Abstract
Some eukaryotes are able to gain access to well-protected carbon sources in plant biomass by exploiting microorganisms in the environment or harbored in their digestive system. One is the land pulmonate Arion ater, which takes advantage of a gut microbial consortium that can break down the widely available, but difficult to digest, carbohydrate polymers in lignocellulose, enabling them to digest a broad range of fresh and partially degraded plant material efficiently. This ability is considered one of the major factors that have enabled A. ater to become one of the most widespread plant pest species in Western Europe and North America. Using metagenomic techniques we have characterized the bacterial diversity and functional capability of the gut microbiome of this notorious agricultural pest. Analysis of gut metagenomic community sequences identified abundant populations of known lignocellulose-degrading bacteria, along with well-characterized bacterial plant pathogens. This also revealed a repertoire of more than 3,383 carbohydrate active enzymes (CAZymes) including multiple enzymes associated with lignin degradation, demonstrating a microbial consortium capable of degradation of all components of lignocellulose. This would allow A. ater to make extensive use of plant biomass as a source of nutrients through exploitation of the enzymatic capabilities of the gut microbial consortia. From this metagenome assembly we also demonstrate the successful amplification of multiple predicted gene sequences from metagenomic DNA subjected to whole genome amplification and expression of functional proteins, facilitating the low cost acquisition and biochemical testing of the many thousands of novel genes identified in metagenomics studies. These findings demonstrate the importance of studying Gastropod microbial communities. Firstly, with respect to understanding links between feeding and evolutionary success and, secondly, as sources of novel enzymes with biotechnological potential, such as, CAZYmes that could be used in the production of biofuel.
Highlights
Slugs are a highly successful group of organisms that are members of the order Pulmonata, found in high abundance in many terrestrial and aquatic ecosystems worldwide
In a previous study we demonstrated that the gut microbial consortium of A. ater is directly involved in breakdown of the lignocellulose portion of its diet (Joynson et al, 2014), while showing that this enzymatic activity is stable at a broad range of temperatures and pH levels
Relative abundance of microbial groups was assessed using MetaPhlAn. This analysis indicated that the majority of the gut microbial community corresponded to members of the Gammaproteobacteria class (82%) with most assignments being to members of the Enterobacteriaceae (64.5%) and Pseudomonadaceae (10.6%) families, which both contain widespread environmentally-adapted bacteria
Summary
Slugs are a highly successful group of organisms that are members of the order Pulmonata, found in high abundance in many terrestrial and aquatic ecosystems worldwide. The common black slug, Arion ater, is prevalent in Western Europe and North America These slugs travel long distances at night feeding on a variety of foodstuffs including vegetation (both live and decaying), carrion, and fungi. They use a tonguelike appendage containing barb-like teeth—the radula—to shred their food into uniformly sized pieces, increasing the surface area for enzymatic degradation in the gut. These slugs feed actively down to temperatures approaching 0◦C, and adults and eggs have been observed to survive freezing at −3◦C for 3 days or more (Slotsbo et al, 2011). The ability to utilize a broad range of food sources and their physiological robustness to environmental challenges are amongst the reasons why slugs are such a successful group of organisms, despite the best efforts of humans to eradicate them from agricultural and suburban land
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