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    Distinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouse

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    Author
    van de Wouw, Marcel
    Walsh, Aaron M.
    Crispie, Fiona
    van Leuven, Lucas
    Lyte, Joshua M
    Boehme, Marcus
    Clarke, Gerard
    Dinan, Timothy G
    Cotter, Paul D.
    Cryan, John F
    Keyword
    Microbiota
    Kefir
    Mouse
    Brain
    Behaviour
    GABA
    Immunity
    Serotonin
    Reward
    Lactobacillus
    Date
    2020-05-18
    
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    URI
    https://doi.org/10.1186/s40168-020-00846-5; http://hdl.handle.net/11019/2165
    Citation
    van de Wouw, M., Walsh, A.M., Crispie, F. et al. Distinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouse. Microbiome 8, 67 (2020). https://doi.org/10.1186/s40168-020-00846-5
    Abstract
    Background Mounting evidence suggests a role for the gut microbiota in modulating brain physiology and behaviour, through bi-directional communication, along the gut-brain axis. As such, the gut microbiota represents a potential therapeutic target for influencing centrally mediated events and host behaviour. It is thus notable that the fermented milk beverage kefir has recently been shown to modulate the composition of the gut microbiota in mice. It is unclear whether kefirs have differential effects on microbiota-gut-brain axis and whether they can modulate host behaviour per se. Methods To address this, two distinct kefirs (Fr1 and UK4), or unfermented milk control, were administered to mice that underwent a battery of tests to characterise their behavioural phenotype. In addition, shotgun metagenomic sequencing of ileal, caecal and faecal matter was performed, as was faecal metabolome analysis. Finally, systemic immunity measures and gut serotonin levels were assessed. Statistical analyses were performed by ANOVA followed by Dunnett's post hoc test or Kruskal-Wallis test followed by Mann-Whitney U test. Results Fr1 ameliorated the stress-induced decrease in serotonergic signalling in the colon and reward-seeking behaviour in the saccharin preference test. On the other hand, UK4 decreased repetitive behaviour and ameliorated stress-induced deficits in reward-seeking behaviour. Furthermore, UK4 increased fear-dependent contextual memory, yet decreased milk gavage-induced improvements in long-term spatial learning. In the peripheral immune system, UK4 increased the prevalence of Treg cells and interleukin 10 levels, whereas Fr1 ameliorated the milk gavage stress-induced elevation in neutrophil levels and CXCL1 levels. Analysis of the gut microbiota revealed that both kefirs significantly changed the composition and functional capacity of the host microbiota, where specific bacterial species were changed in a kefir-dependent manner. Furthermore, both kefirs increased the capacity of the gut microbiota to produce GABA, which was linked to an increased prevalence in Lactobacillus reuteri. Conclusions Altogether, these data show that kefir can signal through the microbiota-gut-immune-brain axis and modulate host behaviour. In addition, different kefirs may direct the microbiota toward distinct immunological and behavioural modulatory effects. These results indicate that kefir can positively modulate specific aspects of the microbiota-gut-brain axis and support the broadening of the definition of psychobiotic to include kefir fermented foods. Video abstract.
    Funder
    Science Foundation Ireland
    Grant Number
    SFI/12/RC/2273; (15/JPHDHL/3270
    ae974a485f413a2113503eed53cd6c53
    https://doi.org/10.1186/s40168-020-00846-5
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    Teagasc publications in Biomed Central

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