Abstract
BackgroundHelminth parasites represent a significant threat to the health of human and animal populations, and there is a growing need for tools to treat, diagnose, and prevent these infections. Recent work has turned to the gut microbiome as a utilitarian agent in this regard; components of the microbiome may interact with parasites to influence their success in the gut, meaning that the microbiome may encode new anthelmintic drugs. Moreover, parasite infections may restructure the microbiome’s composition in consistent ways, implying that the microbiome may be useful for diagnosing infection. The innovation of these utilities requires foundational knowledge about how parasitic infection, as well as its ultimate success in the gut and impact on the host, relates to the gut microbiome. In particular, we currently possess limited insight into how the microbiome, host pathology, and parasite burden covary during infection. Identifying interactions between these parameters may uncover novel putative methods of disrupting parasite success.ResultsTo identify interactions between parasite success and the microbiome, we quantified longitudinal associations between an intestinal helminth of zebrafish, Pseudocapillaria tomentosa, and the gut microbiome in 210 4-month-old 5D line zebrafish. Parasite burden and parasite-associated pathology varied in severity throughout the experiment in parasite-exposed fish, with intestinal pathologic changes becoming severe at late time points. Parasite exposure, burden, and intestinal lesions were correlated with gut microbial diversity. Robust generalized linear regression identified several individual taxa whose abundance predicted parasite burden, suggesting that gut microbiota may influence P. tomentosa success. Numerous associations between taxon abundance, burden, and gut pathologic changes were also observed, indicating that the magnitude of microbiome disruption during infection varies with infection severity. Finally, a random forest classifier accurately predicted a fish’s exposure to the parasite based on the abundance of gut phylotypes, which underscores the potential for using the gut microbiome to diagnose intestinal parasite infection.ConclusionsThese experiments demonstrate that P. tomentosa infection disrupts zebrafish gut microbiome composition and identifies potential interactions between the gut microbiota and parasite success. The microbiome may also provide a diagnostic that would enable non-destructive passive sampling for P. tomentosa and other intestinal pathogens in zebrafish facilities.
Highlights
Intestinal helminth infections present a major global health concern [1, 2]
P. tomentosa infection induces progressive weight loss and gut lesions To quantify the impact of P. tomentosa infection in zebrafish, we followed the progressive impacts of the infection on parasite burden, weight loss, and gut pathology in 105 exposed and 105 unexposed fish
By applying robust regression approaches, we identified associations between parasite burden, infection associated pathologies, and host gut microbiome composition, which suggests that microbiome taxa might inhibit or enhance parasite success in the gut
Summary
Intestinal helminth infections present a major global health concern [1, 2]. Over one billion people suffer helminth infections [1, 2], which often manifest developmental, cognitive, nutritional, and gastrointestinal defects [3,4,5]. While safe and effective drugs can treat helminth infection, the rapid rise of anthelmintic drug resistance [6] necessitates development of new strategies for parasite control Hope for such strategies springs from the observation that parasite-associated morbidity unevenly distributes across populations [5], which indicates that personalized factors impact infection outcome [7,8,9]. The extent to which microbiome composition or diversity associates with parasite burden and intestinal pathology across the length of infection remains unclear Understanding these dynamics will enhance our ability to resolve specific microbial taxa that may influence or respond to parasite exposure and identify putative microbial therapeutics and diagnostics. We currently possess limited insight into how the microbiome, host pathology, and parasite burden covary during infection Identifying interactions between these parameters may uncover novel putative methods of disrupting parasite success
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