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

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.

Immunogenetic-pathogen networks shrink in Tome’s spiny rat, a generalist rodent inhabiting disturbed landscapes

“…Co-infections remain an underappreciated issue of wildlife and disease ecology 82 , 83 . Immune suppression by nematodes can, for instance, facilitate tuberculosis infections in African buffalo ( Syncerus caffer 84 ), a reduction of parasite-specific IgA antibodies following co-infection with multiple intestinal parasites increases parasite burden in wild wood mice ( Apodemus sylvaticus 85 ), and concurrent bacterial and viral infections shape the gut microbial diversity in bank voles ( Myodes glareolus 86 ). With respect to our data, our findings paint the picture of more complex host-parasite interactions in undisturbed, protected (though fragmented in the case of islands) landscapes without contact with humans and domestic animals.…”

Field survey and molecular characterization of apicomplexan parasites in small mammals from military camps in Afghanistan

“…Co-infections with different parasites not only in vectors but also in their hosts can be classified as a naturally occurring phenomenon (Rizzoli et al 2004 ; Broker 2012 ). Moreover, there is increasing evidence for co-infections of different agents, e.g., endoparasites and viruses or bacteria and viruses, or multiple co-infections (Telfer et al 2010 ; Salvador et al 2011 ; Guivier et al 2014 ; Schmidt et al 2014 ; Madrières et al 2019 ; Jeske et al 2021 ; Brila et al 2022 ; Schlohsarczyk et al 2023 ). Such co-infections might be important in several ways.…”

“…On the opposite, the infection with one infectious agent might decrease the susceptibility to get infected by another one. In addition, the immune status that is modulated by the microbiome might influence the susceptibility or outcome of an infection by a pathogen; or vice versa, the systemic infection with a pathogen may influence the gut microbiome in structure and functionality (Brila et al 2022 ). Nevertheless, this study corroborates current knowledge that infections with multiple pathogens are a rather normal phenomenon.…”

Co‐infections mask pathogen‐specific associations with the gut microbiota in wild voles

“…In their recent publication in the Journal of Animal Ecology , Brila et al (2022) investigate associations between co‐infecting pathogens and commensal gut microbes in wild bank voles Myodes glareolus . The authors pair surveillance data on four systemic pathogenic microbes (two bacterial, one protozoan, and one viral) with faecal microbiota profiling (Figure 1a).…”