Chronic stress and captivity alter the cloacal microbiome of a wild songbird

Author:

Madden Anne A.12ORCID,Oliverio Angela M.34ORCID,Kearns Patrick J.1,Henley Jessica B.5ORCID,Fierer Noah56ORCID,Starks Philip T. B.1ORCID,Wolfe Benjamin E.1ORCID,Romero L. Michael1ORCID,Lattin Christine R.17ORCID

Affiliation:

1. Department of Biology, Tufts University, Medford, MA 02155, USA

2. The Microbe Institute, Everett, MA 02149, USA

3. Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523, USA

4. Yale School of the Environment, Yale University, New Haven, CT 06511, USA

5. Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80309, USA

6. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA

7. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA

Abstract

ABSTRACT There are complex interactions between an organism's microbiome and its response to stressors, often referred to as the ‘gut–brain axis’; however, the ecological relevance of this axis in wild animals remains poorly understood. Here, we used a chronic mild stress protocol to induce stress in wild-caught house sparrows (Passer domesticus), and compared microbial communities among stressed animals, those recovering from stress, captive controls (unstressed) and a group not brought into captivity. We assessed changes in microbial communities and abundance of shed microbes by culturing cloacal samples on multiple media to select for aerobic and anaerobic bacteria and fungi. We complemented this with cultivation-independent 16S and ITS rRNA gene amplification and sequencing, pairing these results with host physiological and immune metrics, including body mass change, relative spleen mass and plasma corticosterone concentrations. We found significant effects of stress and captivity on the house sparrow microbiomes, with stress leading to an increased relative abundance of endotoxin-producing bacteria – a possible mechanism for the hyperinflammatory response observed in captive avians. While we found evidence that the microbiome community partially recovers after stress cessation, animals may lose key taxa, and the abundance of endotoxin-producing bacteria persists. Our results suggest an overall link between chronic stress, host immune system and the microbiome, with the loss of potentially beneficial taxa (e.g. lactic acid bacteria), and an increase in endotoxin-producing bacteria due to stress and captivity. Ultimately, consideration of the host's microbiome may be useful when evaluating the impact of stressors on individual and population health.

Funder

National Science Foundation

Tufts University

Tufts Graduate School of Arts and Sciences

Tufts Institute of the Environment

Society of Integrative and Comparative Biology

Environmental Protection Agency

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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