Dissecting the Genetic Components of Adaptation of Escherichia coli to the Mouse Gut

Giraud, Antoine; Arous, Safia; Paepe, Marianne De; Gaboriau-Routhiau, Valérie; Bambou, Jean-Christophe; Rakotobé, Sabine; Lindner, Ariel B.; Taddéi, François; Cerf‐Bensussan, Nadine

doi:10.1371/journal.pgen.0040002

Cited by 93 publications

(108 citation statements)

References 51 publications

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“…In contrast to S. thermophilus, the implantation was maximal in a few days for Escherichia coli (32), R. gnavus and B. thetaiotaomicron (17), Lactobacillus casei and Bifidobacterium breve (33), and Lactococcus lactis (23). This adaptive response of S. thermophilus was not accompanied by significant morphological changes, contrary to what was observed with L. sakei or E. coli (28,34). The proteomic analysis of S. thermophilus before (milk inoculum) and after GIT transit (feces) shed light on its adaptive metabolic profile.…”

Section: Discussionmentioning

confidence: 63%

Impact of the Metabolic Activity of Streptococcus thermophilus on the Colon Epithelium of Gnotobiotic Rats

Rul

Ben-Yahia

Chegdani

et al. 2011

Journal of Biological Chemistry

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The thermophilic lactic acid bacterium Streptococcus thermophilus is widely and traditionally used in the dairy industry. Despite the vast level of consumption of S. thermophilus through yogurt or probiotic functional food, very few data are available about its physiology in the gastrointestinal tract (GIT). The objective of the present work was to explore both the metabolic activity and host response of S. thermophilus in vivo. Our study profiles the protein expression of S. thermophilus after its adaptation to the GIT of gnotobiotic rats and describes the impact of S. thermophilus colonization on the colonic epithelium. S. thermophilus colonized progressively the GIT of germ-free rats to reach a stable population in 30 days (10 8 cfu/g of feces). This progressive colonization suggested that S. thermophilus undergoes an adaptation process within GIT. Indeed, we showed that the main response of S. thermophilus in the rat's GIT was the massive induction of the glycolysis pathway, leading to formation of lactate in the cecum. At the level of the colonic epithelium, the abundance of monocarboxylic acid transporter mRNAs (SLC16A1 and SLC5A8) and a protein involved in the cell cycle arrest (p27 kip1 ) increased in the presence of S. thermophilus compared with germ-free rats. Based on different mono-associated rats harboring two different strains of S. thermophilus (LMD-9 or LMG18311) or weak lactate-producing commensal bacteria (Bacteroides thetaiotaomicron and Ruminococcus gnavus), we propose that lactate could be a signal produced by S. thermophilus and modulating the colon epithelium.Streptoccocus thermophilus belongs to the group of the thermophilic lactic acid bacteria and is traditionally and widely used as a starter in manufacturing dairy products (Emmental, Gruyere, Parmigiano, mozarella, yogurt, etc.). Yogurt, which results from the fermentation of milk by S. thermophilus and Lactobacillus delbrueckii sp. bulgaricus (L. bulgaricus), fulfills the current specifications required to be recognized as a probiotic product (1). The health beneficial effect of yogurt consumption is linked to the metabolic properties of S. thermophilus and L. bulgaricus. As such, it improves lactose digestion in the gastrointestinal tract (GIT) 3 through their lactose-hydrolyzing activity present in yogurt and in the GIT, thus reducing symptoms of lactose intolerance (2, 3).Yogurt cultures have been shown to induce other health benefits, such as reduction of diarrhea or allergic disorders as well as modulation of the immune system (1, 4). S. thermophilus is also present at high concentration in VSL#3, a probiotic mixture of eight different bacterial strains that possesses beneficial effects in several intestinal conditions (5, 6).Recent data indicate that strains related to S. thermophilus LMD-9 are among the 57 bacteria species found in the intestinal microbiota of 90% of 124 European individuals (7). In comparison with the overall human intestinal microbiota, S. thermophilus is a numerically nondominant species with variable levels...

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Section: Discussionmentioning

confidence: 63%

Impact of the Metabolic Activity of Streptococcus thermophilus on the Colon Epithelium of Gnotobiotic Rats

Rul

Ben-Yahia

Chegdani

et al. 2011

Journal of Biological Chemistry

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“…Giraud et al (2008) have suggested that, with respect to E. coli, mutations in global regulators allow physiological modifications to occur when bacteria must adapt to altered environments. Regulation of catabolic pathways in gut commensals must be extremely important in bowel habitats where available substrates may change from day to day because of alterations in dietary intake of the host.…”

Section: Discussionmentioning

confidence: 99%

Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach

et al. 2011

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Phylogenetic analysis of gut communities of vertebrates is advanced, but the relationships, especially at the trophic level, between commensals that share gut habitats of monogastric animals have not been investigated to any extent. Lactobacillus reuteri strain 100-23 and Lactobacillus johnsonii strain 100-33 cohabit in the forestomach of mice. According to the niche exclusion principle, this should not be possible because both strains can utilise the two main fermentable carbohydrates present in the stomach digesta: glucose and maltose. We show, based on gene transcription analysis, in vitro physiological assays, and in vivo experiments that the two strains can co-exist in the forestomach habitat because 100-23 grows more rapidly using maltose, whereas 100-33 preferentially utilises glucose. Mutation of the maltose phosphorylase gene (malA) of strain 100-23 prevented its growth on maltose-containing culture medium, and resulted in the numerical dominance of 100-33 in the forestomach. The fundamental niche of L. reuteri 100-23 in the mouse forestomach can be defined in terms of 'glucose and maltose trophism'. However, its realised niche when L. johnsonii 100-33 is present is 'maltose trophism'. Hence, nutritional adaptations provide niche differentiation that assists cohabitation by the two strains through resource partitioning in the mouse forestomach. This real life, trophic phenomenon conforms to a mathematical model based on in vitro bacterial doubling times, in vitro transport rates, and concentrations of maltose and glucose in mouse stomach digesta.

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“…This is because of the cells ability to more rapidly metabolize lactate, the sole electron donor and carbon source provided. Previous laboratory evolution studies have identified mutations in regulatory elements (Cooper et al, 2003;Crozat et al, 2005;Herring et al, 2006;Knight et al, 2006;D'Argenio et al, 2007;Giraud et al, 2008 et al, 2010), but these were all within global regulatory 'hubs' that subsequently affected gene expression on a large scale. In contrast, this study offers the finding of a mutated transcriptional regulator that appears to have a very narrow gene target, repression of two genes that encode for a single key enzyme.…”

Section: Discussionmentioning

confidence: 99%

Laboratory evolution of Geobacter sulfurreducens for enhanced growth on lactate via a single-base-pair substitution in a transcriptional regulator

et al. 2011

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The addition of organic compounds to groundwater in order to promote bioremediation may represent a new selective pressure on subsurface microorganisms. The ability of Geobacter sulfurreducens, which serves as a model for the Geobacter species that are important in various types of anaerobic groundwater bioremediation, to adapt for rapid metabolism of lactate, a common bioremediation amendment, was evaluated. Serial transfer of five parallel cultures in a medium with lactate as the sole electron donor yielded five strains that could metabolize lactate faster than the wild-type strain. Genome sequencing revealed that all five strains had non-synonymous single-nucleotide polymorphisms in the same gene, GSU0514, a putative transcriptional regulator. Introducing the single-base-pair mutation from one of the five strains into the wild-type strain conferred rapid growth on lactate. This strain and the five adaptively evolved strains had four to eight-fold higher transcript abundance than wild-type cells for genes for the two subunits of succinyl-CoA synthase, an enzyme required for growth on lactate. DNA-binding assays demonstrated that the protein encoded by GSU0514 bound to the putative promoter of the succinyl-CoA synthase operon. The binding sequence was not apparent elsewhere in the genome. These results demonstrate that a single-base-pair mutation in a transcriptional regulator can have a significant impact on the capacity for substrate utilization and suggest that adaptive evolution should be considered as a potential response of microorganisms to environmental change(s) imposed during bioremediation.

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Dissecting the Genetic Components of Adaptation of Escherichia coli to the Mouse Gut

Cited by 93 publications

References 51 publications

Impact of the Metabolic Activity of Streptococcus thermophilus on the Colon Epithelium of Gnotobiotic Rats

Impact of the Metabolic Activity of Streptococcus thermophilus on the Colon Epithelium of Gnotobiotic Rats

Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach

Laboratory evolution of Geobacter sulfurreducens for enhanced growth on lactate via a single-base-pair substitution in a transcriptional regulator

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