Functional Properties of Microorganisms in Fermented Foods (2024)

Table 1

Probiotic Microorganisms

Probiotics are defined as live microorganisms that, when administered in adequate amounts, confer a health benefit on the host (Hill et al., 2014). Probiotic organisms used in foods must have the ability to resist gastric juices, exposure to bile, and be able to proliferate and colonize the digestive tract (Saad et al., 2013). The beneficial effects of probiotic foods on human health and nutrition are constantly increasing (de LeBlanc et al., 2007; Monteagudo-Mera et al., 2012), and probiotics are popularly using bio-ingredients in many functional fermented foods (Chávarri et al., 2010). The most commonly used probiotic bacteria belong to the heterogeneous group of LAB (Lactobacillus, Enterococcus) and to the genus Bifidobacterium, however, yeasts and other microbes have also been developed as potential probiotics during recent years (Ouwehand et al., 2002). Some popular commercial probiotic cultures which are available in global markets include Bacillus coagulans BC30 marketed by Ganeden Biotech, Inc., Cleveland, OH, USA; Lactobacillus acidophilus NCFM, Lactobacillus rhamnosus HN001 (DR20) and Bifidobacterium lactis HN019 (DR10) marketed by Danisco (Madison, WI, USA), L. casei strain Shirota and B. breve strain Yakult marketed by Yakult (Tokyo, Japan), L. fermentum VRI003 (PCC) marketed by Probiomics (Eveleigh, NSW, Australia), L. rhamnosus R0011 marketed by Institut Rosell (Montreal, QC, Canada), Streptococcus oralis KJ3 marketed by Oragenics, Inc. (Alachua, FL, USA), and Saccharomyces cerevisiae (boulardii) marketed by Biocodex (Creswell, OR, USA; US Probiotics Home, 2011).

Products containing probiotic bacteria generally include foods and supplements (Varankovich et al., 2015). Fermented milk products are the most traditional source of probiotic strains of lactobacilli (Bernardeau et al., 2006; Shah, 2015); however, commercial probiotic lactobacilli have also been added to meat products, snacks, fruit juice, etc. (Ranadheera et al., 2010). Probiotic properties of Lactobacillus plantarum isolated from kimchi, Korean fermented vegetable product, has been reported (Ji et al., 2013), and is also found to prevent the growth of Helicobacter pylori (Lim and Im, 2009). Probiotic strain L. acidophilus La-5 produces conjugated linoleic acid (CLA), an anti-carcinogenic agent (Macouzet et al., 2009). Pediococcus pentosaceus CIAL-86 isolated from wine shows anti-adhesion activity against Escherichia coli CIAL-153, indicating its probiotic potential in wine (García-Ruiz et al., 2014).

Antimicrobial Properties

Many species of LAB isolated from fermented vegetable and milk products have antimicrobial activities due to production of antimicrobial compounds such as bacteriocin and nisin (Tamang et al., 2009; Khan et al., 2010; Gaggia et al., 2011; Jiang et al., 2012; Grosu-Tudor and Zamfir, 2013). Many strains of LAB isolated from kimchi produce antimicrobial compounds such as bacteriocin by L. lactis BH5 (Hur et al., 2000) and L. citreum GJ7 (Chang et al., 2008), and pediocin by P. pentosaceus (Shin et al., 2008). Species of LAB isolated from kimchi show strong antimicrobial activity against Listeria monocytogenes, Staphylococcus aureus, E. coli, and Salmonella typhimurium (Lee et al., 2009). Weissella cibaria isolated from fermented cabbage product shows antimicrobial activity against Gram-positive and Gram-negative pathogens (Patel et al., 2014). Lactococcus lactis isolated from dahi, Indian curd, produces nisin Z that inhibits L. monocytogenes and S. aureus (Mitra et al., 2010). Several LAB species isolated from Romanian traditional fermented fruits and vegetables have antimicrobial activity against L. monocytogenes, E. coli, Salmonella, and Bacillus (Grosu-Tudor and Zamfir, 2013). Microorganisms as protective cultures, e.g., bacteriocin producers, may have several advantages, as they can contribute to the flavor, texture and nutritional value of the product besides the production of bacteriocin (Gaggia et al., 2011).

Antioxidant Activity

Antioxidant activities in fermented foods include 1,1-diphenyl-2-picryl hydrazyl (DPPH) radical scavenging activity, 2,2′-azino-bis (3-ethylbenzo-thiazoline-6-sulfonic acid; ABTS) radical scavenging activity, total phenol content (TPC) estimation, and reducing power assay (Liu and Pan, 2010; Abubakr et al., 2012). Many Asian fermented soybean foods have antioxidant properties, e.g., natto, Bacillus-fermented soybean food of Japan (Ping et al., 2012), chungkokjang and jang, fermented soybean foods of Korea (Shon et al., 2007; Shin and Jeong, 2015), douchi, a fermented soybean food of China (Wang et al., 2007a), kinema, Bacillus-fermented soybean food of India and Nepal (Moktan et al., 2008; Tamang, 2015), bekang and tungrymbai, Bacillus-fermented soybean foods of India (Chettri and Tamang, 2014), thua nao, Bacillus-fermented soybean food of Thailand (Dajanta et al., 2013), and tempe mold-fermented soybean food of Indonesia (Nurrahman et al., 2013). Antioxidant activities have also been observed in kimchi (Park et al., 2011) and yogurt (Sabeena et al., 2010).

Peptide Production

Bioactive peptides are formed during food fermentation by proteolytic microorganisms (De Mejia and Dia, 2010). In fermented foods peptides have some functional properties such as immunomodulatory (Qian et al., 2011), antithrombic (Singh et al., 2014), and antihypertensive properties (Phelan and Kerins, 2011). Species of Bacillus are involved in enzymatic hydrolysis of protein producing peptides and amino acids, which claim to have health benefits (Nagai and Tamang, 2010). Inhibitory properties of Angiotensin converting enzyme (ACE) have been studied in various fermented milk products such as kefir (Quiros et al., 2005), koumiss (Chen et al., 2010), yogurt (Papadimitriou et al., 2007), fermented camel milk (Moslehishad et al., 2013), cheese (Meyer et al., 2009), and fermented fish products (Ichimura et al., 2003).

Production of Enzymes by Microorganisms

Another important reason to ferment foods is to coax microorganisms into producing enzymes that also provide very useful services. During food fermentation microorganisms produce enzymes to break down complex compounds to simple bio-molecules for several biological activities such as proteinase, amylase, mannase, cellulase, and catalase in many Asian fermented soybean foods by Bacillus spp. (Tamang and Nikkuni, 1996; Chettri and Tamang, 2014). Common genera of mycelial fungi in fermented foods and beverages such as Actinomucor, Amylomyces, Aspergillus, Monascus, Mucor, Neurospora, and Rhizopus produce various carbohydrases such as α- amylase, amyloglucosidase, maltase, invertase, pectinase, ß-galactosidase, cellulase, hemi-cellulase; acid and alkaline proteases; and lipases (Nout and Aidoo, 2002). Taka-amylase A (TAA), an enzyme produced by Aspergillus oryzae in koji has many uses in industry (Suganuma et al., 2007). Dry, solid, cake-like mixed amylolytic starters used for alcohol production in the Himalayas have yeasts Saccharomycopsis fibuligera, S. capsularis and Pichia burtonii with high amylase activities (Tsuyoshi et al., 2005; Tamang et al., 2007).

Bacillus subtilis subsp. natto in natto produces nattokinase showing fibrinolytic activity (Mine et al., 2005; Kotb, 2012). Among bacteria isolated from fermented foods, B. subtilis and B. amyloliquefaciens (Chang et al., 2012; Zeng et al., 2013; Singh et al., 2014), Vagococcus carniphilus, V. lutrae, Enterococcus faecalis, E. faecium, E. gallinarum, and P. acidilactici (Singh et al., 2014), and Virgibacillus halodenitrificans SK1-3-7 isolated from fish sauce fermentation (Montriwong et al., 2012) produce fibrinolytic enzymes.

Increase in Isoflavones and Saponin and Production of PGA

Isoflavones are daidzein, genistein and glycitein, each of which exists in four chemical forms viz., aglycones, β-glucoside, acetylglucoside, and malonylglucoside in soybeans (Kudou et al., 1991). Isoflavone glucosides are hydrolyzed into their corresponding aglycones during fermentation of some Asian fermented soybean foods such as sufu and douchi of China (Wang et al., 2007b; Yin et al., 2007), miso and natto of Japan (Chiou and Cheng, 2001), chungkokjang and doenjang of Korea (Lee et al., 2007), tempe of Indonesia (Lu et al., 2009), and thua nao of Thailand (Dajanta et al., 2009). During tempe fermentation, isoflavone particularly Factor-II and aglycone contents are found to increase (Nakajima et al., 2005). Isoflavones in doenjang increase the activation of an LDL-C receptor, which is beneficial to prevent vascular diseases (Kwak et al., 2012).

Soybean saponins, which are oleanane triterpenoid glycosides, are again of two types viz., Group A and DDMP (2,3-dihydro-2,5-dihydroxy-6-metyl-4H-pyran-4-one; Paucar-Menacho et al., 2010). DDMP and their derivatives, Groups B and E saponins show health promoting benefits such as prevention of hypercholesterolemia (Murata et al., 2006), suppression of colon cancer cell proliferation (Ellington et al., 2006), and anti-peroxidation of lipids (Ishii and Tanizawa, 2006). Saponin contents are increased in natto, which are generated by Bacillus natto (Yanagisawa and Sumi, 2005). Kinema has high content of Group B saponin, which may indicate its health-promoting benefits to consumers (Omizu et al., 2011).

Poly-glutamic acid (PGA) is not synthesized by ribosomal proteins (Oppermann-Sanio and Steinbüchel, 2002), but is produced by some strains of Bacillus spp. in fermented soybean foods of Asia (Urushibata et al., 2002; Meerak et al., 2007; Nish*to et al., 2010; Chettri and Tamang, 2014). B. subtilis and B. licheniformis are widely used industrial producers of γ-PGA (Stanley and Lazazzera, 2005). It is safe eating the viscous materials of Asian fermented soybean foods since PGA is completely biodegradable and water-soluble and non-toxic to human (Yoon et al., 2000).

Degradation of Anti-nutritive Compounds

Some microorganisms present in fermented foods may degrade anti-nutritive substances and thereby convert the substrates into consumable products (Nout, 1994; Tamang, 2015). Various steps employed during the processing of gari and fufu, fermented cassava products of Africa, such as peeling, washing, grating, fermentation, dewatering and roasting minimizes the residual cyanide contents of the product (Babalola, 2014). Bitter varieties of cassava tubers contain the cyanogenic glycoside linamarin and lotaustralin, which are detoxified by species of Leuconostoc, Lactobacillus, and Streptococcus during traditional method to gari and fufu productions to yield hydrocyanic acid (HCN) which has low boiling point and escapes from the dewatered pulp during toasting rendering the product safe for human consumption (Lambri et al., 2013; Babalola, 2014; Bamidele et al., 2015). In tempe, Rhizopus oligosporus eliminates the flatulence causing indigestible oligosaccharides such as stachyose and verbascose into the absorbable monosaccharides and disaccharides (Hesseltine, 1983; Sanchez, 2008). Degradation of anti-nutritive compounds by B. subtilis has been reported in kinema (Sarkar et al., 1997). Phytic acid is reduced during fermentation of idli (Reddy and Salunkhe, 1980) and rabadi, a fermented cereal food of India (Gupta et al., 1992).

Table 2

Some bioactive compounds in fermented foods and their health benefits.

Synthesis of Nutrient

Enrichment of substrates with vitamins, essential amino acids, and bioactive compounds occur during food fermentation (Holzapfel et al., 1995; Steinkraus, 1996; Thapa and Tamang, 2015). In tempe, mold-fermented soybean food of Indonesia, contents of folic acid, niacin, riboflavin, nicotinamide and pyridoxine are found to be increased by Rhizopus oligosporus (Astuti, 2015), whereas vitamin B₁₂ is synthesized by non-pathogenic strains of Klebsiella pneumoniae and Citrobacter freundii (Liem et al., 1977; Okada, 1989; Keuth and Bisping, 1994). Contents of thiamine, riboflavin and methionine in idli, a rice-legume based fermented food of India and Sri Lanka enhance during fermentation (Ghosh and Chattopadhyay, 2011). Similarly, vitamins B complex and C, lysine and tryptophane, and iron contents have been found to increase during fermentation of pulque, an alcoholic drink of Mexico made from cactus plant (Ramirez et al., 2004). Riboflavin and niacin contents are increased in many Bacillus-fermented Asian fermented foods (Sarkar et al., 1998; Kim and Hahm, 2002; Nagai, 2015). Riboflavin and folic acid were found to be synthesized in kimchi by L. mesenteroides and L. sakei (Jung et al., 2013). Yeasts Saccharomyces cerevisiae, Candida tropicalis, Aureobasidium sp., and Pichia manschuria isolated from idli and jalebi, fermented cereal foods of India and Pakistan produce vitamin B₁₂ (Syal and Vohra, 2013). Free amino acids are increased in fermented soybean foods (Nikkuni et al., 1995; Sarkar and Tamang, 1995; Tamang and Nikkuni, 1998; Kiers et al., 2000; Dajanta et al., 2011).

Prevention of Hypertension and Heart Disease

Antihypertensive properties of many fermented milk products have been validated using animal models and clinical trials (Seppo et al., 2002; Sipola et al., 2002). Consumption of fermented milks or probiotic bacteria (Agerholm-Larsen et al., 2000) and fermented soybean foods (Liu and Pan, 2010) lowers the risk of heart diseases. Fermented whole grain foods can lower the serum LDL-cholesterol values, hypertriacylglycerolaemia, hypertension, coronary heart disease, insulin resistance, and hyperhom*ocysteinaemia (Anderson, 2003). Consumption of some fermented foods reduces the cholesterol level in tempe (Hermosilla et al., 1993), fermented soybean foods (Lee, 2004), and kefir (Otes and Cagindi, 2003). Calpis, the Japanese fermented sour milk containing two peptides VPP and IPP has shown hypotensive effect (Nakamura et al., 1996). L. helvetius in fermented milk reduces elevated blood pressure (Aihara et al., 2005; Shah, 2015). Monascus purpureus in fermented red-rice of China locally called angkak, prohibits creation of cholesterol by blocking a key enzyme, HMG-CoA reductase due to presence of mevinolin citrinin (Pattanagul et al., 2008).

Drinking of fermented tea of China prevents heart disease (Mo et al., 2008). Some Asian fermented soybean foods have antihypertensive properties as observed in natto (Nagai, 2015) and tempe (Astuti, 2015). Isoflavone in doenjang, mold-fermented soybean food of Korea, plays an important role in preventing cardiovascular diseases (Kwak et al., 2012; Shin et al., 2015). Fermented whole-grain intake appears to protect from development of heart disease and diabetes (Anderson, 2003). Moderate consumption of wine is healthier (Walker, 2014). Polyphenols in red wine probably are synergists of the tocopherol (Vitamin E) and ascorbic acid (Vitamin C), thus they inhibit lipid peroxidation (Feher et al., 2007). Regular consumption of the Korean fermented soybean foods by hypertensive and Type 2 diabetic patients results in favorable changes in cardiovascular risk factors (Jung et al., 2014) and reduction of hypocholesterolemic effect (Lim et al., 2014). ACEs inhibitory peptides derived from food proteins are used for treating hypertension (Jakubczyk et al., 2013). Fermented foods, which are rich in fibrinolytic enzymes, are useful for thrombolytic therapy to prevent rapidly emerging heart diseases (Mine et al., 2005; Singh et al., 2014).

Prevention from Cancer

Some LAB-fermented foods have antimutagenic and anticarcinogeinc activities (Lee et al., 2004). Kefir is used for the treatment of cancer (Otes and Cagindi, 2003; Yanping et al., 2009). Sauerkraut, fermented vegetable of Germany, contains s-methylmethionine, which reduces tumourigenesis risk in the stomach (Kris-Etherton et al., 2002). Consumption of fermented milk products containing live cells of L. acidophilus decreases ß-glucuronidase, azoreductase, and nitroreductase (catalyze conversion of procarcinogens to carcinogens), probably removes procarcinogens, and activate the immune system of consumers (Goldin and Gorbach, 1984; Macouzet et al., 2009). Similarly, Indian dahi has anti-carcinogenic property (Mohania et al., 2013). Cancer preventive potential of W. cibaria, and L. plantarum has been reported in kimchi (Kwak et al., 2014). Consumption of yogurt can reduce bladder, colon and cervical cancer has been observed (Chandan and Kilara, 2013).

Protection against Gastrointestinal Disorders

Lactic acid bacteria present in fermented foods may decrease number of incidence, duration and severity of some gastrointestinal disorders (Verna and Lucak, 2010). Administration of some strains of Lactobacillus improves the inflammatory bowel disease, paucities and ulcerative colitis (Orel and Trop, 2014). L. rhamnosus GG is effective in the treatment of acute diarrhea (Szajewska et al., 2007) and administration of L. helveticus-fermented milk in healthy older adults produced improvements in cognition function (Chung et al., 2014). Consumption of fermented milk products containing live bacteria has immunomodulation capacity (Granier et al., 2013), and cures diarrhea (Balamurugan et al., 2014). Korean kimchi is suitable for control of inflammatory bowel diseases (Lim et al., 2011).

Anti-allergic Reactions

Lactobacillus kefiranofaciens M1 isolated from kefir grains has an anti-allergic effect (Hong et al., 2010). Digestion of caseins during maturation of fermented milk products has shown to facilitate loss of allergenic reactivity thus increases tolerance (Alessandri et al., 2012). Chongkokjang has anti-allergic effect such as dermis thickness, decreased ear thickness, auricular lymph node and infiltrating mast cells (Lee et al., 2014). Lactobacillus species isolated from kimchi are found to modulate Th1/Th2 balance by producing a large amount of IL-12 and IFN-γ with ability to alleviate atopic dermatitis and food allergy (Won et al., 2011). Fermented fish oil, which is rich with Omega-3 polyunsaturated fatty acids, can reduce sensitization of allergy (Han et al., 2012).

Protection from Diabetes and Osteoporosis

Intake of high fiber foods may decrease the insulin requirements in diabetic persons (Meyer et al., 2000), and may increase the sensitivity to insulin for non-diabetic persons (f*ckagawa et al., 1990; Anderson, 2003). Probiotic dahi-supplemented diet significantly delays the glucose intolerance, hyperglycemia, hyperinsulinemia, oxidative stress and dyslipidemia indicating a lower risk of diabetes (Yadav et al., 2007). Daily consumption of chungkokjang may increase the insulin resistivity thus controls diabetics (Shin et al., 2011; Tolhurst et al., 2012).

Vitamin K2 present in natto stimulates the formation of bone, which may help to prevent osteoporosis in older women in Japan (Yanagisawa and Sumi, 2005). Mineral such magnesium, calcium, phosphorus, potassium, and also protein present in yogurt may function together to promote formation of healthy bones (Chandan and Kilara, 2013).

Alleviation of Lactose Malabsorption

Some people suffer from lactose malabsorption, a condition in which lactose, the principal carbohydrate of milk, is not completely digested into glucose and galactose due to lack of ß-D-galactosidase (Shah, 2015). L. delbrueckii subsp. bulgaricus and S. thermophilus used in production of yogurt contain substantial quantities of ß-D-galactosidase which improve the symptoms of lactose malabsorption in lactose intolerant people (Shah et al., 2013). Consumption of fresh yogurt (with live yogurt cultures) has been demonstrated better lactose digestion and absorption than with the consumption of a pasteurized product (Pedone et al., 2000). Kefir can minimize the symptoms of lactose intolerance by providing extra source of β-galactosidase (Hertzler and Clancy, 2003).

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