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

Year of publication

2023

Authors

Brila, Ilze; Lavrinienko, Anton; Tukalenko, Eugene; Kallio, Eva R.; Mappes, Tapio; Watts, Phillip C.

Abstract

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. 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. 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). 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. 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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Organizations and authors

University of Oulu

Brila Ilze

University of Jyväskylä

Kallio Eva Orcid -palvelun logo

Watts Phillip Orcid -palvelun logo

Mappes Tapio Orcid -palvelun logo

Lavrinienko Anton

Brila Ilze

Tukalenko Yevhen

Publication type

Publication format

Article

Parent publication type

Journal

Article type

Original article

Audience

Scientific

Peer-reviewed

Peer-Reviewed

MINEDU's publication type classification code

A1 Journal article (refereed), original research

Publication channel information

Volume

92

Issue

4

Pages

826-837

​Publication forum

59558

​Publication forum level

3

Open access

Open access in the publisher’s service

No

Self-archived

Yes

Other information

Fields of science

Ecology, evolutionary biology; Plant biology, microbiology, virology

Keywords

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Publication country

United Kingdom

Internationality of the publisher

International

Language

English

International co-publication

Yes

Co-publication with a company

No

DOI

10.1111/1365-2656.13869

The publication is included in the Ministry of Education and Culture’s Publication data collection

Yes