Experimental Infection of the Biomphalaria glabrata Vector Snail by Schistosoma mansoni Parasites Drives Snail Microbiota Dysbiosis.

Anaïs Portet,David Duval,Ana Lokmer,Benjamin Gourbal,Richard Galinier,Eve Toulza,Camille Huot

doi:10.3390/microorganisms9051084

Abstract

Host-parasite interaction can result in a strong alteration of the host-associated microbiota. This dysbiosis can affect the fitness of the host; can modify pathogen interaction and the outcome of diseases. Biomphalaria glabrata is the snail intermediate host of the trematode Schistosoma mansoni, the agent of human schistosomiasis, causing hundreds of thousands of deaths every year. Here, we present the first study of the snail bacterial microbiota in response to Schistosoma infection. We examined the interplay between B. glabrata, S. mansoni and host microbiota. Snails were infected and the microbiota composition was analysed by 16S rDNA amplicon sequencing approach. We demonstrated that the microbial composition of water did not affect the microbiota composition. Then, we characterised the Biomphalaria bacterial microbiota at the individual scale in both naive and infected snails. Sympatric and allopatric strains of parasites were used for infections and re-infections to analyse the modification or dysbiosis of snail microbiota in different host-parasite co-evolutionary contexts. Concomitantly, using RNAseq, we investigated the link between bacterial microbiota dysbiosis and snail anti-microbial peptide immune response. This work paves the way for a better understanding of snail/schistosome interaction and should have critical consequences in terms of snail control strategies for fighting schistosomiasis disease in the field.

Highlights

Published: 18 May 2021Biomphalaria glabrata is a freshwater snail (Lophotrochozoa, Planorbidae), living in inter-tropical regions of Latin America, in rivers, ponds, waterways and other freshwater environments
The water membranes of Planorbarius metdjensis and Bulinus truncatus were relatively separated from the water membranes of Biomphalaria snails and closer to their respective associated snail species (Figure S1B)
These results revealed that the bacterial communities of the water would tend to become more similar to the microbiota of the molluscs, potentially due to the faeces released by the snails in the water tanks

Summary

Introduction

Biomphalaria glabrata is a freshwater snail (Lophotrochozoa, Planorbidae), living in inter-tropical regions of Latin America, in rivers, ponds, waterways and other freshwater environments. B. glabrata snails have important medical and epidemiological impacts due to their role as the main intermediate host of Schistosoma mansoni (Lophotrochozoa, Platyhelminthes, Trematoda), the agent of intestinal schistosomiasis. The gonochoric Schistosoma adult parasites mate in the human host venous system. Female worms produce eggs that cross endothelial mesenteric vessels and intestinal epithelium to reach faeces and the aquatic environment. Eggs hatch and release miracidia, the free-living snail-infective parasite stage. At the following step of the life cycle, the miracidium needs to infect the freshwater snail B. glabrata. Intensive asexual multiplication in the snail tissues leads to the continuous production of hundreds of generations of cercariae, the free-living human-infective parasite stage

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Conclusion