Principal genera of the lactic acid bacteria .
The usage of lactic acid bacteria (LAB) in food as starters in fermentation technologies has a long tradition. Although the theorized idea of host‐friendly bacteria found in yoghurt has been formulated only over a century ago, both groups are widely used nowadays. Lactic acid bacteria alone or with special adjunct probiotic strains are inevitable for the preparation of various specific fermented and probiotic foods. Moreover, because of their growth and metabolism, the final products are preserved for a certain time. Growth dynamics of probiotic LAB and Fresco DVS 1010 in milk‐ and water‐based maize mashes with sucrose or flavours (chocolate, caramel and vanilla) were evaluated in this study. Although milk is typical growth medium for the LAB growth, observed strains showed sufficient growth in each of prepared mashes as well as they were able to maintain their content above 106 CFU ml-1 during storage period (6°C/21 d). Designed flavoured mashes were acceptable from the microbiological point of view, but according to the sensory evaluation they were provided with an attractive overall acceptability and are adequate alternative for celiac patients, people suffering from milk protein allergies or lactose intolerance.
- lactic acid bacteria
- functional products
For centuries, human civilization had used different approaches to preserve different types of food products. If we look back in history, we can find the preparation of different types of foods, for example, alcoholic beverages by ancient Egyptians, the preparation of yoghurt and kefir by the nomadic people from central Asia, fermentation of meat by the Germanic tribes and fish by the Eskimos, preparation of boza by the ancient Persians or fermenting maize by the native tribes in pre‐Columbian America . The earliest records about fermentation process were dated back to 6000 BC, and thus fermentation represents one of the oldest food preservation methods [2, 3]. The ancient people probably did not have any knowledge of microbiology, but in the middle of the nineteenth century, Louis Pasteur significantly contributed to the understanding of the fermentation process itself. He established the role of microorganisms and proved that there are many different kinds of fermentation . The original and primary purpose of fermentation was a preservation effect. Subsequently, with the development of many available preservation technologies, plenty of fermented foods were therefore manufactured because of their unique flavours, aromas and textures much appreciated to a consumer [4, 5]. Fermentation process created plenty of traditional food products, such as milk products (cheese, butter and yoghurt), fermented meat, plants and fruits (sausages, silage, sauerkraut, olives and grapes) and finally fermented cereal products such as bread and beer . Fermented food and beverages are defined as those that have been subjected to the effect of microbial enzymes, particularly amylases, proteases and lipases that cause biochemical transformation of polysaccharides, proteins and lipids to non‐toxic variety of desirable products with tastes, aromas and textures attractive to a consumer [4, 7].
In food fermentations, conditions of treatment and storage create an environment in which certain types of organism can flourish and these have a benign effect on the food rather than spoiling it. The majority of fermented foods is produced by the activity of lactic acid bacteria (LAB) and fungi, principally yeasts but also, to a lesser extent, moulds. Both groups of organisms share a common ecological niche, are able to grow under conditions of low pH and reduced water activity, although only lactic acid bacteria and facultative yeasts will prosper under anaerobic conditions. They frequently occur together in fermented products, dairy and non‐dairy, but in some cases, they play the role of a spoilage agent .
Microorganisms responsible for the fermentation process may be presented naturally in the substrate, or may be added as a starter and adjunct cultures .
2. Lactic acid bacteria
Lactic acid bacteria (LAB) represent an ubiquitous and heterogeneous species with common feature of lactic acid production as a result of sugar metabolism which leads to an acidification of the environment down to a pH of 3.5 . The monograph by Orla‐Jensen (1919) formed the basis of the present classification of LAB that take into account the cellular morphology, mode of glucose fermentation, growth temperature and sugar utilization possibilities . Taxonomically, LAB are divided into two distinct phyla:
Lactic acid bacteria are Gram‐positive, non‐sporulating, non‐pigmented and non‐motile rods and cocci, most of which are non‐respiring but aerotolerant anaerobes. They lack cytochromes and porphyrins and are therefore catalase‐ and oxidase‐negative. LAB tend to be nutritionally fastidious, often requiring specific amino acids, B‐vitamins and other growth factors. Some do take up oxygen through the mediation of flavoprotein oxidases, thus producing hydrogen peroxide and/or re‐oxidizing NADH during dehydrogenation of sugars. The cellular energy is derived from the fermentation of carbohydrates to produce major lactic acid. They use one of two different pathways and this provides a useful diagnostic feature in their classification. Since many species of lactic acid bacteria (LAB) and other food‐associated bacteria had a long historical association with human foods, they are recognized as generally regarded as safe (GRAS) bacteria. Infections by LAB are characterized as opportunistic that rely on host factors rather than on intrinsic pathogenicity. Only rare cases of clinical infections have been reported in humans, for example, in patients with endocarditis or with immune deficiency [8, 12–15].
Homofermentative organisms produce only lactic acid from the glucose fermentation during the Embden‐Meyerhof‐Parnas glycolytic pathway. Heterofermenters produce roughly equimolar concentration of lactate, ethanol/acetate and carbon dioxide from glucose (Table 1).
|Genera||Morphology||Fermentation||Lactate isomer||DNA (mole % G‐C)|
|Rods||Homo/hetero||d, l, dl||32–53|
2.1. Starters used in lactic acid fermentation
Many strains of
Twelve species of genera
Species from the genus
The most frequently found strains in the human gastrointestinal tract include
The most important species of
3. Antimicrobial compounds produced by lactic acid bacteria
Lactic acid bacteria may produce substances and thus create conditions harmful for undesired bacteria, yeasts and moulds which lead to the increase of food shelf life . Temperature and incubation period are the main factors modulating production of antimicrobial substances. Sathe et al.  in their study evaluated the impact of the growth phase on antimicrobial activity of
When lactic acid is produced, the pH decreases and consequently the organic acids or small fatty acids (SFAs) become undissociated and represent the main antimicrobial activity of the LAB . It has been shown that organic acids penetrate bacterial membrane of the target microorganism and inhibit transport mechanism in the cell by reducing pH values . The effect of acids depends not only in combination with lowering pH and reduction of redox potential but also on the type and concentration of acid presented in the environment . Acetic acid in comparison to lactic acid was described as being more effective, and is able to inhibit growth of moulds, yeasts and bacteria . Propionic acid inhibits moulds and selected Gram‐positive microorganism . Phenyllactic acid and pyroglutamic acid are able to inhibit growth of
Liptáková and co‐workers  focused on the growth of yoghurt contaminant
|Initial inoculation of
||Growth rate (log CFU ml-1 h-1)||Lag‐phase duration (h)|
3.1. Hydrogen peroxide
Most lactic acid bacteria produce hydrogen peroxide in the presence of oxygen. After its accumulation, inhibitory effect is mediated through oxidizing effect on membrane lipids and cell proteins of targeted microorganism. The antimicrobial activity of the compound in lower concentrations mostly in food is enhanced by treatment with the formation of hypothiocyanite catalysed by lactoperoxidase system . Fitzsimmons and Berry  reported in their study the inhibitory effect of hydrogen peroxide on the growth of
3.2. Carbon dioxide
Carbon dioxide at low concentrations may stimulate the growth of selected bacteria. Creating an anaerobic environment may be toxic to some aerobic food microorganisms through its action on cell membranes and its ability to reduce internal and external pH values .
Bacteriocins are ribosomally synthesized antimicrobial group of heterogeneous peptides with antimicrobial effect that kill or inhibit the growth of other bacterial strains. Typically, LAB bacteriocins have a narrow antibacterial spectrum, but some strains may also produce bacteriocins with a broad antibacterial spectrum. Selected lactic acid bacteria may inhibit the growth of Gram‐positive pathogenic and spoilage bacteria, as well as yeasts. It has been reported that bacteriocins also inhibit the growth of some Gram‐negative species. Lozo et al.  showed the production of bacteriocin 217 (Bac 217) by the strain
Reuterin is a product of glycerol fermentation produced during stationary phase by
4. Probiotics and functional foods
The word probiotic originated from Greek meaning ‘for life’. The first definition of probiotics was described by Vergin, 1954, as the opposite to antibiotics, and 1 year later Kolb proposed that the microbial imbalance in the human body as a result of antibiotic therapy could be restored by probiotics. Parker in 1974 defined the probiotics as organisms and substances that contribute to gut‐microbial balance. Most frequently cited definition is that of Fuller's (1992), who defined them as ‘a live microbial feed supplement, which beneficially affects the host animal by improving its intestinal microbial balance’. According to the recommendations of a Food and Agriculture Organization/World Health Organization (FAO/WHO)‐working group on probiotics suggested definition describes probiotics as live microorganisms that when administered in adequate amounts confer health benefit on the host (2002). Health benefits must be scientifically established by clinical studies in humans and published in peer‐reviewed journals . A number of genera and strains of bacteria (
The choice of which microbe to use as a probiotic is determined by many factors: probiotics have to be safe, non‐pathogenic and non‐toxic species, survive the passage through the intestinal tract and adhere to the intestinal mucosa and organic acid production, lactic and acetic [57, 79]. According to Tripathi and Giri , the viability of probiotics in food is affected by many factors such as pH, water activity, redox potential of foods, presence of salt, sugar, hydrogen peroxide, bacteriocins, aroma and colouring compounds, processing, packaging and storage conditions. Probiotic foods should preferably be stored at a temperature between 4 and 5°C. The highest viability of
The mechanisms of health‐improving properties of probiotics are still not completely understood, but their anti‐carcinogenic and anti‐mutagenic activity, the suppression of allergies, reduction of serum cholesterol level and reduction in blood pressure are known [12, 80, 92, 93].
4.2. Fermented cereals and pseudocereals functional products
Recently, there is an explosion of consumer's interest in functional foods; therefore, a key priority for food industry is the development of such products with a high quality and safety . The aim of these products is to have beneficial effect on host health affecting gut microbial composition subsequently with reducing the risk of chronic diseases . Cereals have been investigated in recent years regarding their potential use in the production of functional foods .
Possible application of cereals in functional food can be summarized as follows:
as fermentable substrates for the growth of probiotic bacteria (lactobacilli, bifidobacteria);
as prebiotics due to their content of non‐digestible oligosaccharides (galacto‐oligosaccharides and fructo‐oligosaccharides);
as dietary fibre promoting beneficial effects on human host;
Cereals have been and still are one of the most important sources of human diet  and are grown over 73% of total harvest area . A number of cereals are grown in different countries, including wheat, barley, oat, corn, rye, rice and millet, particularly important from an economical point of view. According to FAO's latest forecast, cereal production in 2015 stands at close to 2525 million tonnes but is still 1.4% below than the record in 2014 . Cereal grains and their derivatives represent an important nutritive component both in developed and in developing countries . They are considered as one of the most important sources of dietary proteins, carbohydrates (starch and fibre), vitamins (B group) and minerals for people all over the world .
4.2.1. Nutritional value of cereals
Cereal grains are primarily a source of carbohydrates, and thus a good source of energy . They form about two‐thirds up to three‐quarters of dry matter . Monosaccharides are the basic components of oligo‐ and polysaccharides and are most represented in the forms of hexoses (fructose, glucose and galactose) and pentoses, arabinose and xylose . Starch, the major component of cereal grains, occurs in starch granules of different sizes in endosperm.
Within common varieties, 25–27% of starch is presented as amylase and 72–75% represents amylopectin. However, in cereals a portion of the presented starch is not digested and absorbed in the small intestine. This is referred to as resistant starch and it appears to act in a similar way to a dietary fibre . A wide variety of biochemical processes occur in cereals during fermentation as a result of lactic acid bacteria. Fermentation process itself may lead to an increase in the content of reducing sugars, which was confirmed also in a study by Marko et al. . Simple carbohydrates are metabolized directly to organic acids and the glucose as a final product of starch metabolism is utilized immediately . Lambo et al.  described the decrease in starch content during fermentation of barley with lactobacilli.
Cereals are in general good sources of proteins. The proportions of essential amino acids and their digestibility mainly determine protein nutritional quality. Because of different production systems, environmental factors, as well as genotype, it is difficult to obtain comparative values of protein contents of different cereals. Thus, ranges of 5.8–7.7% of protein on a dry weight have been measured for rice, 8.0–15.0% for barley and 9.0–11.0% for maize. The amount of lysine, which is the limiting amino acid for all cereals, varies between species with the highest values in oat and rice and lowest in wheat and maize . The most represented is glutamic acid in the form of glutamine . Degradation and depolymerization of proteins during fermentation process depend not only on the metabolic activity of presented bacteria but also on enzymes that naturally occurred in cereals. Peptides are converted to amino acids by the activity of lactic acid bacteria by the specific intracellular peptidases that are subsequently converted to the specific products influencing the aroma and taste of final products . Antony and co‐workers  in their study pointed out that the fermentation process does not generally significantly change the total protein content of cereals. However, in the case of yeast corn fermentation, Cui et al.  found a significant increase (
Lipids are only a minor component of cereal grains with the amount varying from 1.7 to 7.0% on a dry mass basis, dependent on the type of cereal grain. The germ is the richest source of lipids. In particular, cereals are rich in essential fatty acids and contain only trace amounts of saturated fatty acids . Oxidation of lipids during fermentation process creates volatiles that contribute to the flavour of final products. Linoleic, oleic and linolenic acids are oxidized by lipoxygenases by forming hydroperoxides that are formed to aldehydes . Aldehydes are converted to alcohols by alcohol dehydrogenases during fermentation process . Antony et al.  in their study did not record any changes in the total lipid content during the millet fermentation with the endogenous microorganisms.
Cereals may contribute to vitamin intake due to the presence of most B‐vitamins and appreciable amounts of vitamin E. Wholegrain cereals also contain considerable amount of calcium, magnesium, iron, zinc, as well as lower levels of many trace elements, for example, selenium. The content of minerals ranges from 1.0 to 2.5% [113, 126]. Cereals contain relatively high levels of phytate (0.2–1.4%), concentrated mostly in the aleurone layer, which can bind minerals and there is an evidence of its decreased absorption in the presence of phytate, so minerals are not available to microorganisms. However, at a pH values less than 5.5, phytates are hydrolysed by endogenous phytases, thus minerals are released from the complex . In our investigation, changes in chemical composition of maize flours before and after expiry date were determined (Table 3). The percentage of starch and reducing sugars is one of the most important aspects showing the suitability of the tested substrate in fermentation technologies. A decline in the content of reducing sugars (60.1%) and starch (7.9%) was observed. Matejčeková and co‐workers  recorded a decline of reducing sugars in amaranth flours before and after expiry date of about 31% in their study.
In comparison to milk and dairy products, the nutritional quality of cereals and their products is sometimes inferior, or poor. The reason is the lower protein content in comparison to milk, limitations in the amounts of certain amino acids, notably lysine, and the presence of antinutritive compounds (phytic acid, tannins and polyphenols) and a coarse nature of grains [7, 127]. Cereals typically undergo a range of processes that change the nutritional content. Milling is the main process associated with cereals; also, extrusion is used to produce a variety of different types of products .
|3.21 ± 0.00||1.59 ± 0.03||68.71 ± 0.12||4.24 ± 0.01|
|4.46 ± 0.07||2.49 ± 0.00||63.30 ± 0.24||1.69 ± 0.01|
Helland et al.  studied the growth and metabolism of four selected probiotic strains in rice‐ or maize‐based puddings with milk or water. All four tested strains showed good growth and survival in cereal‐based puddings.
4.2.2. Fermented cereal and pseudocereal food and beverages
Fermented food and beverages are defined as those products that have been subjected to the effect of microbial enzymes, particularly amylases, proteases and lipases that causes biochemical transformation of polysaccharides, proteins and lipids to non‐toxic variety of desirable products with tastes, aromas and textures attractive to a consumer [4, 7]. Microorganisms responsible for the fermentation process may be presented naturally in the substrate, or may be added as a starter culture .
Traditional cereal‐ and pseudocereal‐fermented products are made of various kinds of substrates all over the world, mainly widespread in Asia and Africa. Fermentation may have multiple effects on the nutritional value of food .
The development of non‐dairy‐fermented products is a challenge to the food industry by producing high‐quality functional products. The main aims of cereal fermentation can be summarized as follows:
preservation, which relies mainly on acidification (production of lactic, acetic and propionic acid) and/or alcoholic production often in combination with reduction of water activity ;
enhances the safety of final products by the inhibition of pathogens ;
affecting sensory properties (taste, aroma, colour and texture);
improves the nutritional value by removing antinutritive compounds (phytic acid, enzyme inhibitors, tannins and polyphenols) and enhances the bioavailability of components;
reduces the level of carbohydrates as well as non‐digestible poly‐ and oligosaccharides .
Cereal fermentations affected by characteristic variables include the following:
the type of cereal determining the content of fermentable substrates, growth factors, nutrients, minerals, nitrogen sources and buffering capacity;
duration and temperature of fermentation process;
additional components (sugars, salt and exposure to oxygen);
Fermented cereal‐based products are prepared in different parts of the world, mainly in developing countries—Asia and Africa, in combination with legumes to improve overall protein quality of the final fermented products . Petruláková and Valík  evaluated the growth and metabolic activity of
|Fermented food/country||Raw material/substrate||Microorganism|
|Maize, millet, sorghum|
|Maize||Moulds, yeasts, bacteria|
|Maize, millet, sorghum|
As an example, the growth of Fresco DVS 1010 culture at 37 °C and the survival of probiotic strain
|Microorganism||Substrate corn flour||Gr
|Milk + caramel||0.446||–||-0.345|
|Milk + chocolate||0.563||–||-0.172|
|Water + caramel||0.508||0.59||-0.298|
|Water + chocolate||0.540||–||-0.462|
In botanical terms, amaranth, quinoa and buckwheat are not true cereals. They are dicotyledonous plants, and thus not cereals (monocotyledonous). Their seeds are in function and composition similar to true cereals, so they are referred as pseudocereals [136, 137]. Gluten‐free pseudocereals increased attention worldwide, because they represent alternative to conventional gluten‐containing cereals and industrially are used for the production of gluten‐free products, especially for celiac patients. They enrich the nutrition of health people and contribute to their balanced diet. In comparison to cereals, pseudocereals are characterized by the increased availability of proteins, as well as its higher content. Moreover, pseudocereals are the major source of minerals and vitamins, and in comparison to cereals, the content of essential amino acid lysine is higher [138–141].
Due to its chemical composition, amaranth is considered as one of the most nutritious plants that is easy to grow and over 60 species of amaranth are known worldwide . Grains are characterized with balanced composition of essential amino acids, especially lysine and methionine, higher content of proteins (15–17%) and starch (60–65%) [143, 144]. Compared to other cereals, the fat content is higher, ranging from 7 to 8%. Overall, amaranth is a good source of vitamins (riboflavin, niacin and vitamin E) and minerals such as calcium and magnesium . A growing number of studies have investigated the usage of amaranth in cereal technology not only in the production of nutrient‐rich gluten‐free products but also to enrich diet of health people . Several studies have also reported the possibility to enrich wheat‐based products with amaranth to improve the quality and overall nutritional value of final products . Matejčeková et al.  confirmed in their study the growth of probiotic and potentially probiotic strains (
|Substrate corn flour|
|Milk + caramel||-0.0031||–||8.57||7.91|
|Milk + chocolate||-0.0200||–||7.91||7.04|
|Water + caramel||-0.0033||141.78||8.27||7.65|
|Water + chocolate||-0.0093||–||7.47||7.03|
|Substrate buckwheat flour||Gr
|Milk + vanilla||0.251||2.7||6.80||8.02|
|Milk + caramel||0.641||1.1||6.25||8.49|
|Milk + chocolate||0.332||3.0||6.74||8.32|
|Water + vanilla||0.275||2.4||6.93||8.48|
|Water + caramel||0.580||–||6.12||8.40|
|Water + chocolate||0.258||1.3||6.76||8.49|
Together with amaranth, buckwheat and its products are studied in connection with celiac disease. Buckwheat was initially grown mainly in Asia and later has spread to Europe, Australia as well as to USA and Canada. The total carbohydrate content is 67–70%, of which 55% represents starch stored in the endosperm, as in common cereals. Buckwheat has a good content of thiamine, riboflavin and pyridoxine, and also represents a good source of minerals—magnesium, copper and potassium. It is characterized by a unique concentration of phytochemicals, in particular rutin, which has a positive effect on health especially in the prevention of cardiovascular diseases [148, 149]. Pelikánová et al.  evaluated the growth dynamics of
|Substrate buckwheat flour|
|Milk + vanilla||0.0006||–||8.54|
|Milk + caramel||-0.0002||–||8.42|
|Milk + chocolate||0.0009||–||8.89|
|Water + vanilla||0.0000||–||8.38|
|Water + caramel||-0.0002||–||8.41|
|Water + chocolate||0.0000||–||8.49|
As for the example, growth and fermentative metabolism of probiotic strain
The interest of consumers in fermented cereal‐ or pseudocereal‐based products is growing. The development of non‐dairy‐fermented products including probiotics may lead to enrichment of the diet in patients suffering from celiac disease, people with allergies, or intolerances, but it may contribute to the balanced diet of healthy subjects . If the cereal or pseudocereal products are presented with an attractive sensory taste, it may represent a suitable option for the development of new probiotic foods. Thus, in our study we evaluate the overall sensory acceptability of maize‐flavoured (chocolate/caramel) mashes (Figures 4 and 5). The overall acceptability was evaluated from 2.80 to 3.30 (four‐point scale) that indicated pleasant acceptance except caramel water mash (2.56). Kocková and Valík  noted negative effect of a 21‐day storage period on overall acceptability buckwheat product with salt fermented by probiotic strain
Sustainable diets and cultured consumer interests, for example, in personal health, represent the main driving forces for the development of new functional foods in the world. Throughout the world, many fermented foods that are produced cover a wide range of substances and microorganisms. Ensuring high quality and safety for such a product requires deep understanding of fermentation process, types and roles of microorganisms used and specific final product characteristics. Lactic acid bacteria are the alternatives of food biopreservation primarily due to the production of weak organic acids and other inhibitory substances in combination with lowering pH and reduction of redox potential. LAB and their metabolites are able to slow or inhibit the growth of undesirable bacteria, yeasts and toxigenic fungi in food. There is evidence that LAB are also able to reduce the gluten content of cereals that represents increasing problem for 0.5–1% of population worldwide. Many lactic acid bacteria and other microbial strains such as
The development of fermented cereal‐ or pseudocereal‐based products supplemented with probiotics represents an available alternative to milk products and may lead to enrichment of the diet of people suffering from celiac disease, allergy to milk proteins, lactose intolerance people or otherwise metabolically handicapped consumers, but it may also contribute to a balanced diet of healthy subjects.
The authors would like to thank for the financial contribution from the STU Grant scheme for Support of Young Researchers no. 1617/16.
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