Carbohydrate Metabolism Is Essential for the Colonization of Streptococcus thermophilus in the Digestive Tract of Gnotobiotic Rats

Thomas, Muriel; Wrzosek, Laura; Ben-Yahia, Leila; Noordine, Marie-Louise; Gitton, Christophe; Chevret, Didier; Langella, Philippe; Mayeur, Camille; Cherbuy, Claire; Rul, Françoise

doi:10.1371/journal.pone.0028789

Cited by 33 publications

(23 citation statements)

References 45 publications

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“…Similar results were obtained with other mono associated rats [20], [22]. On a molecular basis, it is also illustrated by the similar amounts of the cell cycle arrest protein p21 Cip1 and the proliferation marker cycline D2 between GF and BSL rats (data not shown).…”

Section: Discussionsupporting

confidence: 87%

“…salivarius 4.6, and L. fermentum 3.9.2 have been selected for their genetic equipment and their phenotypic attributes favorable to their survival in the gastrointestinal tract and their high potential for binding to the epithelial cells of the intestinal tract [8], [9]. Several studies have used a single species or a cocktail of bacteria for their probiotic potential on the host [31], [32]; however, only a few of them focused on the host response, particularly on the structural maturation of the epithelium that occurred in the presence of bacteria [20]–[22].…”

Section: Discussionmentioning

confidence: 99%

“…Most studies describe the education and modulation of the immune system when triggered by the microbiota [14], [15], but the intestinal microbiota is also involved in the proliferation and maturation of the GIT [16]–[19]. Previously, we have shown that the structural maturation of the GIT by microbiota is linked to a sequential activation of different proteins involved in proliferation (Ki67 and proliferating cell nuclear antigen, PCNA), and proteins involved in cell cycle arrest protein (p21 Cip1 and p27 Kip1 ) [20]–[22]. The epithelium homeostasis of the digestive tract is essential for the prevention of injury, inflammation, protection against pathogen infection, digestion and absorption of nutrients [23], however, little is known concerning the lactobacilli-linked effect.…”

Section: Introductionmentioning

confidence: 99%

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Behavior of Lactobacilli Isolated from Fermented Slurry (ben-saalga) in Gnotobiotic Rats

et al. 2013

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Most bacterial strains, which have been studied so far for their probiotic functions, are extensively used by manufacturers in developed countries. In our work, we sought to study a mix (called BSL) comprising three strains belonging to Lactobacillus fermentum, L. paraplantarum and L. salivarius, that were isolated from a traditional African pearl millet based fermented slurry. Our objective was to study this BSL cocktail in gnotobiotic rats, to evaluate their survival and their behavior in the digestive tract conditions. After a single oral inoculation of germfree rats with BSL, the species established stably in the digestive tract with the following hierarchy of abundance: L. salivarius> L. plantarum> L. fermentum. BSL cocktail was metabolically active since it produced 50 mM lactate and it expressed genes involved in binding mechanism in the caecum. Furthermore, the global morphology of the colon epithelium was not disturbed by the BSL cocktail. BSL cocktail did not modify mucus content and host mucus-related genes (MUC1, MUC2, MUC3 or resistin-like molecule β). The cocktail of lactobacilli enhanced the proliferating cell nuclear antigen (PCNA) at a level comparable to what was observed in conventional rats. PCNA was involved in proliferation and DNA repair, but the presence of the cocktail did not provoke proliferative events (with Ki67 as indicator), so we suppose BSL may help gut preservation. This work is the first step towards the selection of strains that are derived from traditional fermented food to formulate new probiotic mixture.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Behavior of Lactobacilli Isolated from Fermented Slurry (ben-saalga) in Gnotobiotic Rats

et al. 2013

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“…The clear winner in the competition for glucose was S. thermophilus (see Table S8a in the supplemental material). Consistently, streptococci dominate the small intestinal microbiota through the efficient and rapid uptake of simple carbohydrates (39), and carbohydrate metabolism is essential for the colonization of the intestine by S. thermophilus (54). The losers included L. lactis and K. pneumoniae.…”

Section: Discussionmentioning

confidence: 99%

Anoxic Conditions Promote Species-Specific Mutualism between Gut Microbes In Silico

Heinken

Thiele

2015

Appl Environ Microbiol

117

100

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bThe human gut is inhabited by thousands of microbial species, most of which are still uncharacterized. Gut microbes have adapted to each other's presence as well as to the host and engage in complex cross feeding. Constraint-based modeling has been successfully applied to predicting microbe-microbe interactions, such as commensalism, mutualism, and competition. Here, we apply a constraint-based approach to model pairwise interactions between 11 representative gut microbes. Microbe-microbe interactions were computationally modeled in conjunction with human small intestinal enterocytes, and the microbe pairs were subjected to three diets with various levels of carbohydrate, fat, and protein in normoxic or anoxic environments. Each microbe engaged in species-specific commensal, parasitic, mutualistic, or competitive interactions. For instance, Streptococcus thermophilus efficiently outcompeted microbes with which it was paired, in agreement with the domination of streptococci in the small intestinal microbiota. Under anoxic conditions, the probiotic organism Lactobacillus plantarum displayed mutualistic behavior toward six other species, which, surprisingly, were almost entirely abolished under normoxic conditions. This finding suggests that the anoxic conditions in the large intestine drive mutualistic cross feeding, leading to the evolvement of an ecosystem more complex than that of the small intestinal microbiota. Moreover, we predict that the presence of the small intestinal enterocyte induces competition over host-derived nutrients. The presented framework can readily be expanded to a larger gut microbial community. This modeling approach will be of great value for subsequent studies aiming to predict conditions favoring desirable microbes or suppressing pathogens.T he human intestine is inhabited by a complex ecosystem consisting of thousands of microbial species. Its collective genome (the microbiome) contains more than 150 times as many genes as our own genome (1). The community of gut microbes has coevolved with humans and has adapted to the competitive conditions in the intestine. Gut microbes differ in their metabolic potential to exploit various environmental conditions and to persist in the intestine (2). They respond differently to the availability of dietary nutrients (3). Moreover, the gut microbiota has to contend with a steep oxygen gradient, which ranges from a partial O 2 pressure of approximately 80 mm Hg to nearly anoxic conditions (4). The diverse physiology of the small intestine creates a wide range of local oxygen microenvironments that favor particular groups of bacteria (4). Furthermore, metabolic interaction patterns between microbes affect microbial growth. Generally, six types of speciesspecies interactions can be distinguished (5) (Fig. 1a). In the case of neutralism, two organisms do not depend on each other for growth. If shared resources become scarce, this condition leads to competition (5). In the gut, competition over fermentable carbohydrates typically arises (6). If only one...

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“…A number of works indicate that utilization of glucose, lactose and fructose by S. thermophilus is a common characteristic in all existing studies, while galactose, mannose, sucrose, maltose, melibiose, and raffinose utilizations have variable profiles [40,41,42,43,44,45,46,47]. At the same time, it has been found that carbohydrate metabolism is essential for the colonization of S. thermophilus in the digestive tract of gnotobiotic rats [48]. Colonization ability is an important determining factor for developing bacterial health function in humans.…”

Section: Technological and Functional Properties Of S Thermophilusmentioning

confidence: 99%

New Insights into Various Production Characteristics of Streptococcus thermophilus Strains

Cui

et al. 2016

IJMS

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Streptococcus thermophilus is one of the most valuable homo-fermentative lactic acid bacteria, which, for a long time, has been widely used as a starter for the production of fermented dairy products. The key production characteristics of S. thermophilus, for example the production of extracellular polysaccharide, proteolytic enzymes and flavor substances as well as acidifying capacity etc., have an important effect on the quality of dairy products. The acidification capacity of the strains determines the manufacturing time and quality of dairy products. It depends on the sugar utilization ability of strains. The production of extracellular polysaccharide is beneficial for improving the texture of dairy products. Flavor substances increase the acceptability of dairy products. The proteolytic activity of the strain influences not only the absorption of the nitrogen source, but also the formation of flavor substances. Different strains have obvious differences in production characteristics via long-time evolution and adaptation to environment. Gaining new strains with novel and desirable characteristics is an important long-term goal for researchers and the fermenting industry. The understanding of the potential molecular mechanisms behind important characteristics of different strains will promote the screening and breeding of excellent strains. In this paper, key technological and functional properties of different S. thermophilus strains are discussed, including sugar metabolism, proteolytic system and amino acid metabolism, and polysaccharide and flavor substance biosynthesis. At the same time, diversity of genomes and plasmids of S. thermophilus are presented. Advances in research on key production characteristics and molecular levels of S. thermophilus will increase understanding of molecular mechanisms of different strains with different important characteristics, and improve the industrialization control level for fermented foods.

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Carbohydrate Metabolism Is Essential for the Colonization of Streptococcus thermophilus in the Digestive Tract of Gnotobiotic Rats

Cited by 33 publications

References 45 publications

Behavior of Lactobacilli Isolated from Fermented Slurry (ben-saalga) in Gnotobiotic Rats

Behavior of Lactobacilli Isolated from Fermented Slurry (ben-saalga) in Gnotobiotic Rats

Anoxic Conditions Promote Species-Specific Mutualism between Gut Microbes In Silico

New Insights into Various Production Characteristics of Streptococcus thermophilus Strains

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