TitleA longitudinal assessment of host-microbe-parasite interactions resolves the zebrafish gut microbiome's link to Pseudocapillaria tomentosa infection and pathology.
Publication TypeJournal Article
Year of Publication2019
AuthorsGaulke, CA, Martins, ML, Watral, VG, Humphreys, IR, Spagnoli, ST, Kent, ML, Sharpton, TJ
JournalMicrobiome
Volume7
Issue1
Pagination10
Date Published2019 Jan 24
ISSN2049-2618
Abstract

BACKGROUND: Helminth 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.

RESULTS: To 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.

CONCLUSIONS: These 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.

DOI10.1186/s40168-019-0622-9
Alternate JournalMicrobiome
PubMed ID30678738
PubMed Central IDPMC6346533
Grant List1557192 / / National Science Foundation /
R21 AI135641 / AI / NIAID NIH HHS / United States
R21 AI135641 / / National Institute of Allergy and Infectious Diseases /
R24 OD010998 / / National Institutes of Health /
CNPq 202030/2014-8 / / Conselho Nacional de Desenvolvimento Científico e Tecnológico /
P30 ES000210 / / National Institute of Environmental Health Sciences /
R24 OD010998 / OD / NIH HHS / United States
P30 ES000210 / ES / NIEHS NIH HHS / United States