University of Oulu

Brila, I., Lavrinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T., & Watts, P. C. (2023). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole Myodes glareolus. Journal of Animal Ecology, 92, 826– 837. https://doi.org/10.1111/1365-2656.13869

Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole Myodes glareolus

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Author: Brila, Ilze1,2; Lavrinienko, Anton2,3; Tukalenko, Eugene1,2,4;
Organizations: 1Ecology and Genetics Research Unit, University of Oulu, Oulu, Finland
2Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland
3Laboratory of Food Systems Biotechnology, Institute of Food, Nutrition and Health, ETH Zürich, Zurich, Switzerland
4Department of Radiobiology and Radioecology, Institute for Nuclear Research of National Academy of Science of Ukraine, Kyiv, Ukraine
5School of Resource Wisdom, University of Jyväskylä, Jyväskylä, Finland
Format: article
Version: accepted version
Access: embargoed
Persistent link: http://urn.fi/urn:nbn:fi-fe2023042739108
Language: English
Published: John Wiley & Sons, 2022
Publish Date: 2024-04-05
Description:

Abstract

1. The effects of systemic pathogens on gut microbiota of wild animals are poorly understood. Furthermore, coinfections are the norm in nature, yet most studies of pathogen–microbiota interactions focus on effects of single pathogen infections on gut microbiota.

2. We examined the effects of four systemic pathogens (bacteria Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato, apicomplexan protozoa Babesia microti and Puumala orthohantavirus) and coinfections among them on the (bacterial) gut microbiota of wild bank voles Myodes glareolus.

3. We hypothesized that: (1) the effects of coinfection on gut microbiota generally differ from those of a single pathogen infection, (2) systemic pathogens have individual (i.e. distinct) associations with gut microbiota, which are modified by coinfection and (3) the effects of coinfection (compared with those of single infection) are idiosyncratic (i.e. pathogen-specific).

4. The gut microbiota of coinfected bank voles differed from that of single pathogen infected individuals, although, as predicted, the effects of coinfections were unique for each pathogen. After accounting for coinfections, only Puumala orthohantavirus was associated with higher α-diversity; however, all pathogens affected gut microbiota ß-diversity in a pathogen-specific way, affecting both rare and abundant gut bacteria.

5. Our results showed that the effects of systemic pathogens on host’s gut microbiota vary depending on the pathogen species, resulting in idiosyncratic signatures of coinfection. Furthermore, our results emphasize that neglecting the impact of coinfections can mask patterns of pathogen–microbiota associations.

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Series: Journal of animal ecology
ISSN: 0021-8790
ISSN-E: 1365-2656
ISSN-L: 0021-8790
Volume: 92
Issue: 4
Pages: 826 - 837
DOI: 10.1111/1365-2656.13869
OADOI: https://oadoi.org/10.1111/1365-2656.13869
Type of Publication: A1 Journal article – refereed
Field of Science: 1181 Ecology, evolutionary biology
Subjects:
Funding: This research was funded through the 2017-2018 Belmont Forum and BiodivERsA joint call for research proposals, under BiodivScen ERA-Net COFUND programme, and with the funding organization the Academy of Finland (project numbers 329334 and 326534 to P.C.W., 329308, 335651 and 329332 to E.R.K., 268670 and 324605 to T.M.). Further support was provided by the Kvantum Institute at the University of Oulu.
Academy of Finland Grant Number: 326534
Detailed Information: 326534 (Academy of Finland Funding decision)
Copyright information: © 2022 The Authors. Journal of Animal Ecology © 2022 British Ecological Society. This is the peer reviewed version of the following article: Brila, I., Lavrinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T., & Watts, P. C. (2023). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole Myodes glareolus. Journal of Animal Ecology, 92, 826– 837, which has been published in final form at https://doi.org/10.1111/1365-2656.13869. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. This article may not be enhanced, enriched or otherwise transformed into a derivative work, without express permission from Wiley or by statutory rights under applicable legislation. Copyright notices must not be removed, obscured or modified. The article must be linked to Wiley’s version of record on Wiley Online Library and any embedding, framing or otherwise making available the article or pages thereof by third parties from platforms, services and websites other than Wiley Online Library must be prohibited.