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Lifestyle of Lactobacillus plantarum in the mouse caecum.

ABSTRACT: Lactobacillus plantarum is a common inhabitant of mammalian gastrointestinal tracts. Strains of L. plantarum are also marketed as probiotics intended to confer beneficial health effects upon delivery to the human gut. To understand how L. plantarum adapts to its gut habitat, we used whole genome transcriptional profiling to characterize the transcriptome of strain WCFS1 during colonization of the caeca of adult germ-free C57Bl/6 J mice fed a standard low-fat rodent chow diet rich in complex plant polysaccharides or a prototypic Western diet high in simple sugars and fat. Lactobacillus plantarum colonized the digestive tracts of these animals to high levels, although L. plantarum was found in 10-fold higher amounts in the caeca of mice fed the standard chow. Metabolic reconstructions based on the transcriptional data sets revealed that genes involved in carbohydrate transport and metabolism form the principal functional group that is upregulated in vivo compared with exponential phase cells grown in three different culture media, and that a Western diet provides a more nutritionally restricted, growth limiting milieu for the microbe in the distal gut. A set of bacterial genes encoding cell surface-related functions were differentially regulated in both groups of mice. This set included downregulated genes required for the d-alanylation of lipoteichoic acids, extracellular structures of L. plantarum that mediate interactions with the host immune system. These results, obtained in a reductionist gnotobiotic mouse model of the gut ecosystem, provide insights about the niches (professions) of this lactic acid bacterium, and a context for systematically testing features that affect epithelial and immune cell responses to this organism in the digestive tract.

SUBMITTER: Marco ML

PROVIDER: S-EPMC2978903 | biostudies-literature | 2009 Oct

REPOSITORIES: biostudies-literature

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Lifestyle of Lactobacillus plantarum in the mouse caecum.

Marco Maria L ML Peters Theodorus H F TH Bongers Roger S RS Molenaar Douwe D van Hemert Saskia S Sonnenburg Justin L JL Gordon Jeffrey I JI Kleerebezem Michiel M

Environmental microbiology 20090720 10

Lactobacillus plantarum is a common inhabitant of mammalian gastrointestinal tracts. Strains of L. plantarum are also marketed as probiotics intended to confer beneficial health effects upon delivery to the human gut. To understand how L. plantarum adapts to its gut habitat, we used whole genome transcriptional profiling to characterize the transcriptome of strain WCFS1 during colonization of the caeca of adult germ-free C57Bl/6 J mice fed a standard low-fat rodent chow diet rich in complex plan ...[more]

PMID: 19638173

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Project description:Lactobacillus plantarum is a common inhabitant of mammalian gastrointestinal tracts and specific strains belonging to this species are marketed as probiotics intended to confer beneficial health effects. To assist in determining the physiological status and host-microbe interactions of L. plantarum in the digestive tract we assessed changes in the transcriptome of L. plantarum WCFS1 during colonization of the cecum of germ-free mice. According to the transcript profiles L. plantarum WCFS1 was metabolically active and not under severe stress in this intestinal compartment. Carbohydrate metabolism was the most strongly affected functional gene category whereby many genes encoding diverse sugar transport and degradation pathways were induced in mice even compared to L. plantarum grown in a mouse chow-derived laboratory medium. This suggests that the ability of L. plantarum WCFS1 to consume diverse energy sources including plant-associated and host-derived carbohydrates was increased during its residence in the digestive tract. Many of these genes were also induced in L. plantarum colonizing germ-free mice fed a humanized Western-style diet. Similarly a core set of genes encoding cell surface-related properties were differentially expressed in mice. This set includes genes required for the D-alanylation and glycosylation of lipoteichoic acids that were strongly down-regulated in mice. In total L. plantarum exhibits a distinct in vivo transcriptome directed towards adaptation to the mouse intestinal environment. Keywords: cell type comparison Six-week old germ-free C57 Black-6 male mice were inoculated with a single dose of 109 CFU of exponential-phase L. plantarum WCFS1 cells. The mice were sacrificed 15 days later, after sufficient time had passed for several turnovers of the intestinal epithelium and its overlying mucosal layer. Four mice were fed on Chow diet and two mice were fed on western style diet. RNA was isolated from the cecum of these mice. The transcriptome of L. plantarum in these mice was compared to that of L. plantarum grown on MRS broth, Chow broth, or on chemically defined media with either glucose or lactose as carbon- and energy source.

Project description:Heat stress resistance and response were studied in strains of Lactobacillus plantarum. Stationary-phase cells of L. plantarum DPC2739 had decimal reduction times (D values) (D value was the time that it took to reduce the number of cells by 1 log cycle) in sterile milk of 32.9, 14.7, and 7.14 s at 60, 72, and 75 degrees C, respectively. When mid-exponential-phase cells were used, the D values decreased. The temperature increases which caused a 10-fold reduction in the D value ranged from 9 to 20 degrees C, depending on the strain. Part of the cell population treated at 72 degrees C for 90 s recovered viability during incubation at 7 degrees C in sterile milk for 20 days. When mid-exponential- or stationary-phase cells of L. plantarum DPC2739 were adapted to 42 degrees C for 1 h, the heat resistance at 72 degrees C for 90 s increased ca. 3 and 2 log cycles, respectively. Heat-adapted cells also showed increased growth at pH 5 and in the presence of 6% NaCl. Two-dimensional gel electrophoresis of proteins expressed by control and heat-adapted cells revealed changes in the levels of expression of 31 and 18 proteins in mid-exponential- and stationary-phase cells, respectively. Twelve proteins were commonly induced. Nine proteins induced in the heat-adapted mid-exponential- and/or stationary-phase cells of L. plantarum DPC2739 were subjected to N-terminal sequencing. These proteins were identified as DnaK, GroEL, trigger factor, ribosomal proteins L1, L11, L31, and S6, DNA-binding protein II HlbA, and CspC. All of these proteins have been found to play a role in the mechanisms of stress adaptation in other bacteria. Antibodies against GroES detected a protein which was induced moderately, while antibodies against DnaJ and GrpE reacted with proteins whose level of expression did not vary after heat adaptation. This study showed that the heat resistance of L. plantarum is a complex process involving proteins with various roles in cell physiology, including chaperone activity, ribosome stability, stringent response mediation, temperature sensing, and control of ribosomal function. The physiological mechanisms of response to pasteurization in L. plantarum are fundamental for survival in cheese during manufacture.

Dataset Information

Lifestyle of Lactobacillus plantarum in the mouse caecum.

Publications

Lifestyle of Lactobacillus plantarum in the mouse caecum.

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