LACTIC ACID BACTERIA A Functional Approach Editors Marcela Albuquerque Cavalcanti de Albuquerque Department of Food and Human Nutrition School of Pharmaceutical Sciences University of São Paulo São Paulo, SP, Brazil Food Research Center - FoRC University of São Paulo São Paulo, SP, Brazil Alejandra de Moreno de LeBlanc Centro de Referencia para Lactobacilos (CERELA-CONICET) San Miguel de Tucumán Argentina Jean Guy LeBlanc Centro de Referencia para Lactobacilos (CERELA-CONICET) San Miguel de Tucumán Argentina Raquel Bedani Department of Biochemical and Pharmaceutical Technology University of São Paulo São Paulo, SP, Brazil p, p, A SCIENCE PUBLISHERS BOOK A SCIENCE PUBLISHERS BOOK Cover credit: Fabiana Zan CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2020 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Version Date: 20191210 International Standard Book Number-13: 978-1-138-39163-5 (Hardback) Th is book contains information obtained from authentic and highly regarded sources. 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Title: Lactic acid bacteria : a functional approach / editors, Marcela Albuquerque Cavalcanti de Albuquerque, Alejandra de Moreno de LeBlanc, Jean Guy LeBlanc, and Raquel Bedani. Other titles: Lactic acid bacteria (Albuquerque) Description: Boca Raton : CRC Press, Taylor & Francis Group, [2020] | Includes bibliographical references and index. | Summary: “The book deals with advances made in the functionalities of lactic acid bacteria (LAB) such as, their effect on vitamin D receptor expression, impact on neurodegeneratives pathologies, production of B-vitamins for food bio-enrichment, production of bacteriocins to improve gut microbiota dysbiosis, production of metabolites from polyphenols and their effects on human health, effect on reducing the immunoreaction of food allergens, as biological system using time-temperature to improve food safety, and the use of probiotic in animal feed. The book also reviews the use of LAB and probiotics technologies to develop new functional foods and functional pharmaceutical”-- Provided by publisher. Identifiers: LCCN 2019056212 | ISBN 9781138391635 (hardback) Subjects: MESH: Lactobacillales--physiology | Probiotics--therapeutic use | Nutritive Value | Lactobacillales--metabolism | Functional Food--microbiology Classification: LCC QR82.L3 | NLM QU 145.5 | DDC 579.3/7--dc23 LC record available at https://lccn.loc.gov/2019056212 Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com Preface Lactic Acid Bacteria have been used for centuries in the food and beverage industries, first for food preservation, but in the last century also because of their health benefits. They are regarded as GRAS (generally regarded as safe) organisms for human consumption, and even benefit human health as in the case of probiotics. Probiotics are defined as “Life microorganisms, which, when administered in adequate amounts, confer a health benefit to the host”. Despite several decades of research on probiotics, the mechanisms of action of the bacteria are still far from being elucidated or understood. Topics covered in this book include such simple things as ‘what is an adequate amount?’, and ‘are multi-strain products better than single-strain products’? Probably, because health effects are strain dependent, and diseases and disorders are multifactorial, there are no straightforward answers to even these fundamental questions (Chapter 2). Lactic acid bacteria can also be used to enrich the vitamin B status of foods, through in situ production (Chapter 7), or they can interact with vitamin D and its receptor, through influencing the gut microbiota and thereby induce immunomodulatory effects (Chapter 6). They can also impact gut diseases and disorders such as inflammatory bowel disease and irritable bowel syndrome (Chapter 10). But also diseases and disorders distant from the gut, such as cardiovascular diseases (Chapter 12) and associated with that, obesity (Chapter 9), have been shown to be modulated by probiotics. Moreover, it has recently been discovered that they influence the brain and neurodegenerative pathologies too (Chapter 11). Several possible modes of action have been entertained, which range from the production of antimicrobial peptides called bacteriocins (Chapter 5); cell-cell communication through the production of quorum sensing molecules (Chapter 1); through (modulation of) production of short-chain fatty acids which play a role in gut homeostasis (Chapter 8) or metabolites of polyphenols with anti-inflammatory or even anticancer activity (Chapter 13). Furthermore, lactic acid bacteria may impact the bioavailability and digestibility of food components, such as minerals or proteins (Chapter 3), and in one particular application may be used to decrease the allergenicity of food by fermenting the immunostimulatory epitopes (Chapter 4). Apart from human health, they also impact animal health (and if these are used for human food consumption, then indirectly also again human health; Chapter 15). And because of their versatility, they can even be used as biological sensors for improving food safety (Chapter 14) and preventing spoilage, amongst others through their production of bacteriocins and acids. iv Lactic Acid Bacteria: A Functional Approach In this timely book, expert international authors have reviewed these selected hot- topics to provide an up-to-date overview. This book is essential reading for everyone aiming to functionally apply lactic acid bacteria/probiotics for human health, from the PhD student to the experienced scientist. Prof. Dr. Koen Venema Founder and CEO of Beneficial Microbes® Consultancy Chair of Gut Microbiology at the Centre for Healthy Eating & Food Innovation of Maastricht University – campus Venlo Contents Preface iii 1. Cell-Cell Communication in Lactic Acid Bacteria: Potential 1 Mechanisms Lima, EMF, Quecán, BXV, Cunha, LR, Franco, BDGMF, and Pinto, UM 2. Probiotic Dose-Response and Strain Number 15 Ouwehand, A 3. Role of Lactic Acid Bacteria in Impacting Nutrient Bioavailability 35 Hess, J 4. Lactic Acid Bacteria Application to Decrease Food Allergies 58 Bíscola, V, Albuquerque, MAC, Nunes, TP, Vieira, ADS and Franco, BDGM 5. Lactic Acid Bacteria Bacteriocins and their Impact on Human Health 79 Todorov, S and Chikindas, ML 6. Probiotics, Vitamin D, and Vitamin D Receptor in Health and Disease 93 Battistini, C, Nassani, N, Saad, SMI and Sun, J 7. B-Group Vitamin-Producing Lactic Acid Bacteria: A Tool to 106 Bio-Enrich Foods and Delivery Natural Vitamins to the Host Albuquerque, MAC, Terán, MM, Garutti, LHG, Cucik, ACC, Saad, SMI, Franco, BDGM and LeBlanc, JG 8. Effect of Short-Chain Fatty Acids Produced by Probiotics: 124 Functional Role Toward the Improvement of Human Health da Silva, MF, de Lima, MSF and Converti, A 9. Impact of Probiotics on Human Gut Microbiota and the 142 Relationship with Obesity Bianchi, F and Sivieri, K 10. Probiotics in the Management of Inflammatory Bowel Disease 170 and Irritable Bowel Syndrome Celiberto, LS, Vallance, BA and Cavallini, DCU vi Lactic Acid Bacteria: A Functional Approach 11. The Potential Use of Lactic Acid Bacteria in Neurodegenerative 191 Pathologies Perez Visñuk, D, Terán, MM, de Giori, GS, LeBlanc, JG and de Moreno de LeBlanc, A 12. The Role of the Microbiota and the Application of Probiotics 205 in Reducing the Risk of Cardiovascular Diseases Bedani, R and Saad, SMI 13. Metabolites of Polyphenols Produced by Probiotic Microorganisms 223 and Their Beneficial Effects on Human Health and Intestinal Microbiota Beres, C, Cabezudo, I and Maidin, NM 14. Application of Lactic Acid Bacteria in Time-Temperature 241 Integrators: A Tool to Monitor Quality and Safety of Perishable Foods Girardeau, A, Bíscola, V, Keravec, S, Corrieu, G and Fonseca, F 15. Impact of Probiotics on Animal Health 261 Sabo, SS, Villalobos, EF, Piazentin, ACM, Lopes, AM and Oliveira, RPS Index 291 1 Cell-Cell Communication in Lactic Acid Bacteria Potential Mechanisms Emília Maria França Lima,1 Beatriz Ximena Valencia Quecán,1 Luciana Rodrigues da Cunha,2 Bernadette Dora Gombossy de Melo Franco1 and Uelinton Manoel Pinto1,* Lactic Acid Bacteria Lactic acid bacteria (LAB) are a diverse group of bacteria, yet with similar properties and all produce lactic acid as an end product of the fermentation process (Ferreira 2012). Taxonomically, the species are found in the phylum Firmicutes, Class Bacilli and order Lactobacillales, and include the genera Lactobacillus, Lactococcus, Leuconostoc, Oenococcus, Pediococcus, Streptococcus, Enterococcus, Tetragenococcus, Aerococcus, Carnobacterium, Vagococcus and Weissella (De Angelis et al. 2007, Reddy et al. 2008) which are all low guanine-cytosine (GC) content organisms (< 50%). However, some authors also consider Atopobium and Bifidobacterium genera, from the Actinobacteria phylum, as belonging to the LAB group for sharing some similar characteristics (Ferreira 2012, Wedajo 2015), despite the higher GC content. Phenotypically, LAB are Gram-positive rods or cocci, catalase negative (some species can produce pseudocatalase), chemoorganotrophs and non-spore forming bacteria (Dellagio et al. 1994, Holt et al. 1994). They are aerotolerant, microaerophilic or facultative anaerobic microorganisms with optimum temperature of growth between 30ºC and 40ºC, but some strains are able to grow at temperatures lower than 5ºC or higher than 45ºC (Gorner and Valik 2004). 1 University of São Paulo, Food Research Center, Faculty of Pharmaceutical Sciences, São Paulo, SP, Brazil. Emails: [email protected]; [email protected]; [email protected] 2 Federal University of Ouro Preto, Nutrition School, Ouro Preto, MG, Brazil. Email: [email protected] * Corresponding author: [email protected] 2 Lactic Acid Bacteria: A Functional Approach The essential feature of LAB metabolism is efficient carbohydrate fermentation coupled to substrate-level phosphorylation. This group of bacteria exhibits an enormous capacity to degrade different carbohydrates and related compounds (Mozzi et al. 2010). Based on the end products of glucose metabolism they are classified as homofermentative and heterofermentative microorganisms (Ribeiro et al. 2014). Those that produce lactic acid as the major or sole products of glucose fermentation are designated homofermenters and include some Lactobacillus and most Enterococcus species, Lactococcus, Pediococcus, Streptococcus, Tetragenococcus and Vagococcus. Meanwhile, those that produce equal molar amounts of lactate, carbon dioxide, and ethanol from hexoses are designated heterofermentative, including Leuconostoc, some species of Lactobacillus, Oenococcus and Weissella (Jay et al. 2005). The apparent difference on the enzyme level between these two categories is the presence or absence of the key cleavage enzymes of the Embden-Meyerhof pathway (fructose 1,6-diphosphate) and the PK pathway (phosphoketolase). Lactic bacteria represent one of the most important groups of microorganisms for humans, both for their role in the production and preservation of food, as well as for the aspects related to human health (Ferreira 2012). Some members of this group, isolated from the intestinal tract of humans, possess probiotic characteristics, which when ingested in adequate amounts offer innumerous benefits to the host’s health, such as prevention of colon cancer (Dallal et al. 2015, Nouri et al. 2016), attenuation of intestinal constipation (Riezzo et al. 2018, Ou et al. 2019), reduction of serum cholesterol (Wang et al. 2018), improvement of lactose digestion (Dhama et al. 2016), stimulation of the immune system (Imani et al. 2013) and protection from allergy (Wu et al. 2016) and intestinal infections (Collado et al. 2006). Besides the human health benefits, LAB play a significant role in the food industries, both in food production and preservation. These cultures have been used as starter or adjunct cultures for the fermentation of foods and beverages, accelerating and directing its fermentation process (Leroy and Vuyst 2004). In addition, they contribute to the sensorial characteristics of these products by the acid production, degradation of proteins and lipids, and production of alcohols, aldehydes, acids, esters and sulphur compounds (Zotta et al. 2009). LAB also help to increase the safety and the shelf life of products by producing metabolites, such organic acids, bacteriocins and hydrogen peroxide which possess an inhibitory effect on the growth of pathogenic microorganisms (Servin 2004). The organic acid safety effect is related to the non- dissociated form of the molecule (Podolak et al. 1996), which being lipophilic and apolar can passively diffuse through the membrane (Kashket 1987) and promote acidification of the cellular cytoplasm and impairment of the metabolic function of the competing microorganism (Vasseur et al. 1999). Hydrogen peroxide promotes oxidation of sulfhydryl groups and inactivation of various enzymes. Moreover, it may alter the permeability of the cell membrane by peroxidation of lipids and further cause damages to DNA by the formation of free radicals such as (O–) and 2 hydroxyl (OH–) (Byezkowski and Gessner 1988). On the other hand, bacteriocins act promoting collapse of the membrane potential by means of electrostatic bonds with the phospholipids (negatively charged). After bonding, the hydrophobic portion of the bacteriocin is inserted in the membrane forming pores allowing the out flow of ions, mainly potassium and magnesium. This promotes dissipation of the proton motive force, compromising synthesis of macromolecules and production of energy Cell-Cell Communication in Lactic Acid Bacteria: Potential Mechanisms 3 and resulting in cell death (Montville et al. 1995). Studies have shown that regulation of bacteriocin production is contingent on cell density in a phenomenon known as ‘quorum sensing’ (Kuipers et al. 1998, Kleerebezem 2004, Johansen and Jespersen 2017). Quorum Sensing in Bacteria Bacteria can communicate and regulate the expression of several genes according to cell density. This mechanism is a type of communication known as quorum sensing (QS), which is based on the production, secretion, and detection of small signaling molecules, whose concentration correlates with the cell density of microorganisms secreting these molecules in the surroundings (Choudhary and Schmidt-Dannert 2010). All quorum sensing systems usually involve the synthesis of a biomolecule with low molecular weight, also termed autoinducer (AI), which is recognized by the responder cell (Declerck et al. 2007, LaSarre and Federle 2013). As bacterial population density increases, the concentration of autoinducer molecules in the environment also rises (Johansen and Jespersen 2017). Quorum sensing plays a role in many complex processes such as secretion of virulence factors, biofilm formation, sporulation, production of bacteriocins and antimicrobial compounds, among others; activities that would not be possible or beneficial in low population density (Rocha-Estrada et al. 2010, Saeidi et al. 2011, Smid and Lacroix 2013, Monnet and Gardan 2015, Johansen and Jespersen 2017, Quecán et al. 2018). The signaling molecules may be different according to each bacterial group, as shown in Table 1. The phenomenon has been extensively studied in Gram-negative bacteria, in which signaling is commonly mediated by acylated homoserine lactone molecules (AHLs), known as auto-inducer-1 (AI-1) (Kuipers 1998, Williams 2007, Papenfort and Bassler 2016). However, in Gram-positive bacteria, signaling usually occurs by auto-inducing peptides (AIP) (Kleerebezem et al. 1997, Banerjee and Ray 2017). New molecules have been discovered with the advancement of studies in the area, indicating the existence of alternative types of QS signaling mechanisms besides AHL and AIP (LaSarre and Federle 2013, Zhao et al. 2018). The molecule known as autoinducer 2 (AI-2) is associated with the quorum sensing in the two bacterial groups (Miller and Bassler 2001, Fuqua and Greenberg 2002), and there are also other molecules apart from these classes, such as the Pseudomonas quinolone signal (PQS) and the autoinducer-3 (AI-3) in Gram-negative bacteria. Autoinducer molecules clearly differ in structure and composition (Table 1), but have common characteristics such as high receptor specificity and transport across the cell membrane which may be active or passive (Vadakkan et al. 2018). Some signaling molecules can have a dual function, acting mainly as antimicrobial compounds, besides being involved in the QS system as inducer molecules (Sturme et al. 2007, Smid and Lacroix 2013). This is the case of bacteriocins, which will be discussed in more detail later in this chapter. Table 2 shows the most common signaling molecules involved in quorum sensing by LAB, like bacteriocin production. The mechanism of quorum sensing was first observed in Aliivibrio fischeri (formely Vibrio fischeri), a Gram-negative marine bacterium that produces bioluminescence and lives in symbiosis with the Hawaiian squid Euprymna scolopes