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Milk kefir alters fecal microbiota impacting gut and brain health in mice

  • Genomics, Transcriptomics, Proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Kefir is a fermented beverage made of a symbiotic microbial community that stands out for health benefits. Although its microbial profile is still little explored, its effects on modulation of gut microbiota and production of short-chain fatty acids (SCFAs) seems to act by improving brain health. This work aimed to analyze the microbiota profile of milk kefir and its effect on metabolism, oxidative stress, and in the microbiota-gut-brain axis in a murine model. The experimental design was carried out using C57BL-6 mice (n = 20) subdivided into groups that received 0.1 mL water or 0.1 mL (10% w/v) kefir. The kefir proceeded to maturation for 48 h, and then it was orally administered, via gavage, to the animals for 4 weeks. Physicochemical, microbiological, antioxidant analyzes, and microbial profiling of milk kefir beverage were performed as well as growth parameters, food intake, serum markers, oxidative stress, antioxidant enzymes, SCFAs, and metabarcoding were analyzed in the mice. Milk kefir had 76.64 ± 0.42% of free radical scavenging and the microbiota composed primarily by the genus Comamonas. Moreover, kefir increased catalase and superoxide dismutase (colon), and SCFAs in feces (butyrate), and in the brain (butyrate and propionate). Kefir reduced triglycerides, uric acid, and affected the microbiome of animals increasing fecal butyrate-producing bacteria (Lachnospiraceae and Lachnoclostridium). Our results on the brain and fecal SCFAs and the antioxidant effect found were associated with the change in the gut microbiota caused by kefir, which indicates that kefir positively influences the gut-microbiota-brain axis and contributes to the preservation of gut and brain health.

Graphical Abstract

Key points

• Milk kefir modulates fecal microbiota and SCFA production in brain and colon.

• Kefir treatment increases the abundance of SCFA-producing bacteria.

• Milk kefir increases antioxidant enzymes and influences the metabolism of mice.

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Data availability

Illumina Hiseq raw sequences generated and analyzed during the current study are available in the Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/sra/PRJNA925110) under the BioProject PRJNA925110.

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Acknowledgements

The authors thank the National Council for Scientific and Technological Development (CNPq), Coordination for the Improvement of Higher Education Personnel (CAPES) – Financing Code 001, and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the support to the researches. We thank the Diretoria de Tecnologia de Informação (DTI) at Universidade Federal de Viçosa for the availability of the computational cluster and software used in this work, also thank the Rede Minas Microbiomas for the metagenomic analysis funding.

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Authors and Affiliations

Authors

Contributions

AOBR, TAOM and MCGP, Conceptualization; MFAP, LGMA, GCAA, TAOM, and MCGP, Data curation; MFAP, LGMA, GCAA, TAOM, and MCGP, Formal analysis; AOBR, TAOM and MCGP Funding acquisition; MFAP, LGMA, GCAA, BCSC, LFA, JMS, ALB, IXC, AOBR, TAOM, and MCGP Investigation; MFAP, LGMA, GCAA, BCSC, LFA, JMS, ALB, IXC, AOBR, TAOM and MCGP, Methodology; TAOM and MCGP, Project administration; AOBR, TAOM and MCGP, Resources; MFAP, LGMA, and TAOM, Software; AOBR, TAOM and MCGP, Supervision; MFAP, LGMA, GCAA, BCSC, LFA, JMS, ALB, IXC, AOBR, TAOM, and MCGP, Validation; MFAP, LGMA, GCAA, TAOM, and MCGP, Visualization; MFAP, LGMA, GCAA, Writing—original draft; MFAP, LGMA, GCAA, BCSC, LFA, JMS, ALB, IXC, AOBR, TAOM, and MCGP, Writing—review & editing. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Maria do Carmo Gouveia Peluzio.

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All authors declare that they have no conflict of interest.

Ethical approval

The experimental protocol was approved by the National Technical Commission on Biosafety (CTNBio) and by the Ethics Committee on Animal Experimentation (CEUA) of the Federal University of Viçosa (Universidade Federal de Viçosa, Minas Gerais, Brazil), under process number 35/2020, in compliance with current legislation (Law No. 11,794, of October 8, 2008). The experiment was conducted following the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines, the European Community Guidelines (Directive 2010/63/EU), and the normative resolutions issued by the National Research Council's Guide for the Care and Use of Laboratory Animals, as well as the National Council for the Control of Animal Experimentation (CONCEA), the Brazilian Practice Guideline for the Care and Use of Animals for Scientific and Didactic Purposes (DBCA), and the Guidelines for the Practice of Euthanasia recommended by CONCEA.

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Albuquerque Pereira, M.d.F., Morais de Ávila, L.G., Ávila Alpino, G.d.C. et al. Milk kefir alters fecal microbiota impacting gut and brain health in mice. Appl Microbiol Biotechnol 107, 5161–5178 (2023). https://doi.org/10.1007/s00253-023-12630-0

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  • DOI: https://doi.org/10.1007/s00253-023-12630-0

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