Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populations

Abstract

BackgroundDespite its central role in host fitness, the gut microbiota may differ greatly between individuals. This variability is often mediated by environmental or host factors such as diet, genetics, and infections. Recently, a particular attention has been given to the interactions between gut bacteriome and helminths, as these latter could affect host susceptibility to other infections. Further studies are still required to better understand the three-way interactions between gut bacteriome, helminths and other parasites, especially because previous findings have been very variable, even for comparable host-parasite systems.MethodsIn our study, we used the V4 region of the 16S rRNA gene to assess the variability of gut bacteriome diversity and composition in wild populations of a small mammal, the bank vole Myodes glareolus. Four sites were sampled at a fine geographical scale (100 km) along a North-South transect in Eastern France. We applied analyses and concepts of community and microbial ecology to evaluate the interactions between the gut bacteriome, the gastro-intestinal helminths and the pathogenic bacteria detected in the spleen.ResultsRegarding the gut bacteriome composition and diversity among bank voles, we identified important variations that were mainly explained by sampling localities and reflected the North/South sampling transect. In addition, we detected two main enterotypes, that might correspond to contrasted diets. We found geographic variations of the gut bacteriome richness and Firmicutes/Bacteroidetes ratio, both correlating positively with body mass index. We found positive correlations between the specific richness of the gut bacteriome and of the helminth community, as well as between the composition of these two communities, even when accounting for the influence of geographical distance. For the pathogenic bacteria community, no broad patterns have been detected. The helminths Aonchothecha murissylvatici, Heligmosomum mixtum and the bacteria Bartonella sp were the main taxa associated with the whole gut bacteriome composition. Besides, changes in relative abundance of particular gut bacteriome taxa were specifically associated with other helminths (Mastophorus muris, Catenotaenia henttoneni, Paranoplocephala omphaloides and Trichuris arvicolae) or pathogenic bacteria. Especially, infections with Neoehrlichia mikurensis, Orientia sp or Rickettsia sp were associated with lower relative abundance of the family Erysipelotrichaceae (Firmicutes), while coinfections with higher number of bacterial infections were associated with lower relative abundance of a Bacteroidales family (Bacteroidetes).ConclusionsThese results emphasize complex interlinkages between gut bacteriome and infections in wild animal populations. They remain difficult to generalize due to the strong impact of environment, even at fine geographical scales, on these interactions. Abiotic features, as well as small mammal community composition and within host parasite coinfections, should now be considered to better understand the spatial variations observed in the relationships between gut bacteriome, gastro-intestinal helminths and bacterial infections.