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

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dc.contributor.authorvan de Wouw, Marcel
dc.contributor.authorWalsh, Aaron M.
dc.contributor.authorCrispie, Fiona
dc.contributor.authorvan Leuven, Lucas
dc.contributor.authorLyte, Joshua M.
dc.contributor.authorBoehme, Marcus
dc.contributor.authorClarke, Gerard
dc.contributor.authorDinan, Timothy G.
dc.contributor.authorCotter, Paul D.
dc.contributor.authorCryan, John F.
dc.contributor.funderScience Foundation Irelanden
dc.date.accessioned2022-04-06T15:06:36Z
dc.date.available2022-04-06T15:06:36Z
dc.date.issued2020-05
dc.date.updated2022-04-06T14:40:05Z
dc.description.abstractBACKGROUND: 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.en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.articleid67en
dc.identifier.citationvan de Wouw, M., Walsh, A. M., Crispie, F., van Leuven, L., Lyte, J. M., Boehme, M., Clarke, G., Dinan, T. G., Cotter, P. D. and Cryan, J. F. (2020) 'Distinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouse', Microbiome, 8 , 67 (20pp). doi: 10.1186/s40168-020-00846-5en
dc.identifier.doi10.1186/s40168-020-00846-5en
dc.identifier.endpage20en
dc.identifier.issn2049-2618
dc.identifier.journaltitleMicrobiomeen
dc.identifier.startpage1en
dc.identifier.urihttps://hdl.handle.net/10468/13045
dc.identifier.volume8en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Research Centres/12/RC/2273/IE/Alimentary Pharmabiotic Centre (APC) - Interfacing Food & Medicine/en
dc.relation.projectinfo:eu-repo/grantAgreement/ANR//ANR-15-HDHL-0001/FR/A Menu for Brain Responses Opposing Stress-Induced Alterations in Cognition/AMBROSIACen
dc.rights© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.en
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/en
dc.subjectBehaviouren
dc.subjectBrainen
dc.subjectGABAen
dc.subjectImmunityen
dc.subjectKefiren
dc.subjectLactobacillusen
dc.subjectMicrobiotaen
dc.subjectMouseen
dc.subjectRewarden
dc.subjectSerotoninen
dc.titleDistinct actions of the fermented beverage kefir on host behaviour, immunity and microbiome gut-brain modules in the mouseen
dc.typeArticle (peer-reviewed)en
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