Abstract

Due to its wide distribution across the world, the snail Radix auricularia plays a central role in the transferal of energy and biomass by consuming plant biomass in freshwater systems. The gut microbiota are involved in the nutrition, digestion, immunity, and development of snails, particularly for cellulolytic bacteria, which greatly contribute to the digestion of plant fiber. For the first time, this study characterized the gut bacterial communities of R. auricularia, as well as predicted functions, using the Illumina Miseq platform to sequence 16S rRNA amplicons. Both juvenile snails (JS) and adult snails (AS) were sampled. The obtained 251,072 sequences were rarefied to 214,584 sequences and clustered into 1,196 operational taxonomic units (OTUs) with 97% sequence identity. The predominant phyla were Proteobacteria (JS: 36.0%, AS: 31.6%) and Cyanobacteria (JS: 16.3%, AS: 19.5%), followed by Chloroflexi (JS: 9.7%, AS: 13.1%), Firmicutes (JS: 14.4%, AS: 6.7%), Actinobacteria (JS: 8.2%, AS: 12.6%), and Tenericutes (JS: 7.3%, AS: 6.2%). The phylum Cyanobacteria may have originated from the plant diet instead of the gut microbiome. A total of 52 bacterial families and 55 genera were found with >1% abundance in at least one sample. A large number of species could not be successfully identified, which could indicate the detection of novel ribotypes or result from insufficient availability of snail microbiome data. The core microbiome consisted of 469 OTUs, representing 88.4% of all sequences. Furthermore, the predicted function of bacterial community of R. auricularia performed by Phylogenetic Investigation of Communities by Reconstruction of Unobserved States suggests that functions related to metabolism and environmental information processing were enriched. The abundance of carbohydrate suggests a strong capability of the gut microbiome to digest lignin. Our results indicate an abundance of bacteria in both JS and AS, and thus the bacteria in R. auricularia gut form a promising source for novel enzymes, such as cellulolytic enzymes, that may be useful for biofuel production. Furthermore, searching for xenobiotic biodegradation bacteria may be a further important application of these snails.

Highlights

  • Radix auricularia (Linnaeus, 1758), a pulmonate snail, is naturally distributed in freshwater systems across both Europe and Asia (Stift et al, 2004; Vasileva, 2012)

  • Using unweighted PCoA plot, samples were clustered according to their growth stage (JS and adult snails (AS) clusters), indicating that the developmental stage may have an effect on gut bacterial community

  • We used the high-throughput sequencing technique to investigate the bacterial diversity of individuals of the snail R. auricularia and predicted metagenomic functions using PICRUSt

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Summary

Introduction

Radix auricularia (Linnaeus, 1758), a pulmonate snail, is naturally distributed in freshwater systems across both Europe and Asia (Stift et al, 2004; Vasileva, 2012). Snails are common in freshwater systems, and both their energy and biomass can be transferred to fish, turtles, water birds, and mammals (Dewitt, Sih & Hucko, 1999; Eckblad, 1976) In addition to their role in the ecosystem, R. auricularia are intermediate hosts for many parasites (e.g., flukes), which are harmful to cattle, birds, and humans (Soldánová et al, 2010; Bargues et al, 2001). The capacity of decomposing lignocellulosic or pectic biomass increases their ability to utilize a variety of plant biomass, such as algae, water weeds, and leaf litters (Schamp, Horsák & Hájek, 2010; Vasileva, 2012) Beyond their own digestive enzymes, snails utilize vast amounts of additional enzymes, secreted by bacterial activity within their gut, which assists in the digestion of up to 60–80% of the consumed plant fiber (Charrier et al, 2006). The currently available knowledge of the bacterial communities of the snail gut is limited

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