Lactic Acid Bacteria

A Functional Approach

Marcela Albuquerque Cavalcanti de Albuquerque, Alejandra de Moreno de LeBlanc, Jean Guy LeBlanc, Raquel Bedani, Marcela Albuquerque Cavalcanti de Albuquerque, Alejandra de Moreno de LeBlanc, Jean Guy LeBlanc, Raquel Bedani

• Publisher: CRC Press
• Year: 2020
• ISBN:
  9780429749438
• Edition: 1
• Topic: Medicina
• Subtopic: Nutrición, dietética y bariatría

Lactic acid bacteria (LAB) are a diverse group of bacteria that comprise low GC content Gram-positive cocci or rods that produces lactic acid as the major end product of the fermentation process. Bifidobacterium genera may also be considered as a part of the LAB group for possessing some similar phenotypical characteristics despite the higher GC content. The key feature of LAB metabolism is efficient carbohydrate fermentation. This contributes to the production of several microbial metabolites that result in the improvement of flavor and texture of fermented foods, in addition to its positive impact on the human health when LAB is administered as a probiotic.

The book deals with advances made in the functionalities of LAB, such as their effect on vitamin D receptor expression, impact on neurodegenerative 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 probiotics in animal feed. The book also reviews the use of LAB and probiotic technologies to develop new functional foods and functional pharmaceuticals.

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 Pinto^1,*

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 30°C and 40°C, but some strains are able to grow at temperatures lower than 5°C or higher than 45°C (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]

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 (O₂^–) and 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 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.

Table 1: Autoinducer molecules in quorum sensing.

QS system	Signaling molecule	Bacterial group	Reference
AI-1	Many types of acyl homoserine lactones (AHLs) which vary in acyl chain length (4 to 18C) and substitution on C3 (H, OH, or O)	Gram-negative	Fuqua and Greenberg 2002
AI-2	Furanosyl borate diester or (2R,4S)-2-methyl-2,3,3,4-tetrahydroxytetrahidrofuran	Gram-negative and Gram-positive	Park et al. 2016
AI-3	Aromatic aminated, but final structure has not yet been elucidated	Salmonella, E. coli	Kendall and Sperandio 2014
AIPs	Autoinducer peptides (ex. Nisin A)	Gram-positive	Kleerebezem 2004
PQS	2-heptyl-3-hydroxy-4-quinolone	Pseudomonas aeruginosa	Heeb et al. 2011, Allegretta et al. 2017
HAQs	Hydroxyl-2-alkyl-quinolines or 2-alkyl-4(1H)-quinolones	Pseudomonas aeruginosa	Heeb et a...