase the content of fermentable carbohydrates. They used different LAB starters, including those from L. delbrueckii, L. fermentum, L. casei subsp. casei, L. paracasei subsp. paracasei, L. helveticus, L. gasseri, Lactococcus lactis subsp. lactis, L. lactis subsp. cremoris, L. lactis subsp. lactis biovar diacetylactis, and L. mesenteroides. Lactic acid fermentation was carried out at 37 °C (culture with lactobacilli) or 30 °C (culture with mesophilic bacteria). The course of lactic acid fermentation and the final pH of the fermented beverages (after 16 h of fermentation, pH of 3.7–4.5) depended on the LAB cultures used, while the final number of microbial cells was estimated at 7–8 log CFU/mL [82][138]. Similar observations were made by Ziarno et al. [78], who fermented millet-based beverages using a starter containing typical yogurt microflora (two species of LAB: L. delbrueckii subsp. bulgaricus and S. thermophilus). The authors found that the fermented drink had more than 6 log CFU/mL viable LAB cells after 28 days of storage at 6 °C.
The fermentation and biochemical activity of LAB cells, which are specific for type, species, and even strain, also translate into changes observed in the pH of fermented cereal- and pseudocereal-based beverages during cold storage (Table 1). Kowalska and Ziarno [83] reported that the following commercial yogurt starter cultures carried out the effective fermentation of buckwheat-based beverages for up to 5 h: ABY-3 (containing S. thermophilus, L. delbrueckii subsp. bulgaricus, L. acidophilus La-5, and Bifidobacterium animalis subsp. lactis BB-12), YO-MIX 207 (containing S. thermophilus, L. delbrueckii subsp. bulgaricus, L. acidophilus, and Bifidobacterium lactis), YO-MIX 205 (containing S. thermophilus, L. delbrueckii subsp. bulgaricus, L. acidophilus, and B. lactis), and VEGE 033 (containing S. thermophilus, L. delbrueckii subsp. bulgaricus, L. acidophilus NCFM, and B. lactis HN019). The lactic acid fermentation by each of these industrial cultures stabilized the final pH at a value below 5.0. Similar pH values were observed for a soybean beverage obtained after lactic acid fermentation [123][101]. On the contrary, Rathore et al. [93] showed that barley malt fermented with L. plantarum NCIMB 8826 and L. acidophilus NCIMB 8821 strains at 30 °C had a pH value of about 4.0. These differences in results may be related to the specificity of plant matrices, as well as the different bacterial cultures used in the studies.

2. The Importance of LAB for Properties of Cereal- and Pseudocereal-Based Beverages

2.1. Lipid Transformation

The biochemical activity of LAB is not just limited to carbohydrate fermentation. It is known that these bacteria have an intracellular system of hydrolytic enzymes, especially lipases and esterases, which catalyze the conversion of lipids and fatty acids released as triacylglycerides (TAGs) during the production of certain dairy products, such as rennet-ripened cheese [139][140][141][142]. The esterases and lipases of LAB can hydrolyze many free fatty acid esters such as tri-, di-, and monoacylglycerols. It should be noted, however, that these are intracellular enzymes; therefore, a long maturation time and subsequent bacterial cell lysis allow these enzymes to exhibit lipolytic activity during long-term maturation, which is observed in the production of ripened cheeses but not in the case of fermented beverages [143]. Pérez Pulido et al. [144] detected several strains that can exhibit lipolytic activity among lactobacilli, mainly heterofermentative strains of lactobacilli from Lactobacillus brevis (currently classified as Levilactobacillus brevis) and L. fermentum, although the observed lipolytic activity was limited to short- and medium-chain fatty acid esters. Akalin et al. [145] found that the esterified forms of linoleic acid also acted as substrates for the synthesis of conjugated linoleic acids (CLA) by the L. acidophilus La-5 strain in milk yogurts. Due to the metabolism of these bacteria, the content of the fatty acid isomer 18:2cis-9, trans-11 increased almost threefold in the tested products. This suggests that such activity should also be observed in cereal- and pseudocereal-based beverages. The results reported by Barampana and Simarda [146] agree with this assumption. The authors used L. plantarum strains to ferment beans and observed changes in the content of stearic, palmitic, oleic, linoleic, and linolenic fatty acids after 16 h of fermentation at 37 °C.
Lactic acid fermentation with lactobacilli also causes changes in the content of some fatty acids in the sn-2, sn-1, and sn-3 positions and the proportion of individual fatty acids in the sn-2 position. This is most likely due to the transesterification process carried out by these bacteria [147]. Lipases can act specifically on a particular fatty acid or more generally on a certain class of fatty acids. The positional specificity or regiospecificity of bacterial lipases is defined as the ability of these enzymes to distinguish between two outer positions (primary ester bonds, sn-1 and sn-3 positions) and the inner position (secondary ester bonds, sn-2 position) in the TAG backbone. For instance, sn-1,3-regiospecific lipases preferentially hydrolyze sn-1 and sn-3 positions before sn-2 when they hydrolyze triacylglycerols [147].

2.2. Contents of Vitamins

Although most LAB are auxotrophic to many vitamins, some are capable of biosynthesizing water-soluble vitamins such as B vitamins (including folic acid, B2, and B12) [79][148][149][150][151][152][153][154][155][156]. Taranto et al. [149] showed that L. reuteri CRL1098, isolated from sourdough, produced cobalamin, while Burgess et al. [150] genetically modified the Lactococcus lactis subsp. cremoris NZ9000 strain for riboflavin (vitamin B2) biosynthesis, although spontaneous LAB mutants are known to overproduce riboflavin [151]. Such starter strains could be used in the future to increase the content of vitamins in fermented plant-based beverages [152][153]. This is advantageous due to the fact that cereals and pseudocereals, which naturally contain various nutrients, including B vitamins (except vitamin B12), lose a significant amount of these bioactive substances during beverage processing. Lactic acid fermentation may change the content of B vitamins in cereal- or pseudocereal-based beverages, but the changes are influenced by the LAB strains capable of vitamin B biosynthesis, incubation conditions, and parameters used for the processing of plant-based materials into beverages. This has been proven for plant matrices other than cereals or pseudocereals [123][153][154][155][156][157].

2.3. Enzymatic Degradation of Phytates

Lactic acid fermentation may also provide optimal conditions for the enzymatic degradation of phytates present in cereal- or pseudocereal-based beverages as complexes with multivalent cations (e.g., iron, zinc, calcium, and magnesium). The enzymatic reduction of phytate complexes can even significantly increase the content and bioavailability of minerals, which has been confirmed for some types of flour- and experimental cereal-based beverages (Table 8) [158][79][159]. Microbial phytase can hydrolyze phytic acid salts during lactic acid fermentation, and low pH conditions and fermentation temperature can favor the activity of this enzyme. This was proven by Khetarpaul and Chauhan [79], who fermented pearl millet flour using L. brevis and L. fermentum cultures at 30 °C for 72 h. The authors noted a significant reduction in phytic acid as well as polyphenols (up to 83–88% and 80–91% of the initial content). This may improve not only the bioavailability of minerals but also the digestibility of proteins and carbohydrates. Nionelli et al. [34] examined the suitability of oat flakes for making functional beverages fermented with L. plantarum LP09. The researchers noted that fermentation increased the polyphenols’ availability and the antioxidant activity (by 25% and 70%, respectively).

2.4. β-Glucosidase Activities of LAB

A significant activity of LAB, related to some carbohydrates, as well as antioxidant capacity, is β-glucosidase activity [160][161]. β-D-glucosidases remove glucopyranosyl residues from the non-reducing end of β-D-glucosides by catalysing hydrolysis of the glycosidic bond [160]. Most β-glucosidases hydrolyse a broad range of substrates (i.e., phenols, polyphenols, and flavonoids). This way, the fermentations with LAB could increase the concentrations of phyto-oestrogens, bioactive isoflavones, and phenolic compounds in plant materials, leading to a significant contribution to the nutritional attributes of fermented plant food, cereal-, and pseudocereal-based beverages (Table 8) [162][163][164][165]. It is worth noting that β-glucosidase activity can release attractive flavor or fragrance compounds from the glucosylated precursors of fermented products and increases the bioavailability of health-promoting plant metabolites. Most of this type of research has been done on fermented soybean products or fermented vegetables [161][163][164][165].

2.5. The Digestibility of Proteins

The digestibility of proteins in cereal- or pseudocereal-based beverages can also be improved by a mechanism other than the breakdown of phytates or polyphenols (Table 8). Lactic acid fermentation of these beverages leads to changes in the levels of proteins and amino acids. The peptidase system of starter lactic acid bacteria has a major role on the liberation of free amino acids [52][166]. Furthermore, during acidification, the activation of cereal flour endogenous proteinases is observed [167]. For example, it has been shown that lactic acid fermentation increased the level of available lysine (a limiting amino acid for cereal proteins), methionine, and tryptophan in maize, millet, sorghum, and other cereals or pseudocereals [91][168]. However, Nanson and Field [91] observed that the levels of available (free) lysine, methionine, and tryptophan were dependent on the parameters of the lactic acid fermentation process when they studied the fermentation of corn flour. Similar effects and relationships can be expected for all fermented cereal- or pseudocereal-based beverages, but there are no literature data to support this hypothesis.

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Malgorzata Ziarno
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