Table Of ContentLACTIC 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
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A SCIENCE PUBLISHERS BOOK
A SCIENCE PUBLISHERS BOOK
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Library of Congress Cataloging-in-Publication Data
Names: Albuquerque, Marcela Albuquerque Cavalcanti de, 1984- editor. |
LeBlanc, Alejandra de Moreno de, editor. | LeBlanc, Jean Guy (Jean Guy
Joseph), editor. | Bedani, Raquel, editor.
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
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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
