The gut microbiota-immune-brain axis in a wild vertebrate: dynamic interactions and health impacts

Hugo Pereira; Joseph I Hoffman; Oliver Krüger; Gábor Á Czirják; Tony Rinaud; Meinolf Ottensmann; Kai-Philipp Gladow; Barbara A Caspers; Öncü Maraci; Sylvia Kaiser; Nayden Chakarov

doi:10.3389/fmicb.2024.1413976

The gut microbiota-immune-brain axis in a wild vertebrate: dynamic interactions and health impacts

Front Microbiol. 2024 Sep 10:15:1413976. doi: 10.3389/fmicb.2024.1413976. eCollection 2024.

Authors

Hugo Pereira¹, Joseph I Hoffman^#^{1

2

3

4

5}, Oliver Krüger^#^{1

3}, Gábor Á Czirják^#⁶, Tony Rinaud¹, Meinolf Ottensmann¹, Kai-Philipp Gladow¹, Barbara A Caspers^{3

7}, Öncü Maraci^{3

7}, Sylvia Kaiser^{3

8}, Nayden Chakarov^#^{1

3}

Affiliations

¹ Department of Animal Behaviour, Bielefeld University, Bielefeld, Germany.
² Department of Evolutionary Population Genetics, Bielefeld University, Bielefeld, Germany.
³ Joint Institute for Individualisation in a Changing Environment, Bielefeld University and University of Münster, Bielefeld, Germany.
⁴ British Antarctic Survey, Cambridge, United Kingdom.
⁵ Center for Biotechnology (CeBiTec), Faculty of Biology, Bielefeld University, Bielefeld, Germany.
⁶ Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany.
⁷ Department of Behavioural Ecology, Bielefeld University, Bielefeld, Germany.
⁸ Department of Behavioural Biology, University of Münster, Münster, Germany.

^# Contributed equally.

Abstract

The gut microbiota-immune-brain axis is a feedback network which influences diverse physiological processes and plays a pivotal role in overall health and wellbeing. Although research in humans and laboratory mice has shed light into the associations and mechanisms governing this communication network, evidence of such interactions in wild, especially in young animals, is lacking. We therefore investigated these interactions during early development in a population of common buzzards (Buteo buteo) and their effects on individual condition. In a longitudinal study, we used a multi-marker approach to establish potential links between the bacterial and eukaryotic gut microbiota, a panel of immune assays and feather corticosterone measurements as a proxy for long-term stress. Using Bayesian structural equation modeling, we found no support for feedback between gut microbial diversity and immune or stress parameters. However, we did find strong relationships in the feedback network. Immunity was negatively correlated with corticosterone levels, and microbial diversity was positively associated with nestling body condition. Furthermore, corticosterone levels and eukaryotic microbiota diversity decreased with age while immune activity increased. The absence of conclusive support for the microbiota-immune-brain axis in common buzzard nestlings, coupled with the evidence for stress mediated immunosuppression, suggests a dominating role of stress-dominated maturation of the immune system during early development. Confounding factors inherent to wild systems and developing animals might override associations known from adult laboratory model subjects. The positive association between microbial diversity and body condition indicates the potential health benefits of possessing a diverse and stable microbiota.

Keywords: Buteo buteo; bacterial microbiota; body condition; eukaryotic microbiota; immune system; longitudinal study; stress.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft—DFG), as part of the SFB TRR 212 (NC3)—project numbers 316099922 and 396780709 and DFG project numbers 398434413, 433069365, and 233740704. The funding body had no involvement in the study design, data collection, analysis, interpretation, or manuscript writing.