A Comparative Pan-Genome Perspective of Niche-Adaptable Cell-Surface Protein Phenotypes in Lactobacillus rhamnosus

Kant, Ravi; Rintahaka, Johanna; Xia, Yu; Sigvart-Mattila, Pia; Paulín, Lars; Mecklin∥, Jukka–Pekka; Saarela, Maria; Palva, Airi; Ossowski, Ingemar von

doi:10.1371/journal.pone.0102762

Cited by 47 publications

(61 citation statements)

References 67 publications

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“…28 It has been also shown that L. rhamnosus strains carrying particular genomic alterations will likely possess an increased niche-specific fitness. 29 In addition, it has been recently shown that allelic variants of bacterial proteins in the Salmonella enterica serovar Typhimurium likely contribute to pathoadaption to diverse hosts. 30 On the other hand, studying how variations in the host genome will predispose to colonization by specific bacterial strands will also be of interest for understanding the etiology of disease.…”

Section: Discussionmentioning

confidence: 99%

Epigenome-Microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease

et al. 2016

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Preterm birth is the leading cause of infant morbidity and mortality. Necrotizing enterocolitis (NEC) is an inflammatory bowel disease affecting primarily premature infants, which can be lethal. Microbial intestinal colonization may alter epigenetic signatures of the immature gut establishing inflammatory and barrier properties predisposing to the development of NEC. We hypothesize that a crosstalk exists between the epigenome of the host and the initial intestinal colonizing microbiota at critical neonatal stages. By exposing immature enterocytes to probiotic and pathogenic bacteria, we showed over 200 regions of differential DNA modification, which were specific for each exposure. Reciprocally, using a mouse model of prenatal exposure to dexamethasone we demonstrated that antenatal treatment with glucocorticoids alters the epigenome of the host. We investigated the effects on the expression profiles of genes associated with inflammatory responses and intestinal barrier by qPCR-based gene expression array and verified the DNA modification changes in 5 candidate genes by quantitative methylation specific PCR (qMSP). Importantly, by 16S RNA sequencing-based phylogenetic analysis of intestinal bacteria in mice at 2 weeks of life, we showed that epigenome changes conditioned early microbiota colonization leading to differential bacterial colonization at different taxonomic levels. Our findings support a novel conceptual framework in which epigenetic changes induced by intrauterine influences affect early microbial colonization and intestinal development, which may alter disease susceptibility.

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Section: Discussionmentioning

confidence: 99%

Epigenome-Microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease

et al. 2016

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“…For these aforementioned activities, the SpaC subunit is credited as a key adhesive factor, but as well, its functionality was quite recently shown to be essential for helping elicit various cellular responses in gut epithelial cells, such as generating reactive oxygen species (ROS), activating the extracellular signal-regulated kinase (ERK) and mitogen-activated protein kinase (MAPK) pathways, and protecting against radiation-induced intestinal damage [10]. Of particular interest, recent findings from our own pan-genome study provide suggestive evidence that the spaCBA pilus operon is in fact a rare occurrence in the genome of the L. rhamnosus species [11]. Accordingly, for any piliated L. rhamnosus strains, it is likely that they will have an augmented niche-specific fitness.…”

Section: Introductionmentioning

confidence: 99%

Phenotypical Analysis of the Lactobacillus rhamnosus GG Fimbrial spaFED Operon: Surface Expression and Functional Characterization of Recombinant SpaFED Pili in Lactococcus lactis

et al. 2014

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A noticeable genomic feature of many piliated Gram-positive bacterial species is the presence of more than one pilus-encoding operon. Paradigmatically, the gut-adapted Lactobacillus rhamnosus GG strain contains two different fimbrial operons in its genome. However, whereas one of these operons (called spaCBA) is encoding for the functionally mucus-/collagen-binding SpaCBA pilus, for the other operon (called spaFED) any native expression of the SpaFED-called pili is still the subject of some uncertainty. Irrespective of such considerations, we decided it would be of relevance or interest to decipher the gross structure of this pilus type, and as well assess its functional capabilities for cellular adhesion and immunostimulation. For this, and by following the approach we had used previously to explicate the immuno-properties of SpaCBA pili, we constructed nisin-inducible expression clones producing either wild-type or SpaF pilin-deleted surface-assembled L. rhamnosus GG SpaFED pili on Lactococcus lactis cells. Using these piliated lactococcal constructs, we found that the pilin-polymerized architecture of a recombinant-produced SpaFED pilus coincides with sequence-based functional predictions of the related pilins, and in fact is prototypical of those other sortase-dependent pilus-like structures thus far characterized for piliated Gram-positive bacteria. Moreover, we confirmed that among the different pilin subunits encompassing spaFED operon-encoded pili, the SpaF pilin is a main adhesion determinant, and when present in the assembled structure can mediate pilus binding to mucus, certain extracellular matrix proteins, and different gut epithelial cell lines. However, somewhat unexpectedly, when recombinant SpaFED pili are surface-attached, we found that they could not potentiate the existing lactococcal cell-induced immune responses so elicited from intestinal- and immune-related cells, but rather instead, they could dampen them. Accordingly, we have now provided the first phenotypical description of a spaFED pilus operon, and with that furthered the functional understanding of surface piliation for a particular gut-commensalic genre of piliated Gram-positive bacteria.

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“…Such a functional heterogeneity was possibly related to the genetic heterogeneity previously observed within the L. paracasei species . A similar genetic diversity was observed in the L. rhamnosus species . Altogether, these data support the idea that the biological effects of probiotics on the immune system are strain specific.…”

Section: Discussionmentioning

confidence: 99%

Individual strains ofLactobacillus paracaseidifferentially inhibit human basophil and mouse mast cell activation

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Lalanne

Garault

et al. 2016

Immunity, Inflammation and Disease

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IntroductionThe microbiota controls a variety of biological functions, including immunity, and alterations of the microbiota in early life are associated with a higher risk of developing allergies later in life. Several probiotic bacteria, and particularly lactic acid bacteria, were described to reduce both the induction of allergic responses and allergic manifestations. Although specific probiotic strains were used in these studies, their protective effects on allergic responses also might be common for all lactobacilli.MethodsTo determine whether allergic effector cells inhibition is a common feature of lactobacilli or whether it varies among lactobacilli strains, we compared the ability of 40 strains of the same Lactobacillus paracasei species to inhibit IgE‐dependent mouse mast cell and human basophil activation.ResultsWe uncovered a marked heterogeneity in the inhibitory properties of the 40 Lactobacillus strains tested. These segregated into three to four clusters depending on the intensity of inhibition. Some strains inhibited both mouse mast cell and human basophil activation, others strains inhibited only one cell type and another group induced no inhibition of activation for either cell type.ConclusionsIndividual Lactobacillus strains of the same species differentially inhibit IgE‐dependent activation of mouse mast cells and human basophils, two cell types that are critical in the onset of allergic manifestations. Although we failed to identify specific bacterial genes associated with inhibition by gene‐trait matching analysis, our findings demonstrate the complexity of the interactions between the microbiota and the host. These results suggest that some L. paracasei strains might be more beneficial in allergies than others strains and provide the bases for a rational screening of lactic acid bacteria strains as next‐generation probiotics in the field of allergy.

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A Comparative Pan-Genome Perspective of Niche-Adaptable Cell-Surface Protein Phenotypes in Lactobacillus rhamnosus

Cited by 47 publications

References 67 publications

Epigenome-Microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease

Epigenome-Microbiome crosstalk: A potential new paradigm influencing neonatal susceptibility to disease

Phenotypical Analysis of the Lactobacillus rhamnosus GG Fimbrial spaFED Operon: Surface Expression and Functional Characterization of Recombinant SpaFED Pili in Lactococcus lactis

Individual strains ofLactobacillus paracaseidifferentially inhibit human basophil and mouse mast cell activation

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