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

• Published in: The Journal of animal ecology 2023-04, Vol.92 (4), p.826-837
• Main Authors: Brila, Ilze, Lavrinienko, Anton, Tukalenko, Eugene, Kallio, Eva R., Mappes, Tapio, Watts, Phillip C.
• Format: Article
• Language: English
• Subjects: Animals; Apicomplexa; Arvicolinae - microbiology; Arvicolinae - parasitology; Bacteria; Borrelia burgdorferi; coinfection; Coinfection - veterinary; disease ecology; Gastrointestinal Microbiome; gut microbiota; Hantavirus; host–pathogen interactions; Infections; Intestinal microflora; Ixodes - microbiology; Microbiota; Myodes glareolus; Pathogens; Protozoa; Puumala orthohantavirus; Rodent Diseases - microbiology; Rodentia; virus; Wild animals
• ISSN: 0021-8790; 1365-2656
• DOI: 10.1111/1365-2656.13869

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. The authors show that four systemic pathogens can associate with changes in the gut microbiota of their rodent host. Crucially, these changes are affected by coinfection in a pathogen‐specific way; thus, ignoring possible coinfections can lead to erroneous conclusions about pathogen–microbiota associations.