Metagenomic signature of natural strongyle infection in susceptible and resistant horses

Abstract

Gastrointestinal strongyles are a major threat to horses' health and welfare. Given that strongyles inhabit the same niche as the gut microbiota, they may interact with each other. These beneficial or detrimental interactions are unknown in horses and could partly explain contrasted susceptibility to infection between individuals. To address these questions, an experimental pasture trial with 20 worm-free female Welsh ponies (10 susceptible (S) and 10 resistant (R) to parasite infection) was implemented for five months. Fecal egg counts (FEC), hematological and biochemical data, body weight and gut microbiota composition were studied in each individual after 0, 24, 43, 92 and 132 grazing days.

The predicted R ponies exhibited lower FEC after 92 and 132 grazing days, and showed higher levels of circulating monocytes and eosinophils, while S ponies developed lymphocytosis by the end of the trial. Although the overall microbiota diversity remained similar between the two groups, R and S ponies exhibited sustained differential abundances in Clostridium XIVa, Ruminococcus, Acetivibrio and unclassified Lachnospiracea at day 0. These bacteria may hence contribute to the intrinsic pony resistance towards strongyle infection. Moreover, Paludibacter, Campylobacter, Bacillus, Pseudomonas, Clostridium III, Acetivibrio, members of the unclassified Eubacteriaceae and Ruminococcaceae and fungi loads were increased in infected S ponies, suggesting that strongyle and fungi may contribute to each other’s success in the ecological niche of the equine intestines. In contrast, butyrate-producing bacteria such as Ruminococcus, Clostridium XIVa and members of the Lachnospiraceae family decreased in S relative to R ponies. Additionally, these gut microbiota alterations induced changes in several immunological pathways in S ponies, including pathogen sensing, lipid metabolism, and activation of signal transduction that are critical for the regulation of immune system and energy homeostasis. These observations shed light on a putative implication of the gut microbiota in the intrinsic resistance to strongyle infection.

Overall, this longitudinal study provides a foundation to better understand the mechanisms that underpin the relationship between host susceptibility to strongyle infection, immune response and gut microbiota under natural conditions in horses and should contribute to the development of novel biomarkers of strongyle susceptibility and provide additional control options.