Yantyati Widyastuti
Andi Febrisiantosa
Flavio Tidona- 1Research Center for Biotechnology, Indonesian Institute of Sciences (LIPI), Cibinong, Indonesia
- 2Research Division for Natural Product Technology, Indonesian Institute of Sciences (LIPI), Yogyakarta, Indonesia
- 3Council for Agricultural Research and Economics–Research Center for Animal Production and Aquaculture (CREA-ZA), Lodi, Italy
Bacteria of the genus Lactobacillus have been employed in food fermentation for decades. Fermented dairy products, such as cheese and yogurt, are products of high value known as functional food and widely consumed due to their positive health impact. Fermentation was originally based on conversion of carbohydrate into organic acids, mostly lactic acid, intended to preserve nutrient in milk, but then it develops in other disclosure of capabilities associates with health benefit. It is expected that during the manufacture of fermented dairy products, some bioactive peptides from milk protein are released through proteolysis. Lactobacilli have been recognized and received increasing attention as probiotics by balancing gut microbial population. Information of molecular mechanisms of genome sequence focusing on the microbial that normally inhabit gut may explain as to how these bacteria positively give impact on improving host health. Recent post-biotics concept revealed that health benefit can also be associated after bacterial lysis. This mini review focuses on the contribution of lactobacilli in dairy fermentation with health-promoting properties on human health.
Introduction
Fermented foods represent a distinct food culture in every community in the world, symbolizing the heritage and socio-cultural aspects of the people (Tamang et al., 2016). The practice of consuming fermented foods has prevailed across civilizations and strata of societies over centuries because there is an obvious tangible benefit to the consumers of such products (Bagchi, 2014). Recent situation corroborates the statement regarding consumption of fermented food as healthy food which plays an important role in the maintenance of human health condition. Currently, this turned out to be a modern lifestyle.
Lactic acid bacteria, particularly genus Lactobacillus, have been involved and employed in food microbiology especially in the fermentation of milk due to their high potential to produce important metabolites and improve the quality of the product. Moreover, lactobacilli have been documented to have a long history of safe use, supported by recognition of Generally Recognized as Safe by the Food and Drug Administration or Qualified Presumption of Safety by European Food Safety Authority (Bernardeau et al., 2008). In addition, lactobacilli offer exciting research prospects for acquiring fundamental knowledge of how bacterial cells function in the gut ecosystem (Tannock, 2004). Taxonomy and phylogeni of the genus Lactobacillus have been recognized as rather complicated, because of great number of species with a diverse group of species originated from several nutrient-rich niches. Placement and grouping of existing species of Lactobacillus have been done based on the technology that has been developed such as reverse transcriptase sequencing of 16S rRNA (Collins et al., 1991) and genomics sequencing (Salvetti et al., 2012; Sun et al., 2015; Wittouck et al., 2019).
The health benefits of fermented foods may be expressed either directly through the interactions of ingested live microorganisms with the host, as probiotic effect, or indirectly as the result of the ingestion of microbial metabolites synthesized during fermentation as biogenic effect (Wilburn and Ryan, 2016). The effects of some fermented dairy products on human health may vary depending on the species and the fermentation processes. For instance, Lactobacillus helveticus can potentially affect human health through direct mechanisms such as the inhibition of pathogens, modification of gut microbiota and modulation of the host immune system (Taverniti and Guglielmetti, 2012). There are several effects on biological activities of Lacticaseibacillus casei strain Shirota as probiotics when consumed orally as live cells. Their modulating effect on intestinal function and other metabolites has been thought to be their primary benefit for human health mainly on improvement of intestinal function. Moreover, consumption of L. casei strain Shirota is very safe, not only for healthy subjects, but also for patients with a variety of diseases and conditions (Miyazaki and Matsuzaki, 2008). Health-promoting effects of fermented milk of L. helveticus IDCC3801 is shown through improvements of the cognitive function of the elderly people, as assessed by self-rating scales, cognitive tests, and biomarker analysis (Chung et al., 2014). While Jauhiainen et al. (2010) reported that long-term intervention with L. helveticus fermented milk reduces augmentation index in hypertensive subjects.
Taxonomy and Characteristics of Lactobacilli
The genus Lactobacillus is classified in the phylum Firmicutes, class Bacilli, order Lactobacillales, and family Lactobacillaceae. Within the family Lactobacillaceae, genus Lactobacillus represents the largest and most diverse group as indicated by great number of its species, which reaches 261 species (Zheng et al., 2020). Additional of proposal of new species of this genus has increased rapidly especially in the last 20 years. Thus, reclassification of the genus Lactobacillus based on core genome phylogeny (conserved) pairwise average amino acid identity, clade-specific signature genes, physiological criteria and the ecology have been undertaken. Reclassification of the genus Lactobacillus into 25 genera including the emended genus Lactobacillus have been referred to as the Lactobacillus delbrueckii group, Paralactobacillus, and 23 novel genera for which the names Holzapfelia, Amylolactobacillus, Bombilactobacillus, Companilactobacillus, Lapidilactobacillus, Agrilactobacillus, Schleiferilactobacillus, Loigolactobacilus, Lacticaseibacillus, Latilactobacillus, Dellaglioa, Liquorilactobacillus, Ligilactobacillus, Lactiplantibacillus, Furfurilactobacillus, Paucilactobacillus, Limosilactobacillus, Fructilactobacillus, Acetilactobacillus, Apilactobacillus, Levilactobacillus, Secundilactobacillus, and Lentilactobacillus are proposed (Zheng et al., 2020). This new Lactobacillus taxonomic classification may facilitate our understanding of common mechanisms that could mediate probiotic health benefits. Division the genus Lactobacillus based on certain physiological and metabolic properties is timely that can anticipate the addition of new species in the near future.
Lactobacilli are characterized as Gram-positive bacteria with negative reaction to catalase, non-motile, and non-spore forming rods or coccobacilli often in chain configuration with their G+C content usually below 50 mol% (Hammes and Vogel, 1995). Based on the ability to ferment carbohydrate, they are divided into species of homofermentative and heterofermentative, that convert carbohydrate into lactic acid, and lactic acid, acetic acid, ethanol, and CO2, respectively. Lactose catabolism is the most relevant subject area of study related to metabolism in milk fermentation.
Recently, sequencing of whole bacterial genomes revealed important traits in characterization. Functional genomics approaches in lactobacilli, that are associated with food and health, rely on its complete genome sequence (Douillard and de Vos, 2014). It is also emphasized that genomic information allowed a better comprehension of lactobacilli features such as their physiology, metabolic capabilities, probiotic potential, key gene features, and niche adaptation. Regarding the safety of lactobacilli strains as probiotics, their assessment should be performed using the most updated methodology (Salvetti et al., 2012). Some lactobacilli have been reported as strains with high probiotics potential and support efforts to improve probiotics quality such as Ligilactobacillus salivarius strains BCRC14759 and BCRC 12574 with the highest exopolysaccharide (EPS) production (Chiu et al., 2017), Lactobacillus johnsonii ZLJ010 with better adaptation to the gut environment and its probiotic functionalities (Zhang et al., 2019), and Lactobacillus helveticus D75 and D76 that are able to inhibit the growth of pathogens and pathobionts (Toropov et al., 2020).
Lactobacilli in Fermented Dairy Products
The basic fermentative process carried out by lactobacilli can already deliver dairy products with enhanced nutritional properties, as they are able to remove antinutritional factors (mainly lactose and galactose, preventing lactose intolerance, or galactosemia), increase the digestibility and the biological value of the proteins. Lactobacilli strains generally employed as starter cultures show optimal growths in milk although they may display limited biosynthetic abilities compared to wild strains (Settanni and Moschetti, 2010). This is the reason why dairy LAB are defined as “domesticated” strains, revealing the loss of ancestral genes and metabolic simplification toward adaptation to a given environment, as confirmed by comparative genome analysis of multiple species (McAuliffe, 2018).
Notwithstanding, lactobacilli harbor a huge phenotypic and genetic diversity, that is extensively investigated to select strains exhibiting traits of interest. Commercial starter cultures are able to deeply influence the flavor and texture of the product through the breakdown of milk proteins, fats, and other milk constituents (Giraffa et al., 2010). Conversely, lactobacilli can also improve the quality characteristics of the fermented products through specific biosynthetic capabilities, such as the synthesis of thickening hydrocolloids (exopolysaccharides) that enable to deliver yogurts with ameliorated rheological properties (Torino et al., 2015). However, the largest success of lactobacilli in fermented dairy products is assigned to probiotics, that may responsible of the fermentation process together with associated starter cultures or added as adjunct cultures. Ancient people in Asia were proficient in practicing or making fermented milk in a simple way and nowadays they are still produced under the name of traditional fermented milks. The reason of such practice can be due to limited facilities and possibility to use pure starter cultures. Fermentation in these products is generally driven by unidentified indigenous microorganisms derived from the residual milk of previous day. Fermented milk products of Asia including Dahi, a yogurt-like from India, or Dadih from Indonesia, Kumys, originated from Central Asia and Tarag or Airag, a hard-type yogurt from inner Mongolia. Among the mix microorganisms present in Kumys there are Lactobacillus delbrueckii subsp. bulgaricus, Lactobacillus kefiranofaciens, Lactobacillus acidophilus, Lactococcus lactis and yeasts, such as Candida spp., Kluyveromyces lactis, and Torula spp. Tarag is considered to be a rich source of vitamins and minerals (Akuzawa et al., 2011). Whereas, L. helveticus and L. kefiranofaciens were isolated from Airag and L. delbrueckii subsp. bulgaricus, L. helveticus, and Streptococcus thermophilus were the predominant isolates from Tarag (Watanabe et al., 2008). Meanwhile, Yakult and Calpis were developed in Japan. Yakult is well-known fermented milk product on account of various claims of its health-promoting properties. The strain used in Yakult manufacture, L. casei strain Shirota (reclassified as Lacticaseibacillus paracasei subsp. paracasei), is an indigenous human intestinal bacterium, able to resist gastric juices and bile. Calpis, which originated from the fermented milk of Mongolian nomads, contains several peptides derived from milk proteins, claiming a physiological effect on lowering of blood pressure in hypertensive human subjects (Akuzawa et al., 2011). The ability of specific indigenous lactobacilli enabled to develop successful industrial products from traditional fermented milks. In Europe, fermented milks were traditionally prepared and consumed, especially from northern Scandinavia. The main characteristic of these products is the slimy texture of the milks caused by presence of ropy exopolysaccharides and today commercial products based on old starter cultures are manufactured such as “Tjukkmjølk” in Norway, “Långfil” in Sweden, “Viili” in Finland, and “Skyr” in Iceland (Fondén et al., 2006). In eastern Europe and Mediterranean area (ancient Greece and Rome) the production of low alcoholic fermented drinks were used both for nourishment and medicines to relieve pain and to prevent or treat diseases (Marshall and Mejia, 2011). Koumiss, a traditional alcoholic fermented beverage of Kazakh nomads made from mares' milk had been used by Russian doctors for the treatment of tuberculosis and diarrhea (Baschali et al., 2017). Only many years later the presence of lactobacilli with probiotic properties was demonstrated.
Main species identified with probiotic properties belong to Lacticaseibacillus rhamnosus Lactobacillus acidophilus and Lacticaseibacillus casei and Lactiplantibacillus plantarum that are generally found in yogurts, kefir and other fermented milks (Table 1). The efficacy of probiotic lactobacilli was also evaluated in cheeses, although the survival of cells through processing and aging may be more challenging, providing positive mucosal immune responses in vivo, in a mice model (Medici et al., 2004). There are also various application of Lactobacilli strains in the dairy products that have been developed for human health therapy as reported in Table 1.
Table 1. Beneficial effect of probiotic dairy products to human health.
Fermented Dairy Products as Functional Food
Lactobacilli are able to produce an array of metabolites that may be useful to enrich the fermented food, increasing the health-associated value. Among the biologically active metabolites produced after fermentation, a major role is played by bioactive peptides, that are encrypted within milk proteins and made available by the proteolytic system of lactobacilli. Milk proteins are currently considered a relevant source of bioactive peptides but only the strain that possess specific cell envelope proteases and peptidases are able to release oligopeptides or peptides that exert a specific activity, based on the amino acid composition and sequence (Hafeez et al., 2014). The demonstrated presence of such peptides in a fermented product enables to define the category of functional foods, which provide health benefits beyond its nutritional value. One of the first functional dairy food was a soft drink fermented by Lactobacillus helveticus CP790 and a strain of Saccharomyces cerevisiae with antihypertensive effects, although several other products, each with a specific health claim, have been launched into the market (Tidona et al., 2009). These peptides are generally tasteless but those containing hydrophobic amino acids may result bitter, thus it also has to be taken into account. Some rare strains of lactobacilli produce inulin, a prebiotic that is also reported to improve the quality of skim milk fermented by L. acidophilus, L. rhamnosus, Lactobacillus bulgaricus (Patel and Goyal, 2012). A functionalized yogurt was developed using selected strains of L. bulgaricus (associated to S. thermophilus) which naturally increased the folate concentration by almost 250% (Laiño et al., 2013). Besides peptides and vitamins, many other bioactive metabolites can also be synthetized during fermentation, such as bacteriocins and enzymes that could be exploited to produce natural food ingredients. Functional oligosaccharides (GOS and FOS) have been found effective in the prevention of dental caries, facilitation of mineral absorption, antioxidant properties, enhancement of immunity and alternative regulators of blood glucose in diabetics (Patel and Goyal, 2011). The ability of a specifically selected strains may be addressed to provide an added-value to fermented products or to diversify product range, which is the key to implement successful strategies. In other cases, the presence of virtuous lactobacilli is associated to health-promoting properties, such as immune-stimulatory antitumoral effects (Nishimura, 2014) or to lower cholesterol level (Jones et al., 2012). Among fermented milks, Kefir can be naturally considered a functional food given the numerous reports claiming for positive effects, i.e., anti-allergenic, cholesterol metabolism, angiotensin converting enzyme (ACE) inhibition, wound healing, anti-carcinogenic, antimicrobial and gastrointestinal health (Bourrie et al., 2016), although its microbial composition is rich of different LAB species and yeasts.
Metabolism in Lactobacilli: from Probiotics to Post-biotics
The effectiveness of probiotics is related to specific strains, a minimum dosage of viable cells and the specific health claim, according to the World Gastroenterology Organization guidelines. When probiotics are considered dietary supplements, there should be sound scientific evidences for the use of a strain and the beneficial effect claimed; analogously, for probiotic drugs, clinical trials for a specific treatment or disease associated to the presence of a strain should be demonstrated, in compliance with drug legislation (García-Burgos et al., 2020). One of the most common use of probiotics is defined by the cure of Helicobacter pylori infection with Lactobacilli, even in pediatric age, prevention of allergies, treatment of chronic disease irritable bowel syndrome, treatment of inflammatory bowel disease, treatment of vaginitis, and generally suggested after the use of antibiotics (McFarland, 2015). The global market of probiotics is still the largest in the section of functional food and it comprises a huge variety of food products where probiotics are added, mainly to dairy products (yogurts, fermented milks, ice creams, and cheeses), even if the application involving non-dairy matrices (plant-based fermented products, juices, and vegan products) are rapidly emerging. The main role of probiotics is the ability to modulate the intestinal microbiota, although this complex mechanism is still poorly understood. However, it was observed how probiotic lactobacilli promote the growth of beneficial bacteria against harmful microorganisms, such as Echerichia coli, Listeria monocytogenes, Staphylococcus aureus, Salmonella typhimurium, Salmonella enteritidis, Shigella flexneri, Pseudomonas aeruginosa, and Yersinia enterocolitica (Bourrie et al., 2016). In commercial applications, when viability of probiotic cultures is concerned, the beneficial effect of the product may be compromised. In addition to this drawback, starter cultures combined to probiotics in fermented products can possess antibiotic resistance genes that may be potentially transferred to pathogen microorganisms (Hummel et al., 2007). Therefore, current research has also investigated the efficacy of the microbial metabolism of probiotic lactobacilli, devoid of the live cells. The term paraprobiotics, also called inactivated probiotics or ghost probiotics, was introduced to refer to non-viable microbial cells or to raw cellular extracts which, administered orally or topically in adequate amounts, are able to confer health benefits (Taverniti and Guglielmetti, 2011). The concept of post-biotics can also be extended to bioactive metabolites or their cell-free supernatants, that are considered a safe and effective alternative, in comparison to live bacteria, to maintain gut health and to prevent inflammatory bowel diseases. Several strains of L. plantarum are reported to exhibit post-biotic effects, such as those producing bacteriocins employed as antibiotic replacers in the feed of poultry and rats (Foo et al., 2003; Thanh et al., 2009). Post-biotics from L. plantarum also showed cytotoxic effects and induction of apoptosis against malignant cancer and they were proposed as supplement or adjunctive treatment for cancer (Chuah et al., 2019). There are already post-biotics applications in pharmaceutical products, which were legally approved with success, both for medical, veterinary, and food purposes. Several strains (L. acidophilus, L. plantarum, L. rhamnosus, L. bulgaricus, L. salivarius, L. casei, L. reuteri, L. sporogenes, B. bifidum) are commercialized as immunomodulatory supplements. The bioactive metabolites commonly found in post-biotics can be related to organic acids, short-chain fatty acids, carbohydrates, antimicrobial peptides, enzymes, vitamins, cofactors, immune-signaling compounds, and complex agents (Moradi et al., 2019). Post-biotic products are generally more convenient than probiotics due to industrial advantages, as they are stable in a wide range of pH and temperature, often do not require cold-chain, extended shelf-life and little interaction with the matrices (Barros et al., 2020). Furthermore, post-biotics were applied in food active packaging, especially through the incorporation of bacteriocins produced by LAB in antimicrobial films. For instance, the strain of L. lactis ATCC 11454 producing nisin was incorporated in active films based on alginate and collagen, showing a strong inhibition vs. List. monocytogenes, Staph. aureus, and E. coli. (Ma et al., 2020).
Conclusion
Lactobacilli, that hold a long history of safe use, are still of great importance for the dairy fermentations. With the recent and growing information on their genome sequences, the role of lactobacilli in fermentation can be optimized and tailored, giving insights into new product development. The production of bioactive peptides by lactobacilli, although limited to a few strains, represent the most important driver to produce functional foods with specific health claims. The pharmaceutical biotechnology based on the use of lactobacilli with probiotics properties, are highly supported by the evidence of health benefits to the host. On the other hand, post-biotics from lactobacilli, which refer to non-viable microbial cells or their raw cellular extracts are also important emerging alternatives with health-promoting effects.
Author Contributions
YW, AF, and FT reviewed the literature and wrote the manuscript. AF summarized and prepared the table. All authors approved the submitted version.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Ahola, A. J., Yli-Knuuttila, H., Suomalainen, T., Poussa, T., Ahlström, A., Meurman, J. H., et al. (2002). Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch. Oral Biol. 47, 799–804. doi: 10.1016/S0003-9969(02)00112-7
Akuzawa, R., Miura, T., and Surono, I. S. (2011). “Asian Fermented Milks,” in Encyclopedia of Dairy Sciences, eds J. W. Fuquay, P. F. Fox, and P. L. H. McSweeney (San Diego, CA: Academic Press), 507–511. doi: 10.1016/B978-0-12-374407-4.00186-2
Almeida, C. C., Lorena, S. L. S., Pavan, C. R., Akasaka, H. M. I., and Mesquita, M. A. (2012). Beneficial effects of long-term consumption of a probiotic combination of Lactobacillus casei shirota and Bifidobacterium breve yakult may persist after suspension of therapy in lactose-intolerant patients. Nutr. Clin. Pract. 27, 247–251. doi: 10.1177/0884533612440289
Anukam, K. C., Osazuwa, E. O., Osadolor, H. B., Bruce, A. W., and Reid, G. (2008). Yogurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhea and increases CD4 count in HIV/AIDS patients. J. Clin. Gastroenterol. 42, 239–243. doi: 10.1097/MCG.0b013e31802c7465
Ao, X., Zhang, X., Zhang, X., Shi, L., Zhao, K., Yu, J., et al. (2012). Identification of lactic acid bacteria in traditional fermented yak milk and evaluation of their application in fermented milk products. J. Dairy Sci. 95, 1073–1084. doi: 10.3168/jds.2011-4224
Bagchi, T. (2014). Traditional food & modern lifestyle: impact of probiotics. Indian J. Med. Res. 140, 333–335.
Barnes, D., and Yeh, A. M. (2015). Bugs and guts: practical applications of probiotics for gastrointestinal disorders in children. Nutr. Clin. Pract. 30, 747–759. doi: 10.1177/0884533615610081
Barros, C. P., Guimaraes, J. T., Esmerino, E. A., Duarte, M. C., Silva, M. C., Silva, R., et al. (2020). Paraprobiotics and postbiotics: concepts and potential applications in dairy products. Curr. Opin. Food Sci. 32, 1–8. doi: 10.1016/j.cofs.2019.12.003
Baschali, A., Tsakalidou, E., Kyriacou, A., Karavasiloglou, N., and Matalas, A. L. (2017). Traditional low-alcoholic and non-alcoholic fermented beverages consumed in European countries: a neglected food group. Nutr. Res. Rev. 1, 1–24. doi: 10.1017/S0954422416000202
Beausoleil, M., Fortier, N., Guénette, S., L'ecuyer, A., Savoie, M., Franco, M., et al. (2007). Effect of a fermented milk combining Lactobacillus acidophilus Cl1285 and Lactobacillus casei in the prevention of antibiotic-associated diarrhea: a randomized, double-blind, placebo-controlled trial. Can. J. Gastroenterol. 21, 732–736. doi: 10.1155/2007/720205
Bengoa, A. A., Iraporda, C., Acurcio, L. B., de Cicco Sandes, S. H., Costa, K., Moreira Guimarães, G., et al. (2019). Physicochemical, immunomodulatory and safety aspects of milks fermented with Lactobacillus paracasei isolated from kefir. Food Res. Int. 123, 48–55. doi: 10.1016/j.foodres.2019.04.041
Bernardeau, M., Vernoux, J. P., Henri-Dubernet, S., and Guéguen, M. (2008). Safety assessment of dairy microorganisms: the Lactobacillus genus. Int. J. Food Microbiol. 126, 278–285. doi: 10.1016/j.ijfoodmicro.2007.08.015
Bourrie, B. C. T., Willing, B. P., and Cotter, P. D. (2016). The microbiota and health promoting characteristics of the fermented beverage kefir. Front. Microbiol. 7:647. doi: 10.3389/fmicb.2016.00647
Chen, Y., Liu, W., Xue, J., Yang, J., Chen, X., Shao, Y., et al. (2014). Angiotensin-converting enzyme inhibitory activity of Lactobacillus helveticus strains from traditional fermented dairy foods and antihypertensive effect of fermented milk of strain H9. J. Dairy Sci. 97, 6680–6692. doi: 10.3168/jds.2014-7962
Chiu, S.-H., Chen, C.-C., Wang, L.-T., and Huang, L. (2017). Whole-genome sequencing of Lactobacillus salivarius strains BCRC 14759 and BCRC 12574. Genome Announc. 5, e01336–e01317. doi: 10.1128/genomeA.01336-17
Chuah, L., Foo, H. L., Loh, T. C., Alitheen, N. B. M., Yeap, S. K., Mutalib, N. E. A., et al. (2019). Postbiotic metabolites produced by Lactobacillus plantarum strains exert selective cytotoxicity effects on cancer cells. BMC Compl. Altern. Med. 19:114. doi: 10.1186/s12906-019-2528-2
Chung, Y. C., Jin, H. M., Cui, Y., Kim, D. S., Jung, J. M., Park, J. I., et al. (2014). Fermented milk of Lactobacillus helveticus IDCC3801 improves cognitive functioning during cognitive fatigue tests in healthy older adults. J. Funct. Foods 10, 465–474. doi: 10.1016/j.jff.2014.07.007
Collins, M. D., Rodrigues, U. M., Ash, C., Aguirre, M., Farrow, J. A. E., Martinez-Murcia, A., et al. (1991). Phylogenetic analysis of the genus Lactobacillus and related lactic acid bacteria as determined by reverse transcriptase sequencing of 16S rRNA. FEMS Microbiol. Lett. 77, 5–12. doi: 10.1111/j.1574-6968.1991.tb04313.x
Di, W., Zhang, L., Wang, S., Yi, H., Han, X., and Fan, R. (2017). Physicochemical characterization and antitumour activity of exopolysaccharides produced by Lactobacillus casei SB27 from yak milk. Carbohydr. Polym. 171, 307–315. doi: 10.1016/j.carbpol.2017.03.018
Douillard, F. P., and de Vos, W. M. (2014). Functional genomics of lactic acid bacteria: from food to health. Microb Cell Fact. 13 (Suppl. 1):S8. doi: 10.1186/1475-2859-13-S1-S8
Ejtahed, H., Mohtadi-Nia, J., Homayouni, A., Niafar, M., Asghari Jafarabadi, M., Mofid, V., et al. (2011). Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J. Dairy Sci. 94, 3288–3294. doi: 10.3168/jds.2010-4128
Fondén, R., Leporanta, K., and Svensson, U. (2006). “Nordic/Scandinavian fermented milk products,” in Fermented Milks, ed A. Y. Tamine (Oxford: Blackwell Science/SDT), 156–173. doi: 10.1002/9780470995501.ch7
Foo, H. L., Loh, T. C., Lai, P. W., Lim, Y. Z., Kufli, C. N., and Rusul, G. (2003). Effects of adding Lactobacillus plantarum I-UL4 metabolites in drinking water of rats. Pakistan J. Nutr. 2, 283–288. doi: 10.3923/pjn.2003.283.288
García-Burgos, M., Moreno-Fernández, J., Alférez, M. J. M., Díaz-Castro, J., and López-Aliaga, I. (2020). New perspectives in fermented dairy products and their health relevance. J. Funct. Foods 72:104059. doi: 10.1016/j.jff.2020.104059
Giraffa, G., Chanishvili, N., and Widyastuti, Y. (2010). Importance of lactobacilli in food and feed biotechnology. Res. Microbiol. 161, 480–487. doi: 10.1016/j.resmic.2010.03.001
Gleeson, M., Bishop, N. C., and Struszczak, L. (2016). Effects of Lactobacillus casei shirota ingestion on common cold infection and herpes virus antibodies in endurance athletes: a placebo-controlled, randomized trial. Eur. J. Appl. Physiol. 116, 1555–1563. doi: 10.1007/s00421-016-3415-x
Hafeez, Z., Cakir-Kiefer, C., Roux, E., Perrin, C., Miclo, L., and Dary-Mourot, A. (2014). Strategies of producing bioactive peptides from milk proteins to functionalize fermented milk products. Food Res. Int. 63 , 71–80. doi: 10.1016/j.foodres.2014.06.002
Hammes, W. P., and Vogel, R. F. (1995). “The genus Lactobacillus,” in The Lactic Acid Bacteria, Vol. 2. The Genera of Lactic Acid Bacteria, eds B. J. B. Wood and W. H. Holzapfel Blackie (London: Academic and Professional), 19–54. doi: 10.1007/978-1-4615-5817-0_3
Han, S., Suk, K. T., Kim, D. J., Kim, M., Baik, S., Kim, Y. D., et al. (2015). Effects of probiotics (cultured Lactobacillus subtilis/Streptococcus faecium) in the treatment of alcoholic hepatitis. Eur. J. Gastroenterol. Hepatol. 27, 1300–1306. doi: 10.1097/MEG.0000000000000458
Hummel, A. S., Hertel, C., Holzapfel, W. H., and Franz, C. M. A. P. (2007). Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl. Environ. Microbiol. 73, 730–739. doi: 10.1128/AEM.02105-06
Jauhiainen, T., Rönnback, M., Vapaatalo, H., Wuolle, K., Kautiainen, H., Groop, P.-H., et al. (2010). Long-term intervention with Lactobacillus helveticus fermented milk reduces augmentation index in hypertensive subjects. Eur. J. Clin. Nutr. 64, 424–431. doi: 10.1038/ejcn.2010.3
Jones, M. L., Martoni, C. J., and Prakash, S. (2012). Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. Eur. J. Clin. Nutr. 66, 1234–1241. doi: 10.1038/ejcn.2012.126
Kiessling, G., Schneider, J., and Jahreis, G. (2002). Long-term consumption of fermented dairy products over 6 months increases HDL cholesterol. Eur. J. Clin. Nutr. 56, 843–849. doi: 10.1038/sj.ejcn.1601399
Kim, D.-H., Kim, H., Jeong, D., Kang, I.-B., Chon, J.-W., Kim, H.-S., et al. (2017). Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: targeted and untargeted community analysis with correlation of biomarkers. J. Nutr. Biochem. 44, 35–43. doi: 10.1016/j.jnutbio.2017.02.014
Laiño, J. E., Juarez del Valle, M., Savoy de Giori, G., and LeBlanc, J. G. J. (2013). Development of a high folate concentration yogurt naturally bio-enriched using selected lactic acid bacteria. LWT Food Sci. Technol. 54, 1–5. doi: 10.1016/j.lwt.2013.05.035
Leblanc, A. D. M., and De Perdigo, G. (2010). The application of probiotic fermented milks in cancer and intestinal inflammation proceedings of the nutrition society. Proc. Nutr. Soc. 421–428. doi: 10.1017/S002966511000159X
Lorusso, A., Coda, R., Montemurro, M., and Rizello, C. G. (2018). Use of selected lactic acid bacteria and quinoa flour for manufacturing novel yogurt-like beverages. Foods 7, 1–20. doi: 10.3390/foods7040051
Ma, D., Jiang, Y., Ahmed, S., Qin, W., and Liu, Y. (2020). Antilisterialand physical properties of polysaccharide-collagen films embedded with cell-free supernatant of Lactococcus lactis. Int. J. Biol. Macromol. 145, 1031–1038. doi: 10.1016/j.ijbiomac.2019.09.195
Marshall, E., and Mejia, D. (2011). “Fermentation and sustainable livelihoods,” in Traditional Fermented Food and Beverages for Improved Livelihoods, ed E. Marshall (Rome: FAO), 15–27
McAuliffe, O. (2018). Symposium review: Lactococcus lactis from nondairy sources: their genetic and metabolic diversity and potential applications in cheese. J. Dairy Sci. 101, 3597–3610. doi: 10.3168/jds.2017-13331
McFarland, L. V. (2015). From yaks to yogurt: the history, development, and current use of probiotics. Clin. Infect. Dis. 60, S85–S90. doi: 10.1093/cid/civ054
Medici, M., Vinderola, C. G., and Perdigón, G. (2004). Gut mucosal immunomodulation by probiotic fresh cheese. Int. Dairy J. 14, 611–618. doi: 10.1016/j.idairyj.2003.10.011
Mitelmão, F. C. R., Bergamaschi, C. C., Gerenutti, M., Hächel, K., Silva, M. T., Balc, V. M., et al. (2021). The effect of probiotics on functional constipation in adults: double-blind, randomized, placebo-controlled study. Medicine. 100:e24938. doi: 10.1097/MD.0000000000024938
Miyazaki, K., and Matsuzaki, T. (2008). “Health properties of milk fermented with Lactobacillus casei strain shirota (LcS),” in Handbook of Fermented Functional Foods, ed E. E. Farnworth (Boca Raton, FL: CRC Press Taylor & Francis Group; LLC), 165–208
Mohamadshahi, M., Veissi, M., Haidari, F., Shahbazian, H., Kaydani, G., and Mohammadi, F. (2014). Effects of probiotic yogurt consumption on inflammatory biomarkers in patients with type 2 diabetes. BioImpacts 4, 83–88. doi: 10.5681/bi.2014.007
Moradi, M., Tajik, H., Mardani, K., and Ezati, P. (2019). Efficacy oflyophilized cell-free supernatant of Lactobacillus salivarius (Ls-BU2) on Escherichia coli and shelf life of ground beef. Vet. Res. Forum 10, 193–198. doi: 10.30466/vrf.2019.101419.2417
Motey, G. A., Owusu-Kwarteng, J., Obiri-Danso, K., Ofori, L. A., Ellis, W. O., and Jespersen, L. (2021). In vitro properties of potential probiotic lactic acid bacteria originating from ghanaian indigenous fermented milk products. World J. Microbiol. Biotechnol. 37:52. doi: 10.1007/s11274-021-03013-6
Nasrabadi, M. H., Aboutalebi, H., Ebrahimi, M. T., and Zahedi, F. (2011). The healing effect of Lactobacillus plantarum isolated from Iranian traditional cheese on gastric ulcer in rats. African J. Pharm. Pharmacol. 5, 1446–1451. doi: 10.5897/AJPP11.155
Nishimura, J. (2014). Exopolysaccharides produced from Lactobacillus delbrueckii subsp. bulgaricus. Adv. Microbiol. 4, 1017–1023. doi: 10.4236/aim.2014.414112
Ohsawa, K., Nakamura, F., Uchida, N., Mizuno, S., and Yokogoshi, H. (2018). Lactobacillus helveticus-fermented milk containing lactononadecapeptide (NIPPLTQTPVVVPPFLQPE) improves cognitive function in healthy middle-aged adults: a randomised, double-blind, placebo-controlled trial. Int. J. Food Sci. Nutr. 69, 369–376. doi: 10.1080/09637486.2017.1365824
Parker, M., Zobrist, S., Donahue, C., Edick, C., Mansen, K., Nadjari, H. Z., et al. (2018). Naturally fermented milk from northern Senegal: bacterial community composition and probiotic enrichment with Lactobacillus rhamnosus. Front. Microbiol. 9:2218. doi: 10.3389/fmicb.2018.02218
Patel, S., and Goyal, A. (2011). Functional oligosaccharides: production, properties and applications. World J. Microbiol. Biotechnol. 27, 1119–1128. doi: 10.1007/s11274-010-0558-5
Patel, S., and Goyal, A. (2012). The current trends and future perspectives of prebiotics research: a review. 3 Biotech. 2, 115–125. doi: 10.1007/s13205-012-0044-x
Prakoeswa, C. R. S., Herwanto, N., Prameswari, R., Astari, L., Sawitri, S., Hidayati, A. N., et al. (2017). Lactobacillus plantarum IS-10506 supplementation reduced SCORAD in children with atopic dermatitis. Benef. Microbes 8, 833–840. doi: 10.3920/BM2017.0011
Raygan, F., Rezavandi, Z., Bahmani, F., and Ostadmohammadi, V. (2018). The effects of probiotic supplementation on metabolic status in type 2 diabetic patients with coronary heart disease. Diabetol. Metab. Syndr. 10, 1–7. doi: 10.1186/s13098-018-0353-2
Rosa, D. D., Dias, M. M. S., Grzeskowiak, Ł. M., Reis, S. A., Conceição, L. L., and Peluzio, C. G. (2017). Milk kefir : nutritional, microbiological and health benefits. Nutr. Res. Rev. 30, 82–96. doi: 10.1017/S0954422416000275
Rungsri, P., Akkarachaneeyakorn, N., Wongsuwanlert, M., Piwat, S., Nantarakchaikul, P., and Teanpaisan, R. (2017). Effect of fermented milk containing Lactobacillus rhamnosus SD11 on oral microbiota of healthy volunteers : a randomized clinical trial. J. Dairy Sci. 100, 7780–7787. doi: 10.3168/jds.2017-12961
Salvetti, E., Torriani, S., and Felis, G. E. (2012). The genus Lactobacillus: a taxonomic update. Probiotics Antimicro. 4, 217–226. doi: 10.1007/s12602-012-9117-8
Seta, F., Parazzini, F., Leo, R., Banco, R., Maso, G., de santo, D., et al. (2014). Lactobacillus plantarum P17630 for preventing Candida vaginitis recurrence: a retrospective comparative study. Eur. J. Obstet. Gynecol. Reprod. Biol. 182C, 136–139. doi: 10.1016/j.ejogrb.2014.09.018
Settanni, L., and Moschetti, G. (2010). Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol. 27, 691–697. doi: 10.1016/j.fm.2010.05.023
Sun, Z., Harris, H. M., McCann, A., Guo, C., Argimón, S., Zhang, W., et al. (2015). Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat. Commun. 6:8322. doi: 10.1038/ncomms9322
Tamang, J. P., Shin, D.-H., Jung, S.-J., and Chae, S.-W. (2016). Functional properties of microorganisms in fermented foods. Front. Microbiol. 7:578. doi: 10.3389/fmicb.2016.00578
Tang, W., Dong, M., Wang, W., Han, S., Rui, X., Chen, X., et al. (2017). Structural characterization and antioxidant property of released exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus. Carbohydr. Polym. 173, 654–664. doi: 10.1016/j.carbpol.2017.06.039
Tannock, G. W. (2004). A special fondness for lactobacilli. Appl. Environ. Microbial. 70:3189. doi: 10.1128/AEM.70.6.3189-3194.2004
Taverniti, V., and Guglielmetti, S. (2011). The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: proposal of paraprobiotic concept). Genes Nutr. 6, 261–274. doi: 10.1007/s12263-011-0218-x
Taverniti, V., and Guglielmetti, S. (2012). Health-promoting properties of Lactobacillus helveticus. Front. Microbiol. 3:392. doi: 10.3389/fmicb.2012.00392
Thanh, N. T., Loh, T. C., Foo, H. L., Hair-Bejo, M., and Azhar, K. (2009). Effects of feeding metabolite combinations produced by Lactobacillus plantarum on growth performance, faecal microbial population, small intestine villus height and faecal volatile fatty acids in broilers. Br. Poult. Sci. 50, 298–306. doi: 10.1080/00071660902873947
Thumu, S. C. R., and Halami, P. M. (2020). In vivo safety assessment of Lactobacillus fermentum strains, evaluation of their cholesterol-lowering ability and intestinal microbial modulation. J. Sci. Food Agric. 100, 705–713. doi: 10.1002/jsfa.10071
Tidona, F., Criscione, A., Guastella, A. M., Zuccaro, A., Bordonaro, S., and Marletta, D. (2009). Bioactive peptides in dairy products. Ital. J. Anim. Sci. 8, 315–340. doi: 10.4081/ijas.2009.315
Torino, M. I., Font de Valdez, G., and Mozzi, F. (2015). Biopolymers from lactic acid bacteria. Novel applications in foods and beverages. Front. Microbiol. 6:834. doi: 10.3389/fmicb.2015.00834
Toropov, V., Demyanova, E., Shalaeva, O., Sitkin, S., and Vakhitov, T. (2020). Whole-genome sequencing of Lactobacillus helveticus D75 and D76 confirms safety and probiotic potential. Microorganisms. 8:329. doi: 10.3390/microorganisms8030329
Tuo, Y., Zhang, L., Han, X., Du, M., Zhang, Y., Yi, H., et al. (2011). In vitro assessment of immunomodulating activity of the two Lactobacillus strains isolated from traditional fermented milk. World J. Microbiol. Biotechnol. 27, 505–511. doi: 10.1007/s11274-010-0482-8
Watanabe, K., Fujimoto, J., Sasamoto, M., Dugersuren, J., Tumursuh, T., and Demberel, S. (2008). Diversity of lactic acid bacteria and yeasts in airag and tarag, traditional fermented milk products of Mongolia. World J. Microbiol. Biotechnol. 24, 1313–1325. doi: 10.1007/s11274-007-9604-3
Wilburn, J. R., and Ryan, E. P. (2016). “Fermented foods in health promotion and disease prevention,” in Fermented Foods in Health and Disease Prevention, ed J. Frias, C. Martinez-Villaluenga, E. Peñas (London: Academic Press), 3–19. doi: 10.1016/B978-0-12-802309-9.00001-7
Wittouck, S., Wuyts, S., and Lebeer, S. (2019). Towards a genome-based reclassification of the genus Lactobacillus. Appl. Environ. Microbiol. 85, e02155–e02118. doi: 10.1128/AEM.02155-18
Ye, H., Li, Q., Zhang, Z., Sun, M., Zhao, C., and Zhang, T. (2017). Effect of a novel potential probiotic Lactobacillus paracasei Jlus66 isolated from fermented milk on nonalcoholic fatty liver in rats. Food Funct. 8, 4539–4546. doi: 10.1039/C7FO01108C
Yu, L., Han, X., Cen, S., Duan, H., Feng, S., Xue, Y., et al. (2020). Beneficial effect of GABA-rich fermented milk on insomnia involving regulation of gut microbiota. Microbiol. Res. 233:126409. doi: 10.1016/j.micres.2020.126409
Yu, Z., Zhang, X., Li, S., Li, C., Li, D., and Yang, Z. (2013). Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J. Microbiol. Biotechnol. 29, 489–498. doi: 10.1007/s11274-012-1202-3
Zhang, J., Zhao, X., Jiang, Y., Zhao, W., Guo, T., Cao, Y., et al. (2017). Antioxidant status and gut microbiota change in an aging mouse model as influenced by exopolysaccharide produced by Lactobacillus plantarum YW11 isolated from tibetan kefir. J. Dairy Sci. 100, 6025–6041. doi: 10.3168/jds.2016-12480
Zhang, W., Wang, J., Zhang, D., Liu, H., Wang, S., Wang, Y., et al. (2019). Complete genome sequencing and comparative genome characterization of Lactobacillus johnsonii ZLJ010, a potential probiotic with health- promoting properties. Front. Genet. 10:812. doi: 10.3389/fgene.2019.00812
Zheng, J., Wittouck, S., Salvetti, E., Franz, C. M. A. P., Harris, H. M. B., Mattarelli, P., et al. (2020). 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. 70, 2782–2858. doi: 10.1099/ijsem.0.004107
Keywords: lactobacilli, milk, fermentation, probiotics, post-biotics
Citation: Widyastuti Y, Febrisiantosa A and Tidona F (2021) Health-Promoting Properties of Lactobacilli in Fermented Dairy Products. Front. Microbiol. 12:673890. doi: 10.3389/fmicb.2021.673890
Received: 28 February 2021; Accepted: 21 April 2021;
Published: 21 May 2021.
Edited by:
Dan Cristian Vodnar, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, RomaniaReviewed by:
Evandro L. de Souza, Federal University of Paraíba, BrazilJashbhai B. Prajapati, Anand Agricultural University, India
Copyright © 2021 Widyastuti, Febrisiantosa and Tidona. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Yantyati Widyastuti, yantyati.widyastuti@lipi.go.id