Integrative biology defines novel biomarkers of resistance to strongylid infection in horses

Abstract

The widespread failure of anthelmintic drugs against nematodes of veterinary interest requires novel control strategies. Selective treatment of the most susceptible individuals could reduce drug selection pressure but requires appropriate biomarkers of the intrinsic susceptibility potential. To date, this has been missing in livestock species. Here, we selected Welsh ponies with divergent intrinsic susceptibility (measured by their egg excretion levels) to cyathostomin infection and found that their divergence was sustained across a 10-year time window. Using this unique set of individuals, we monitored variations in their blood cell populations, plasma metabolites and faecal microbiota over a grazing season to isolate core differences between their respective responses under worm-free or natural infection conditions. Our analyses identified the concomitant rise in plasma phenylalanine level and faecal Prevotella abundance and the reduction in circulating monocyte counts as biomarkers of the need for drug treatment (egg excretion above 200 eggs/g). This biological signal was replicated in other independent populations. We also unravelled an immunometabolic network encompassing plasma beta-hydroxybutyrate level, short-chain fatty acid producing bacteria and circulating neutrophils that forms the discriminant baseline between susceptible and resistant individuals. Altogether our observations open new perspectives on the susceptibility of equids to strongylid infection and leave scope for both new biomarkers of infection and nutritional intervention.

Variations in the fecal microbiota and their functions of Thoroughbred, Mongolian, and Hybrid horses

“…The above bacteria can produce SCFAs by fermenting the dietary fiber. It is well known that SCFAs can not only provide energy for the intestinal epithelial cells but also firmly maintain the morphology and function of the intestine ( 37 , 38 ). Moreover, SCFAs have also been confirmed to promote glucose intake and metabolism in skeletal muscle, and butyrate can improve the energy metabolism efficiency of muscle fibers ( 39 , 40 ).…”

Comparing the effects of horse grazing alone or with cattle on horse parasitism and vegetation use in a mesophile pasture

“…Cattle, by avoiding the reproductive and dead herbage areas as did horses, also did not improve herbage quality nor the digestibility of the horses' diet. We could also not evidence any reduction of parasite egg excretion in horses grazing with cattle although recorded excretion levels were in a higher range of values ‐ thereby ensuring a fair comparison between the two management systems ‐ and matched the expected seasonal variation under temperate area (Salle et al, 2021; Wood et al, 2012). In this study, 40% of the horse faeces were recorded in the reproductive and dead herbage areas which were avoided by the cattle.…”

Patterns of variation in equine strongyle community structure across age groups and gut compartments

“…the ability for damage control upon infection [ 41 ], higher FEC would be found in individuals able to cope with the presence of a fecund population. Such tolerance would be compatible with the mild modifications found in the blood of the infected host [ 42 , 43 ] or in their gut microbiota whose stable state is not altered in the presence of significant egg excretion [ 43 ]. In this tolerance framework, the host would exert limited effects on the parasite community and, in turn, putative dilution effects of the most fecund parasites in more diverse parasite communities could contribute to obscure the relationship between observed FEC and parasite diversity.…”