Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood.

Geoffrey N Gobert,Malcolm K Jones,Kosala G Weerakoon,Christopher J Creevey,Jack Carson,Hong You,Geoff Mcmullan,Sujeevi S K Nawaratna,Donald P Mcmanus,Josué De Moraes

doi:10.1371/journal.pone.0263188

Abstract

BackgroundSchistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, both of which interact with the host during immune evasion and in nutrient uptake.MethodsFemale ARC Swiss mice (4–6 weeks old) were infected percutaneously with Schistosoma japonicum cercariae freshly shed from Oncomelania hupensis quadrasi snails (Philippines strain). Fluorescent in situ hybridisation (FISH) was performed by using fresh adult S. japonicum perfused from those infected mice. Adult S. japonicum worms were processed to isolate the tegument from the carcass containing the gastrodermis; blood and bile were collected individually from infected and uninfected mice. Total DNA extracted from all those samples were used for microbiome profiling.ResultsFISH and microbiome profiling showed the presence of bacterial populations on two epithelial surfaces of adult worms, suggesting they were distinct not only from the host blood but also from each other. Whereas microbial diversity was reduced overall in the parasite epithelial tissues when compared with that of host blood, specific bacterial taxa, including Anoxybacillus and Escherichia, were elevated on the tegument. Minimal differences were evident in the microbiome of host blood during an active infection, compared with that of control uninfected blood. However, sampling of bile from infected animals identified some differences compared with controls, including elevated levels of Limnohabitans, Clostridium and Curvibacter.ConclusionsUsing FISH and microbial profiling, we were able to demonstrate, for the first time, that bacteria are presented on the epithelial surfaces of adult schistosomes. These schistosome surface-associated bacteria, which are distinct from the host blood microenvironment, should be considered as a new and important component of the host-schistosome interaction. The importance of individual bacterial species in relation to schistosome parasitism needs further elucidation.

Highlights

Helminth parasites cause significant chronic disease both in people and in animals of economic importance
Fluorescent in situ hybridisation (FISH) and microbiome profiling showed the presence of bacterial populations on two epithelial surfaces of adult worms, suggesting they were distinct from the host blood and from each other
Using FISH and microbial profiling, we were able to demonstrate, for the first time, that bacteria are presented on the epithelial surfaces of adult schistosomes

Summary

Introduction

Helminth parasites cause significant chronic disease both in people and in animals of economic importance. The schistosomes are dioecious and cause significant hepatic immunopathology to their mammalian hosts as a result of fibrotic granulomata produced as the host response to entrapped parasite eggs laid by the paired adult worms [2]. Schistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, both of which interact with the host during immune evasion and in nutrient uptake

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Discussion

Conclusion