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Traditional fermented beverages from Mexico as a potential probiotic source

Traditional fermented beverages from Mexico as a potential probiotic source Ann Microbiol (2017) 67:577–586 DOI 10.1007/s13213-017-1290-2 REVIEW ARTICLE Traditional fermented beverages from Mexico as a potential probiotic source 1 1 1 Haydee Eliza Romero-Luna & Humberto Hernández-Sánchez & Gloria Dávila-Ortiz Received: 18 March 2017 /Accepted: 13 July 2017 /Published online: 3 August 2017 Springer-Verlag GmbH Germany and the University of Milan 2017 Abstract Fermentation is one of the oldest ways of process- Introduction ing food. Some fermented food is produced industrially, but can also be produced in an artisanal way by certain ethnic Fermentation is one of the oldest processes for processing and groups, called traditional fermented foods. In Mexico, there preserving food. The use of microorganisms to prepare food are a variety of traditional fermented beverages which are has been known worldwide for thousands of years. The produced in an artisanal way. They include those made with fermented microorganisms can proceed from the natural mi- maize (atole agrio, pozol,and tesgüino), fruit (tepache and crobiota or a starter (Sangwan et al. 2014). During this process, colonche), and obtained by plant fermentation (pulque, tuba, the metabolic activities of microorganisms improve the safety, and taberna). These beverages have been used since ancient nutritional, and sensory properties of different raw materials, times for religious and medicinal purposes. The medicinal such as dairy products, meat, vegetables, tubers, and cereals, so effect may be due to fermented microorganisms. The presence these microorganisms have significant contributions in the hu- of beneficial microorganisms known as probiotics provides mandiet(Sannietal. 2013; Chilton et al. 2015). These foods beneficial effects to consumer health, improving the balance are appreciated for their attributes of flavor, aroma, and pleas- of intestinal host, and reducing the risk of gastrointestinal ant texture, and improved cooking and processing properties diseases, mainly. Most probiotics belong to the genus (Holzapfel 2002). Lactobacillus, but Bifidobacterium, Bacillus, and yeast are Fermented foods are accessible to many people, such as also found. Therefore, it is important that the microbiological those produced industrially (wine, cheese, beer, bread, and diversity of the beverages is studied and documented. This yogurt). However, the so-called Btraditional fermented foods^ review includes information on the microbial diversity and are produced in an artisanal or semi-commercial way by cer- probiotic potential of the most important traditional fermented tain social or ethnic groups (Olivares-Illana et al. 2002), prov- beverages from Mexico. ing to be part of the gastronomic culture of certain social groups. Several authors point to these foods as an example of Bbiological ennoblement^ due to bioenrichment with essen- . . Keywords Traditional fermented beverages Probiotics tial nutrients during fermentation (Platt 1964). In addition to Yeast Bacteria being a source of beneficial microorganisms which have an important role in food preservation, palatability, and nutrient bioavailability (Champagne et al. 2005), fermented food is also a source of probiotics which have been defined by experts * Gloria Dávila-Ortiz from the Food and Agriculture Organization of the United gdavilao@yahoo.com Nations (FAO)/World Health Organization (WHO) in 2001 as Blive microorganisms which when administered in ade- Departamento de Ingeniería Bioquímica, Escuela Nacional de quate amounts confer a health benefit on the host^. Ciencias Biológicas Del Instituto Politécnico Nacional, Unidad Around the world, there are about 3500 traditional Profesional Adolfo López Mateos, Av. Wilfrido Massieu Esq. Cda. fermented foods from cereals, legumes, tubers, and fruits, Miguel Stampa s/n, 07738 Delegación Gustavo A. Madero, Ciudad de México, Mexico where a consortium of bacteria, yeast, and molds are involved, 578 Ann Microbiol (2017) 67:577–586 which may have beneficial effects on consumer health B. pumilus,and B. subtilis have been considered as species (Escalante et al. 2008; Schoustra et al. 2013; de Vuyst et al. with probiotic effects; however, the fact that they are spore- 2014), improving the balance of intestinal host and reducing producing organisms generates conflicting opinions (Zhu the risk of gastrointestinal diseases (Chiang and Pan 2012). et al. 2016). They also relieve lactose intolerance, improve bioavailability On the other hand, yeast can also be used as probiotics; of nutrients, and prevent or reduce the prevalence of allergies. however, despite their wide distribution and importance in Antimutagenic, hypocholesterolemic, antihypertensive, and the production of foods and beverages worldwide, their pro- immunomodulatory effects have also been reported in biotic potential is ignored (Chen et al. 2010). Saccharomyces probiotics (Chiang and Pan 2012). They relieve symptoms of cerevisiae var. boulardii is the only recognized and character- inflammatory bowel disease, irritable bowel syndrome, colitis, ized probiotic yeast (Hatoum et al. 2012), although other spe- and reduce the risk of colon, liver, and breast cancers (Prado cies of the genus Saccharomyces (S.) have probiotic proper- et al. 2008). Several studies have indicated the presence of ties, as well as the genera Pichia, Metschnikowia, Yarrowia, microorganisms that, although not classified as probiotics Candida, Debaryomyces,and Kluyveromyces, which have due to the lack of sufficient evidence, have certain probiotic been reported in fermented foods and beverages (Tamang characteristics (Table 1). and Fleet 2009;Chen etal. 2010;Lv etal. 2013). Consequently, the probiotic consumption, from fermented food and beverages, exert a beneficial effect. So, the aim of this review is to ascertain the information available in the Traditional fermented beverages from Mexico studies about microbial diversity involving potentially probi- otic microorganisms in the fermentation of traditional In Mexico, there are about 200 fermented foods and bever- Mexican beverages. All this with the aim of studying new ages, but only a few have been studied (Herrera 2003). sources of probiotics and rescue a part of culture, like tradi- A wide variety of beverages with historical importance, tional food, that has been lost with the industrialization of such as pulque, and beverages with cultural importance, such food. as pozol and tesgüino, among others, are produced in Mexico (Escalante et al. 2004; Hui and Özgül Evranuz 2012). These Microorganisms with probiotic potential in fermented traditional fermented beverages have been consumed for years foods and beverages and are strongly related to Mexican culture and traditions. Traditional fermented beverages have had a great impor- Most probiotics belong to the lactic acid bacteria (LAB) group tance in the daily lives of Mexican indigenous communities. and to the genus Lactobacillus (Lb.), but not exclusively Since pre-Hispanic times, Mesoamerican civilizations (Prado et al. 2008). Lactobacillus has been isolated in fermented a variety of plants, cereals, native fruits, and other fermented foods and beverages from around the world, but raw material for beverage production, and the consumption of also the genera Lactococcus (Lc.), Leuconostoc (L.), these played an important role in religion, ritual, divinity, and Streptococcus,and Enterococcus have species considered as healing for millennia (Bruman 2000). probiotic (Hill et al. 2014; Holzapfel and Wood 2014). The LAB group is characterized by the production of organic acids Cereals during fermentation, mainly lactic acid, which lowers the pH of the substrate, inhibiting the growth of other microorgan- There is a wide variety of traditional fermented non-dairy isms, including pathogens (Holzapfel et al. 1995). beverages produced around the world. Many of them are Bifidobacterium is also present in some fermented foods non-alcoholic beverages made from cereals as raw material. (Tamang 2010). For years, it has been included in the LAB Cereals have been a part of the staple diet in Mexico for group; however, it belongs to an entirely different phylum centuries, mainly maize (Elizaquível et al. 2015), playing an (Actinobacteria). Bifidobacterium is usually found in the gas- important role in the nutrition of marginalized population trointestinal tract, and its presence is related to reducing the (Jideani and Jideani 2011). incidence of enteric infections and, generally, intestinal health, Cereal fermentation is carried out mainly by species of so it is added to foods, mainly in milk, for their probiotic LAB and yeasts (Corsetti and Settanni 2007). The genera functions (Hutkins 2006). Enterococcus, Lactococcus, Lactobacillus, Leuconostoc, Species of the genus Bacillus (B.) are abundant in foods, Pediococcus, Streptococcus,and Weissella are commonly as- mainly in alkaline fermentations (Tamang 2015). Species that sociated with fermentation. These genera include some probi- have been isolated from vegetable fermentations are B. cereus, otic species (Table 2;Guyot 2010;Moroni et al. 2011). B. amyloliquefaciens, B. circulans, B. coagulans, B. firmus, Although the population of LAB is dominated by the genus B. licheniformis, B. megaterium, B. pumilus, B. subtilis,and Lactobacillus (de Vuyst and Neysens 2005), Leuconostoc has B. thuringiensis (Kubo et al. 2011). Bacillus cereus, been reported as being prevalent in the fermentation of pozol Ann Microbiol (2017) 67:577–586 579 Table 1 Examples of potential probiotic microorganisms in fermented foods from around the world Product Country Substrate Microorganism Potential probiotic characteristics References Kefir grains Brazil Milk L. mesenteroides Antagonistic activity against pathogens Leite et al. (2015) Antibiotic resistance No hemolytic activity Lc. lactis sp. cremoris Antagonistic activity against pathogens Leite et al. (2015) Lc. lactis sp. lactis Antioxidant activity Antibiotic resistance No hemolytic activity Lb. paracasei Antagonistic activity against pathogens Leite et al. (2015) Antioxidant activity Bacteriocin No hemolytic activity Adherence to Caco-2 Antibiotic resistance Red wine Spain Must Pediococcus pentosaceus Survival in GI conditions García-Ruíz et al. (2014) Lb. plantarum Adherence to Caco-2 Reduces E. coli adhesion Lb. casei Survival in GI conditions García-Ruíz et al. (2014) Oenococcus oeni Idli India Rice and Phaseolus mungo Candida tropicalis Survival in GI conditions Syal and Vohra (2013) Saccharomyces cerevisiae Antibiotic resistance Autoaggregation Antimicrobial activity against Salmonella, Staphylococcus aureus,and Pseudomonas sp. Enzymes production B12 vitamin production Cholesterol assimilation Jalebi India Maida (refined wheat flour) Aureobasidium spp. Survival in GI conditions Syal and Vohra (2013) Pichia manshurica Antibiotic resistance Autoaggregation Antimicrobial activity against Salmonella, Staphylococcus aureus,and Pseudomonas sp. Enzymes production Cholesterol assimilation Ricotta cheese Tunisia Milk Lb. plantarum Antimicrobial activity against Listeria Ben Slama et al. (2013) monocytogenes Fermented olives Greece Olives Lb. pentosus, Lb. plantarum, Survival in GI conditions Argyrietal.(2013) Lb. paracasei subs. paracasei No hemolytic activity Adherence to Caco-2 Fermented bambangan Malaysia Bambangan fruit Lb. plantarum Survival in GI conditions Ng et al. (2015) (Mangifera pajang) Lb. brevis High percentage of hydrophobicity and autoaggregation Enzymatic activity Antimicrobial activity against Listeria monocytogenes 580 Ann Microbiol (2017) 67:577–586 Table 1 (continued) Product Country Substrate Microorganism Potential probiotic characteristics References Turchi et al. (2013) Raw milk sheep cheese Italy Milk Lb. plantarum Susceptible to antibiotics Salami Meat Survival in GI conditions Agglutinability Alheira, Chouriça de Vinhais,and Portugal Meat Enterococcus faecium Antimicrobial activity against Listeria Barbosa et al. (2014) Salpicão de Vinhais (sausages) monocytogenes, Listeria innocua,and Staphylococcus aureus Survival in GI conditions Traditional fermented soybean paste China Soybean Lb. plantarum Survival in GI conditions Li et al. (2015) Antimicrobial activity against Escherichia coli, Staphylococcus aureus, Salmonella sp., and Shigella sp. Adherence to Caco-2 Inhibits adhesion of pathogens to Caco-2 Table 2 Microorganisms isolated from some Mexican traditional fermented cereal beverages Product Substrate Sensory properties Fermentation time Microorganisms State References Atole agrio Nixtamalized maize Acid taste Until 3 days Lb. acidophilus and Lb. plantarum, Chiapas Sánchez-Dirzo et al. (2010) Saccharomyces cerevisiae Pozol Nixtamalized maize Acid taste, refreshing, Until 4 days Streptococcus, Streptococcus suis, Campeche, Chiapas, Oaxaca, Ulloa and Herrera (1972); non-alcoholic S. bovis, Enterococcus, Exiguobacterium, Quintana Roo, Tabasco, Wacher-Rodarte et al. (1993); Lc. lactis, Lc. raffinolactis, L. mesenteroides, and Yucatán Nuraida et al. (1995); Lb. confusus, Lb. fermentum, Lb. plantarum, ben Omar and Ampe (2000); Lb. casei, Lb. delbrueckii, Lb. alimentarium, Wacher-Rodarte et al. (2000); Bifidobacterium Escalante et al. (2001); Díaz-Ruíz et al. (2003) Tesgüino Germinated maize Acid taste, refreshing Until 3 days Candida guilliermondii, Hansenula anomala, Chihuahua, Durango, Jalisco, Ulloa et al. (1987); S. kluyveri, Saccharomyces cerevisiae Nayarit, Oaxaca, Sinaloa, Lappe and Ulloa (1989); and Sonora Wacher-Rodarte (1995) Ann Microbiol (2017) 67:577–586 581 (Nuraida et al. 1995). Streptococcus and Enterococcus have also been found in traditional cereal-based fermented bever- ages in Mexico, such as pozol (ben Omar and Ampe 2000; Escalante et al. 2001). In this regard, strains of Streptococcus genera, L. pseudomesenteroides and Weissella paramesenteroides isolated from pozol, present probiotic po- tential, since the microorganisms are able to survive under low pH and bile salts conditions and to adhere to HEp2 cells (Rodríguez et al. 2011). Agrobacterium azotophilium is a bacterium, reported in pozol, that have the ability to produce an antimicrobial com- pound with a broad spectrum (Ray et al. 2000). Saccharomyces cerevisiae has been present in the fermen- tation of traditional fermented beverages of Mexico, which is widely recognized as safe for use in food for human consump- tion and can present probiotic potential. Other yeasts like S. kluyveri, Candida guilliermondii,and Hansenula anomala are also found in traditional fermented beverages of Mexico, and although there have been no studies on their probiotic potential, are good options to consider (Ulloa et al. 1987; Wacher-Rodarte 1995). Meanwhile, Pichia kudriavzevii and Clavispora lusitaniae have been isolated from atole agrio, showing probiotic characteristics (growth capacity at 37 °C, low pH, and in the presence of bile salts survival, and biofilm formation) (Manrique-Donrronsoro et al. 2016). Fruits There are a great variety of fermented drinks made with fruits from Africa, Asia, and Latin America. Grape wine is probably the most important fermented drink, economically speaking, although there are also beverages made with fruits such as dates in North Africa, jackfruit in Asia, and pineapple in Latin America (Battcock 1998). The spontaneous fermentation of these beverages is mainly basedonLAB (Lactobacillus, Leuconostoc, Pediococcus, etc.) and yeast (Saccharomyces, Hansenula, Candida, etc.) found on the fruit surface (Table 3; Di Cagno et al. 2013) and in utensils used during processing (Fleet 2003). Tepache is a traditional Mexican fermented beverage from the pineapple shell. It is a product that can prevent contami- nation caused by canning industries, since the making of pre- serves like pineapple in syrup generates a great amount of waste, which can be transformed into a beverage for human consumption, with nutrients and vitamins obtained from fermenting microorganisms. The presence of several species of Lactobacillus,such as Lb. plantarum, has been reported (Alvarado et al. 2006). In this beverage, bacteriocin- producing bacteria (Lc. lactis, E. faecium) have also been reported, pointing to the beverage as a natural source of po- tential antimicrobials (de la Fuente-Salcido et al. 2015). Leuconostoc mesenteroides is also present in tepache,andis able to produce a bacteriocin named mesentericin, besides Table 3 Microorganisms isolated from some traditional fermented Mexican beverages made from fruit Product Substrate Sensory properties Fermentation time Microorganisms State References Tepache Pineapple Refreshing, low alcohol Up to 3 days Lb. plantarum, L. mesenteroides, Lactobacillus sp., Nava-Garduño (1953); content, sour taste Lc. lactis, Hanseniaspora, Torulopsis inconspicua, Herreraand Ulloa(1982); Saccharomyces cerevisiae, Pichia membranaefaciens, Moreno-Terrazas (2005); Candida queretana Alvarado et al. (2006); de la Fuente-Salcido et al. (2015) Colonche Red prickly Sweet and pleasant taste Up to 3 days Candida valida, Saccharomyces cerevisiae, Chihuahua, Sonora, Diguet (1928); Torulopsis taboadae, Pichia fermentans Zacatecas Ulloa and Herrera (1978); Herrera and Ulloa (1981a); Ulloa et al. (1987); Rodríguez-Lerma et al. (2011) 582 Ann Microbiol (2017) 67:577–586 producing dextran, an extracellular polymer that has a wide Plants industrial use as coadjuvant, emulsifier, carrier, and stabilizer, and which may serve as a prebiotic for other beneficial micro- In Mexico, fermented beverages made from other sources organisms (Moreno-Terrazas 2005;Sarwatet al. 2008). such as agave, coconut palm, or coyol palm are also con- The only yeast recognized as probiotic (Saccharomyces sumed, and will be discussed below (Table 4). cerevisiae var. boulardii) was isolated from fruits of Pulque is one of the oldest beverages in Mexico and is Indochina called lychees (Czerucka et al. 2007), and obtained from the fermentation of the agave sap called agua fermented fruit beverages as well as fruits are a source of miel. Microorganisms that are part of this fermentation are probiotic microorganisms. As for the traditional fermented homo- and heterofermentative LAB (Lb. acidophilus, Lb. beverages of Mexico, S. cerevisiae is present in most of them hilgardii, Lb. plantarum, Lb. acetolerans, Lb. kefir, Lc. lactis (Corona-González et al. 2013). In addition, Hanseniaspora, sp. lactis, L. citreum, L. kimchii, L. mesenteroides, Torulopsis inconspicua , T. taboadae , Pichia L. pseudomesenteroides), an alcohol-producing bacteria membranaefaciens, P. fermentans,and Candida species, such (Zymomonas mobilis), γ-proteobacteria, Acetobacter as C. valida, are also common (Nava-Garduño 1953; malorum, A. pomorium, Microbacterium arborescens, Alvarado et al. 2006; Rodríguez-Lerma et al. 2011;de la Flavobacterium johnsoniae, Gluconobacter oxydans,and Fuente-Salcido et al. 2015). Candida queretana, identified Hafnia alvei (Sánchez-Marroquín 1967;Sánchez-Marroquín as a new species, was isolated from P. fermentans in the central et al. 1967;UlloaandHerrera 1976; Chellapandian et al. Mexican state of Querétaro (Herrera and Ulloa 1982). The 1988; Escalante et al. 2004, 2008), besides yeasts, mainly of search for new potentially probiotic yeasts is very important, the genus Saccharomyces (S. bayanus, S. cerevisiae, since many of the traditional fermented beverages in Mexico S. paradoxus) and others like Candida spp., C. parapsilosis, are obtained using yeasts as the starter microorganism Clavispora lusitaniae, Hanseniaspora uvarum, K. lactis, (Herrera and Ulloa 1982). K. marxianus, Pichia membranaefaciens, Pichia spp., and Torulaspora delbrueckii (Cervantes-Contreras and Pedroza- Tibicos as starters Rodríguez 2007; Lappe-Oliveras et al. 2008), that have been found in raw material such as agua miel; in this case, Traditional fermented fruit beverages from Mexico are some- L. mesenteroides with probiotic potential has been reported times inoculated with starters called tibicos, which play an in agua miel,aswellasin pulque fermentation (Castro- important role in the fermentation of tepache and colonche. Rodríguez et al. 2015; Giles-Gómez et al. 2016). Tibicos are macrocolonies, formed by symbiotic associa- Lactobacillus casei J57 (GenBank accession no. JN182264) tions of bacteria and yeasts, consisting of compact, whitish or was also reported in pulque, showing bile salt hydrolase ac- yellowish, translucent or opalescent, gelatinous masses tivity, a characteristic associated with the probiotic potential of crossed by fine veins or irregular shape and size. They are bacteria, due to an association with serum cholesterol- developed in sugary liquids kept at rest, and in fruits and its lowering effects (González-Vázquez et al. 2015; Patel et al. juices, such as pineapple (Herrera and Ulloa 1981b). 2010). In this beverage, Lb. sanfranciscensis was also found. Tibicos are very similar to water kefir grains, in relation to This bacteria showed anti-inflammatory properties in an their structure (Magalhães et al. 2010). Fermented beverages in vivo model in mice (Torres-Maravilla et al. 2016). with kefir grains, both milk and water, have been shown to On the other hand, the yeast Kluyveromyces marxianus improve health. Furthermore, potentially probiotic cultures isolated from pulque presented probiotic characteristics such have been isolated from these (Zanirati et al. 2015), indicating as antagonistic activity against Klebsiella pneumoniae,as well that tibicos may present microorganisms with probiotic as adhesion to gut mice, mainly (Mendoza-Gardeazábal potential. 2013). Yeasts such as Brettanomyces claussenii, Candida On the other hand, the fermented beverage from palm juice guilliermondii, C. valida, Cryptococcus albidus var. bidus, is known worldwide as Bpalm wine^, taking different names Rhodotorula rubra, and S. cerevisiae, and bacteria such as according to the region and the type of palm from which it is B. brevis, B. polymyxa, B. circulans, B. coagulans, made, for example, toddy or tari in India, mu, bandji, B. firmus, B. macerans,and B. pumilus (Rubio et al. 1993) ogogoro, nsafufuo, nsamba, mnazi, yongo, tua,or tubak in have been isolated from tibicos used for the fermentation of West Africa and South America (Ouoba et al. 2012). fruit beverages, although this microbial composition could In Mexico, palm wines are called taberna, which is obtain- vary at the species level, depending on each local product ed from the palm of coyol, and tuba, obtained from the coco- (Herrera and Ulloa 1981b). nut palm. These are artisanal beverages. For this reason, there Since tibicos are very popular and important in the prepa- is little information on the microbial diversity of palm wines ration of traditional fermented beverages, it would be neces- made in Mexico. However, it was noted the presence of Lc. sary to study the potential probiotic of such strains. lactis and E. faecium, bacteria with antimicrobial activity due Ann Microbiol (2017) 67:577–586 583 Table 4 Microorganisms isolated from some traditional fermented Mexican plants Product Substrate Sensory properties Fermentation time Microorganisms State References Pulque Agave Alcoholic beverage, white, Until 1 day Lb acidophilus, Lb. hilgardii, Lb. plantarum, Center of Mexico Sánchez-Marroquín (1967); viscose, and strong smell Lb. acetolerans, Lb. kefir, Lc. lactis sp., Sánchez-Marroquín et al. (1967); L. citreum, L. kimchii, L. mesenteroides, Ulloaand Herrera(1976); L. pseudomesenteroides, Zymomonas mobilis, Chellapandian et al. (1988); Acetobacter malorum, A. pomorium, Escalante et al. (2004, 2008); Microbacterium arborescens, Flavobacterium Cervantes-Contreras and Pedroza- johnsoniae, Gluconobacter oxydans, Hafnia alvei, Rodríguez (2007); Lappe-Oliveras S. bayanus, S. cerevisiae, S. paradoxus, Candida spp., et al. (2008) C. parapsilosis, Clavispora lusitaniae, Hanseniaspora uvarum, K. lactis, K. marxianus, Pichia membranaefaciens, Pichia spp., Torulaspora delbrueckii Taberna Coyol palm whitish, effervescent, sweet 1 day Fructobacillus durionis, F. fructosus, South of Mexico Balick (1990); Acetobacter pasteurianus, Lb. nagelii, Alcántara-Hernández et al. (2010); Lb. sucicola, Zymomonas mobilis, Santiago-Urbina et al. (2015) Saccharomyces cerevisiae, Hanseniaspora guilliermondii, Candida tropicalis, C. intermedia, Kazachstania unispora, Kazachstania exigua, Meyerozyma guilliermondii, Pichia kudriavzevii (Issatchenkia orientalis), and Pichia kluyveri Tuba Coconut palm Alcoholic Not reported Saccharomyces cerevisiae, L. lactis,and E. faecium Colima, Michoacán, Stringini et al. (2009); beverages, sweet and Guerrero Velázquez-Monreal et al. (2011); Chandrasekhar et al. (2012); Santiago-Urbina et al. (2013); de la Fuente-Salcido et al. (2015) 584 Ann Microbiol (2017) 67:577–586 Ben Slama R, Kouidhi B, Zmantar T, Chaieb K, Bakhrouf A (2013) Anti- to bacteriocin production, in tuba (de la Fuente-Salcido et al. listerial and anti-biofilm activities of potential Probiotic 2015). This is in addition to other investigations where the Lactobacillus strains isolated from Tunisian traditional fermented presence of Lb. pentosus, Lb. plantarum,and L. brevis with food. 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Front Microbiol 7: 296. doi:10.1007/s13213-014-0861-8 718. doi:10.3389/fmicb.2016.00718 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Microbiology Springer Journals

Traditional fermented beverages from Mexico as a potential probiotic source

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Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
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Ann Microbiol (2017) 67:577–586 DOI 10.1007/s13213-017-1290-2 REVIEW ARTICLE Traditional fermented beverages from Mexico as a potential probiotic source 1 1 1 Haydee Eliza Romero-Luna & Humberto Hernández-Sánchez & Gloria Dávila-Ortiz Received: 18 March 2017 /Accepted: 13 July 2017 /Published online: 3 August 2017 Springer-Verlag GmbH Germany and the University of Milan 2017 Abstract Fermentation is one of the oldest ways of process- Introduction ing food. Some fermented food is produced industrially, but can also be produced in an artisanal way by certain ethnic Fermentation is one of the oldest processes for processing and groups, called traditional fermented foods. In Mexico, there preserving food. The use of microorganisms to prepare food are a variety of traditional fermented beverages which are has been known worldwide for thousands of years. The produced in an artisanal way. They include those made with fermented microorganisms can proceed from the natural mi- maize (atole agrio, pozol,and tesgüino), fruit (tepache and crobiota or a starter (Sangwan et al. 2014). During this process, colonche), and obtained by plant fermentation (pulque, tuba, the metabolic activities of microorganisms improve the safety, and taberna). These beverages have been used since ancient nutritional, and sensory properties of different raw materials, times for religious and medicinal purposes. The medicinal such as dairy products, meat, vegetables, tubers, and cereals, so effect may be due to fermented microorganisms. The presence these microorganisms have significant contributions in the hu- of beneficial microorganisms known as probiotics provides mandiet(Sannietal. 2013; Chilton et al. 2015). These foods beneficial effects to consumer health, improving the balance are appreciated for their attributes of flavor, aroma, and pleas- of intestinal host, and reducing the risk of gastrointestinal ant texture, and improved cooking and processing properties diseases, mainly. Most probiotics belong to the genus (Holzapfel 2002). Lactobacillus, but Bifidobacterium, Bacillus, and yeast are Fermented foods are accessible to many people, such as also found. Therefore, it is important that the microbiological those produced industrially (wine, cheese, beer, bread, and diversity of the beverages is studied and documented. This yogurt). However, the so-called Btraditional fermented foods^ review includes information on the microbial diversity and are produced in an artisanal or semi-commercial way by cer- probiotic potential of the most important traditional fermented tain social or ethnic groups (Olivares-Illana et al. 2002), prov- beverages from Mexico. ing to be part of the gastronomic culture of certain social groups. Several authors point to these foods as an example of Bbiological ennoblement^ due to bioenrichment with essen- . . Keywords Traditional fermented beverages Probiotics tial nutrients during fermentation (Platt 1964). In addition to Yeast Bacteria being a source of beneficial microorganisms which have an important role in food preservation, palatability, and nutrient bioavailability (Champagne et al. 2005), fermented food is also a source of probiotics which have been defined by experts * Gloria Dávila-Ortiz from the Food and Agriculture Organization of the United gdavilao@yahoo.com Nations (FAO)/World Health Organization (WHO) in 2001 as Blive microorganisms which when administered in ade- Departamento de Ingeniería Bioquímica, Escuela Nacional de quate amounts confer a health benefit on the host^. Ciencias Biológicas Del Instituto Politécnico Nacional, Unidad Around the world, there are about 3500 traditional Profesional Adolfo López Mateos, Av. Wilfrido Massieu Esq. Cda. fermented foods from cereals, legumes, tubers, and fruits, Miguel Stampa s/n, 07738 Delegación Gustavo A. Madero, Ciudad de México, Mexico where a consortium of bacteria, yeast, and molds are involved, 578 Ann Microbiol (2017) 67:577–586 which may have beneficial effects on consumer health B. pumilus,and B. subtilis have been considered as species (Escalante et al. 2008; Schoustra et al. 2013; de Vuyst et al. with probiotic effects; however, the fact that they are spore- 2014), improving the balance of intestinal host and reducing producing organisms generates conflicting opinions (Zhu the risk of gastrointestinal diseases (Chiang and Pan 2012). et al. 2016). They also relieve lactose intolerance, improve bioavailability On the other hand, yeast can also be used as probiotics; of nutrients, and prevent or reduce the prevalence of allergies. however, despite their wide distribution and importance in Antimutagenic, hypocholesterolemic, antihypertensive, and the production of foods and beverages worldwide, their pro- immunomodulatory effects have also been reported in biotic potential is ignored (Chen et al. 2010). Saccharomyces probiotics (Chiang and Pan 2012). They relieve symptoms of cerevisiae var. boulardii is the only recognized and character- inflammatory bowel disease, irritable bowel syndrome, colitis, ized probiotic yeast (Hatoum et al. 2012), although other spe- and reduce the risk of colon, liver, and breast cancers (Prado cies of the genus Saccharomyces (S.) have probiotic proper- et al. 2008). Several studies have indicated the presence of ties, as well as the genera Pichia, Metschnikowia, Yarrowia, microorganisms that, although not classified as probiotics Candida, Debaryomyces,and Kluyveromyces, which have due to the lack of sufficient evidence, have certain probiotic been reported in fermented foods and beverages (Tamang characteristics (Table 1). and Fleet 2009;Chen etal. 2010;Lv etal. 2013). Consequently, the probiotic consumption, from fermented food and beverages, exert a beneficial effect. So, the aim of this review is to ascertain the information available in the Traditional fermented beverages from Mexico studies about microbial diversity involving potentially probi- otic microorganisms in the fermentation of traditional In Mexico, there are about 200 fermented foods and bever- Mexican beverages. All this with the aim of studying new ages, but only a few have been studied (Herrera 2003). sources of probiotics and rescue a part of culture, like tradi- A wide variety of beverages with historical importance, tional food, that has been lost with the industrialization of such as pulque, and beverages with cultural importance, such food. as pozol and tesgüino, among others, are produced in Mexico (Escalante et al. 2004; Hui and Özgül Evranuz 2012). These Microorganisms with probiotic potential in fermented traditional fermented beverages have been consumed for years foods and beverages and are strongly related to Mexican culture and traditions. Traditional fermented beverages have had a great impor- Most probiotics belong to the lactic acid bacteria (LAB) group tance in the daily lives of Mexican indigenous communities. and to the genus Lactobacillus (Lb.), but not exclusively Since pre-Hispanic times, Mesoamerican civilizations (Prado et al. 2008). Lactobacillus has been isolated in fermented a variety of plants, cereals, native fruits, and other fermented foods and beverages from around the world, but raw material for beverage production, and the consumption of also the genera Lactococcus (Lc.), Leuconostoc (L.), these played an important role in religion, ritual, divinity, and Streptococcus,and Enterococcus have species considered as healing for millennia (Bruman 2000). probiotic (Hill et al. 2014; Holzapfel and Wood 2014). The LAB group is characterized by the production of organic acids Cereals during fermentation, mainly lactic acid, which lowers the pH of the substrate, inhibiting the growth of other microorgan- There is a wide variety of traditional fermented non-dairy isms, including pathogens (Holzapfel et al. 1995). beverages produced around the world. Many of them are Bifidobacterium is also present in some fermented foods non-alcoholic beverages made from cereals as raw material. (Tamang 2010). For years, it has been included in the LAB Cereals have been a part of the staple diet in Mexico for group; however, it belongs to an entirely different phylum centuries, mainly maize (Elizaquível et al. 2015), playing an (Actinobacteria). Bifidobacterium is usually found in the gas- important role in the nutrition of marginalized population trointestinal tract, and its presence is related to reducing the (Jideani and Jideani 2011). incidence of enteric infections and, generally, intestinal health, Cereal fermentation is carried out mainly by species of so it is added to foods, mainly in milk, for their probiotic LAB and yeasts (Corsetti and Settanni 2007). The genera functions (Hutkins 2006). Enterococcus, Lactococcus, Lactobacillus, Leuconostoc, Species of the genus Bacillus (B.) are abundant in foods, Pediococcus, Streptococcus,and Weissella are commonly as- mainly in alkaline fermentations (Tamang 2015). Species that sociated with fermentation. These genera include some probi- have been isolated from vegetable fermentations are B. cereus, otic species (Table 2;Guyot 2010;Moroni et al. 2011). B. amyloliquefaciens, B. circulans, B. coagulans, B. firmus, Although the population of LAB is dominated by the genus B. licheniformis, B. megaterium, B. pumilus, B. subtilis,and Lactobacillus (de Vuyst and Neysens 2005), Leuconostoc has B. thuringiensis (Kubo et al. 2011). Bacillus cereus, been reported as being prevalent in the fermentation of pozol Ann Microbiol (2017) 67:577–586 579 Table 1 Examples of potential probiotic microorganisms in fermented foods from around the world Product Country Substrate Microorganism Potential probiotic characteristics References Kefir grains Brazil Milk L. mesenteroides Antagonistic activity against pathogens Leite et al. (2015) Antibiotic resistance No hemolytic activity Lc. lactis sp. cremoris Antagonistic activity against pathogens Leite et al. (2015) Lc. lactis sp. lactis Antioxidant activity Antibiotic resistance No hemolytic activity Lb. paracasei Antagonistic activity against pathogens Leite et al. (2015) Antioxidant activity Bacteriocin No hemolytic activity Adherence to Caco-2 Antibiotic resistance Red wine Spain Must Pediococcus pentosaceus Survival in GI conditions García-Ruíz et al. (2014) Lb. plantarum Adherence to Caco-2 Reduces E. coli adhesion Lb. casei Survival in GI conditions García-Ruíz et al. (2014) Oenococcus oeni Idli India Rice and Phaseolus mungo Candida tropicalis Survival in GI conditions Syal and Vohra (2013) Saccharomyces cerevisiae Antibiotic resistance Autoaggregation Antimicrobial activity against Salmonella, Staphylococcus aureus,and Pseudomonas sp. Enzymes production B12 vitamin production Cholesterol assimilation Jalebi India Maida (refined wheat flour) Aureobasidium spp. Survival in GI conditions Syal and Vohra (2013) Pichia manshurica Antibiotic resistance Autoaggregation Antimicrobial activity against Salmonella, Staphylococcus aureus,and Pseudomonas sp. Enzymes production Cholesterol assimilation Ricotta cheese Tunisia Milk Lb. plantarum Antimicrobial activity against Listeria Ben Slama et al. (2013) monocytogenes Fermented olives Greece Olives Lb. pentosus, Lb. plantarum, Survival in GI conditions Argyrietal.(2013) Lb. paracasei subs. paracasei No hemolytic activity Adherence to Caco-2 Fermented bambangan Malaysia Bambangan fruit Lb. plantarum Survival in GI conditions Ng et al. (2015) (Mangifera pajang) Lb. brevis High percentage of hydrophobicity and autoaggregation Enzymatic activity Antimicrobial activity against Listeria monocytogenes 580 Ann Microbiol (2017) 67:577–586 Table 1 (continued) Product Country Substrate Microorganism Potential probiotic characteristics References Turchi et al. (2013) Raw milk sheep cheese Italy Milk Lb. plantarum Susceptible to antibiotics Salami Meat Survival in GI conditions Agglutinability Alheira, Chouriça de Vinhais,and Portugal Meat Enterococcus faecium Antimicrobial activity against Listeria Barbosa et al. (2014) Salpicão de Vinhais (sausages) monocytogenes, Listeria innocua,and Staphylococcus aureus Survival in GI conditions Traditional fermented soybean paste China Soybean Lb. plantarum Survival in GI conditions Li et al. (2015) Antimicrobial activity against Escherichia coli, Staphylococcus aureus, Salmonella sp., and Shigella sp. Adherence to Caco-2 Inhibits adhesion of pathogens to Caco-2 Table 2 Microorganisms isolated from some Mexican traditional fermented cereal beverages Product Substrate Sensory properties Fermentation time Microorganisms State References Atole agrio Nixtamalized maize Acid taste Until 3 days Lb. acidophilus and Lb. plantarum, Chiapas Sánchez-Dirzo et al. (2010) Saccharomyces cerevisiae Pozol Nixtamalized maize Acid taste, refreshing, Until 4 days Streptococcus, Streptococcus suis, Campeche, Chiapas, Oaxaca, Ulloa and Herrera (1972); non-alcoholic S. bovis, Enterococcus, Exiguobacterium, Quintana Roo, Tabasco, Wacher-Rodarte et al. (1993); Lc. lactis, Lc. raffinolactis, L. mesenteroides, and Yucatán Nuraida et al. (1995); Lb. confusus, Lb. fermentum, Lb. plantarum, ben Omar and Ampe (2000); Lb. casei, Lb. delbrueckii, Lb. alimentarium, Wacher-Rodarte et al. (2000); Bifidobacterium Escalante et al. (2001); Díaz-Ruíz et al. (2003) Tesgüino Germinated maize Acid taste, refreshing Until 3 days Candida guilliermondii, Hansenula anomala, Chihuahua, Durango, Jalisco, Ulloa et al. (1987); S. kluyveri, Saccharomyces cerevisiae Nayarit, Oaxaca, Sinaloa, Lappe and Ulloa (1989); and Sonora Wacher-Rodarte (1995) Ann Microbiol (2017) 67:577–586 581 (Nuraida et al. 1995). Streptococcus and Enterococcus have also been found in traditional cereal-based fermented bever- ages in Mexico, such as pozol (ben Omar and Ampe 2000; Escalante et al. 2001). In this regard, strains of Streptococcus genera, L. pseudomesenteroides and Weissella paramesenteroides isolated from pozol, present probiotic po- tential, since the microorganisms are able to survive under low pH and bile salts conditions and to adhere to HEp2 cells (Rodríguez et al. 2011). Agrobacterium azotophilium is a bacterium, reported in pozol, that have the ability to produce an antimicrobial com- pound with a broad spectrum (Ray et al. 2000). Saccharomyces cerevisiae has been present in the fermen- tation of traditional fermented beverages of Mexico, which is widely recognized as safe for use in food for human consump- tion and can present probiotic potential. Other yeasts like S. kluyveri, Candida guilliermondii,and Hansenula anomala are also found in traditional fermented beverages of Mexico, and although there have been no studies on their probiotic potential, are good options to consider (Ulloa et al. 1987; Wacher-Rodarte 1995). Meanwhile, Pichia kudriavzevii and Clavispora lusitaniae have been isolated from atole agrio, showing probiotic characteristics (growth capacity at 37 °C, low pH, and in the presence of bile salts survival, and biofilm formation) (Manrique-Donrronsoro et al. 2016). Fruits There are a great variety of fermented drinks made with fruits from Africa, Asia, and Latin America. Grape wine is probably the most important fermented drink, economically speaking, although there are also beverages made with fruits such as dates in North Africa, jackfruit in Asia, and pineapple in Latin America (Battcock 1998). The spontaneous fermentation of these beverages is mainly basedonLAB (Lactobacillus, Leuconostoc, Pediococcus, etc.) and yeast (Saccharomyces, Hansenula, Candida, etc.) found on the fruit surface (Table 3; Di Cagno et al. 2013) and in utensils used during processing (Fleet 2003). Tepache is a traditional Mexican fermented beverage from the pineapple shell. It is a product that can prevent contami- nation caused by canning industries, since the making of pre- serves like pineapple in syrup generates a great amount of waste, which can be transformed into a beverage for human consumption, with nutrients and vitamins obtained from fermenting microorganisms. The presence of several species of Lactobacillus,such as Lb. plantarum, has been reported (Alvarado et al. 2006). In this beverage, bacteriocin- producing bacteria (Lc. lactis, E. faecium) have also been reported, pointing to the beverage as a natural source of po- tential antimicrobials (de la Fuente-Salcido et al. 2015). Leuconostoc mesenteroides is also present in tepache,andis able to produce a bacteriocin named mesentericin, besides Table 3 Microorganisms isolated from some traditional fermented Mexican beverages made from fruit Product Substrate Sensory properties Fermentation time Microorganisms State References Tepache Pineapple Refreshing, low alcohol Up to 3 days Lb. plantarum, L. mesenteroides, Lactobacillus sp., Nava-Garduño (1953); content, sour taste Lc. lactis, Hanseniaspora, Torulopsis inconspicua, Herreraand Ulloa(1982); Saccharomyces cerevisiae, Pichia membranaefaciens, Moreno-Terrazas (2005); Candida queretana Alvarado et al. (2006); de la Fuente-Salcido et al. (2015) Colonche Red prickly Sweet and pleasant taste Up to 3 days Candida valida, Saccharomyces cerevisiae, Chihuahua, Sonora, Diguet (1928); Torulopsis taboadae, Pichia fermentans Zacatecas Ulloa and Herrera (1978); Herrera and Ulloa (1981a); Ulloa et al. (1987); Rodríguez-Lerma et al. (2011) 582 Ann Microbiol (2017) 67:577–586 producing dextran, an extracellular polymer that has a wide Plants industrial use as coadjuvant, emulsifier, carrier, and stabilizer, and which may serve as a prebiotic for other beneficial micro- In Mexico, fermented beverages made from other sources organisms (Moreno-Terrazas 2005;Sarwatet al. 2008). such as agave, coconut palm, or coyol palm are also con- The only yeast recognized as probiotic (Saccharomyces sumed, and will be discussed below (Table 4). cerevisiae var. boulardii) was isolated from fruits of Pulque is one of the oldest beverages in Mexico and is Indochina called lychees (Czerucka et al. 2007), and obtained from the fermentation of the agave sap called agua fermented fruit beverages as well as fruits are a source of miel. Microorganisms that are part of this fermentation are probiotic microorganisms. As for the traditional fermented homo- and heterofermentative LAB (Lb. acidophilus, Lb. beverages of Mexico, S. cerevisiae is present in most of them hilgardii, Lb. plantarum, Lb. acetolerans, Lb. kefir, Lc. lactis (Corona-González et al. 2013). In addition, Hanseniaspora, sp. lactis, L. citreum, L. kimchii, L. mesenteroides, Torulopsis inconspicua , T. taboadae , Pichia L. pseudomesenteroides), an alcohol-producing bacteria membranaefaciens, P. fermentans,and Candida species, such (Zymomonas mobilis), γ-proteobacteria, Acetobacter as C. valida, are also common (Nava-Garduño 1953; malorum, A. pomorium, Microbacterium arborescens, Alvarado et al. 2006; Rodríguez-Lerma et al. 2011;de la Flavobacterium johnsoniae, Gluconobacter oxydans,and Fuente-Salcido et al. 2015). Candida queretana, identified Hafnia alvei (Sánchez-Marroquín 1967;Sánchez-Marroquín as a new species, was isolated from P. fermentans in the central et al. 1967;UlloaandHerrera 1976; Chellapandian et al. Mexican state of Querétaro (Herrera and Ulloa 1982). The 1988; Escalante et al. 2004, 2008), besides yeasts, mainly of search for new potentially probiotic yeasts is very important, the genus Saccharomyces (S. bayanus, S. cerevisiae, since many of the traditional fermented beverages in Mexico S. paradoxus) and others like Candida spp., C. parapsilosis, are obtained using yeasts as the starter microorganism Clavispora lusitaniae, Hanseniaspora uvarum, K. lactis, (Herrera and Ulloa 1982). K. marxianus, Pichia membranaefaciens, Pichia spp., and Torulaspora delbrueckii (Cervantes-Contreras and Pedroza- Tibicos as starters Rodríguez 2007; Lappe-Oliveras et al. 2008), that have been found in raw material such as agua miel; in this case, Traditional fermented fruit beverages from Mexico are some- L. mesenteroides with probiotic potential has been reported times inoculated with starters called tibicos, which play an in agua miel,aswellasin pulque fermentation (Castro- important role in the fermentation of tepache and colonche. Rodríguez et al. 2015; Giles-Gómez et al. 2016). Tibicos are macrocolonies, formed by symbiotic associa- Lactobacillus casei J57 (GenBank accession no. JN182264) tions of bacteria and yeasts, consisting of compact, whitish or was also reported in pulque, showing bile salt hydrolase ac- yellowish, translucent or opalescent, gelatinous masses tivity, a characteristic associated with the probiotic potential of crossed by fine veins or irregular shape and size. They are bacteria, due to an association with serum cholesterol- developed in sugary liquids kept at rest, and in fruits and its lowering effects (González-Vázquez et al. 2015; Patel et al. juices, such as pineapple (Herrera and Ulloa 1981b). 2010). In this beverage, Lb. sanfranciscensis was also found. Tibicos are very similar to water kefir grains, in relation to This bacteria showed anti-inflammatory properties in an their structure (Magalhães et al. 2010). Fermented beverages in vivo model in mice (Torres-Maravilla et al. 2016). with kefir grains, both milk and water, have been shown to On the other hand, the yeast Kluyveromyces marxianus improve health. Furthermore, potentially probiotic cultures isolated from pulque presented probiotic characteristics such have been isolated from these (Zanirati et al. 2015), indicating as antagonistic activity against Klebsiella pneumoniae,as well that tibicos may present microorganisms with probiotic as adhesion to gut mice, mainly (Mendoza-Gardeazábal potential. 2013). Yeasts such as Brettanomyces claussenii, Candida On the other hand, the fermented beverage from palm juice guilliermondii, C. valida, Cryptococcus albidus var. bidus, is known worldwide as Bpalm wine^, taking different names Rhodotorula rubra, and S. cerevisiae, and bacteria such as according to the region and the type of palm from which it is B. brevis, B. polymyxa, B. circulans, B. coagulans, made, for example, toddy or tari in India, mu, bandji, B. firmus, B. macerans,and B. pumilus (Rubio et al. 1993) ogogoro, nsafufuo, nsamba, mnazi, yongo, tua,or tubak in have been isolated from tibicos used for the fermentation of West Africa and South America (Ouoba et al. 2012). fruit beverages, although this microbial composition could In Mexico, palm wines are called taberna, which is obtain- vary at the species level, depending on each local product ed from the palm of coyol, and tuba, obtained from the coco- (Herrera and Ulloa 1981b). nut palm. These are artisanal beverages. For this reason, there Since tibicos are very popular and important in the prepa- is little information on the microbial diversity of palm wines ration of traditional fermented beverages, it would be neces- made in Mexico. However, it was noted the presence of Lc. sary to study the potential probiotic of such strains. lactis and E. faecium, bacteria with antimicrobial activity due Ann Microbiol (2017) 67:577–586 583 Table 4 Microorganisms isolated from some traditional fermented Mexican plants Product Substrate Sensory properties Fermentation time Microorganisms State References Pulque Agave Alcoholic beverage, white, Until 1 day Lb acidophilus, Lb. hilgardii, Lb. plantarum, Center of Mexico Sánchez-Marroquín (1967); viscose, and strong smell Lb. acetolerans, Lb. kefir, Lc. lactis sp., Sánchez-Marroquín et al. (1967); L. citreum, L. kimchii, L. mesenteroides, Ulloaand Herrera(1976); L. pseudomesenteroides, Zymomonas mobilis, Chellapandian et al. (1988); Acetobacter malorum, A. pomorium, Escalante et al. (2004, 2008); Microbacterium arborescens, Flavobacterium Cervantes-Contreras and Pedroza- johnsoniae, Gluconobacter oxydans, Hafnia alvei, Rodríguez (2007); Lappe-Oliveras S. bayanus, S. cerevisiae, S. paradoxus, Candida spp., et al. (2008) C. parapsilosis, Clavispora lusitaniae, Hanseniaspora uvarum, K. lactis, K. marxianus, Pichia membranaefaciens, Pichia spp., Torulaspora delbrueckii Taberna Coyol palm whitish, effervescent, sweet 1 day Fructobacillus durionis, F. fructosus, South of Mexico Balick (1990); Acetobacter pasteurianus, Lb. nagelii, Alcántara-Hernández et al. (2010); Lb. sucicola, Zymomonas mobilis, Santiago-Urbina et al. 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Published: Aug 3, 2017

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