Metagenomic Analysis of the Microbiota from the Crop of an Invasive Snail Reveals a Rich Reservoir of Novel Genes

Abstract

The shortage of petroleum reserves and the increase in CO2 emissions have raised global concerns and highlighted the importance of adopting sustainable energy sources. Second-generation ethanol made from lignocellulosic materials is considered to be one of the most promising fuels for vehicles. The giant snail Achatina fulica is an agricultural pest whose biotechnological potential has been largely untested. Here, the composition of the microbial population within the crop of this invasive land snail, as well as key genes involved in various biochemical pathways, have been explored for the first time. In a high-throughput approach, 318 Mbp of 454-Titanium shotgun metagenomic sequencing data were obtained. The predominant bacterial phylum found was Proteobacteria, followed by Bacteroidetes and Firmicutes. Viruses, Fungi, and Archaea were present to lesser extents. The functional analysis reveals a variety of microbial genes that could assist the host in the degradation of recalcitrant lignocellulose, detoxification of xenobiotics, and synthesis of essential amino acids and vitamins, contributing to the adaptability and wide-ranging diet of this snail. More than 2,700 genes encoding glycoside hydrolase (GH) domains and carbohydrate-binding modules were detected. When we compared GH profiles, we found an abundance of sequences coding for oligosaccharide-degrading enzymes (36%), very similar to those from wallabies and giant pandas, as well as many novel cellulase and hemicellulase coding sequences, which points to this model as a remarkable potential source of enzymes for the biofuel industry. Furthermore, this work is a major step toward the understanding of the unique genetic profile of the land snail holobiont.

Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

“…At least one shipworm species (Lyrodus pedicellatus) has been shown to grow and reproduce normally using wood as its sole particulate food source (3). However, unlike their terrestrial herbivorous and xylophagous counterparts, whose digestive systems contain complex communities of microbes (4)(5)(6)(7)(8)(9), Bankia setacea and several other shipworm species accumulate and digest wood in the cecum ( Fig. 1 A and B), a region of the foregut that is devoid of any conspicuous microbial community (10).…”

Biochemical Characterization of Streptomyces sp. I1.2 Secretome Reveals the Presence of Multienzymatic Complexes Containing Cellulases and Accessory Enzymes

“…In addition to their endo-genous enzymatic repertoire, recent studies revealed that land snails contain a complex and adaptable microbiota that potentially accounts for their great digestive efficiency [17,53,54]. In addition, a metagenomic analysis of A. fulica crop-resident microbiota identified a great number of sequences coding for biomass-degrading enzymes (36 %), including cellulases and hemicellulases [45]. Here, we have shown that Streptomyces sp.…”

“…I1.2 is potentially an important representative of A. fulica microbiota that specifically contributes to nutrient acquisition during lignocellulose deconstruction through the secretion of complexed cellulases into the gastrointestinal lumen, which may provide complementary roles to noncomplexed endo-genous enzymes, such as distinct substrate preferences, kinetics, and/or higher hydrolysis rates. The importance of these complexed cellulase systems is highlighted by the fact that no cohesin or dockerin modules were detected in the contents of crop fluids [45], suggesting that the noncellulosomic multienzymatic complexes detected in this study represent a novel and alternative form of cellulolytic multienzyme complex organization, which is crucial for nutrient uptake in A. fulica.…”

“…The land snail A. fulica is considered the most destructive gastropod worldwide, mainly due to its capacity to efficiently process high amounts of lignocellulosic biomass [43,44]. Achatina fulica digestive juice is found in large quantities filling in its gastrointestinal tract, specially the crop [45]. Although the cellulases found in the digestive juice of A. fulica are only poorly studied [46,47], some activities are well identified in other terrestrial gastropods.…”

Identification of glycosyl hydrolases from a metagenomic library of microflora in sugarcane bagasse collection site and their cooperative action on cellulose degradation

“…Bacteroidetes is a major bacterial group in many lignocellulose degrading environments, such as the crop of an invasive snail (36), and in the bagasse collection site, as shown by direct shotgun pyrosequencing (15). A recent study of genes encoding proteins related to cellulose utilization among 5123 sequenced bacterial genomes revealed that Bacteroidetes are highly represented as potent cellulose degraders in various environments (37).…”