Abstract
The Asian longhorned beetle ( Anoplophoraglabripennis ) is an invasive, wood-boring pest that thrives in the heartwood of deciduous tree species. A large impediment faced by A . glabripennis as it feeds on woody tissue is lignin, a highly recalcitrant biopolymer that reduces access to sugars and other nutrients locked in cellulose and hemicellulose. We previously demonstrated that lignin, cellulose, and hemicellulose are actively deconstructed in the beetle gut and that the gut harbors an assemblage of microbes hypothesized to make significant contributions to these processes. While lignin degrading mechanisms have been well characterized in pure cultures of white rot basidiomycetes, little is known about such processes in microbial communities associated with wood-feeding insects. The goals of this study were to develop a taxonomic and functional profile of a gut community derived from an invasive population of larval A . glabripennis collected from infested host trees and to identify genes that could be relevant for the digestion of woody tissue and nutrient acquisition. To accomplish this goal, we taxonomically and functionally characterized the A . glabripennis midgut microbiota through amplicon and shotgun metagenome sequencing and conducted a large-scale comparison with the metagenomes from a variety of other herbivore-associated communities. This analysis distinguished the A. glabripennis larval gut metagenome from the gut communities of other herbivores, including previously sequenced termite hindgut metagenomes. Genes encoding enzymes were identified in the A . glabripennis gut metagenome that could have key roles in woody tissue digestion including candidate lignin degrading genes (laccases, dye-decolorizing peroxidases, novel peroxidases and β-etherases), 36 families of glycoside hydrolases (such as cellulases and xylanases), and genes that could facilitate nutrient recovery, essential nutrient synthesis, and detoxification. This community could serve as a reservoir of novel enzymes to enhance industrial cellulosic biofuels production or targets for novel control methods for this invasive and highly destructive insect.
Highlights
Cellulose and hemicellulose represent some of the most abundant, renewable carbohydrate resources on the planet, comprising the largest natural source of fermentable sugars, which could be utilized for ethanolic biofuel production [1]
operational taxonomic units (OTUs) taxonomic classification with Ribosomal Database Project (RDP) classifier detected the presence of 166 OTUs in seven bacterial phyla in the midgut community including Actinobacteria (30 OTUs), Bacteroidetes (29 OTUs), Chlamydiae (1 OTU), Firmicutes (14 OTUs), Proteobacteria (80 OTUs), candidate phylum TM7 (3 OTUs), and Verrucomicrobia (5 OTUs), while four OTUs could not be conclusively assigned to any previously-characterized bacterial phyla
The single most-prevalent OTU, which comprised over 21% of the bacterial amplicons, was a member of the family Leuconostocaceae that could not be classified to genus level by RDP
Summary
Cellulose and hemicellulose represent some of the most abundant, renewable carbohydrate resources on the planet, comprising the largest natural source of fermentable sugars, which could be utilized for ethanolic biofuel production [1]. Despite the abundance of these polysaccharides, a major impediment to accessing fermentable sugars from these carbohydrates for large-scale industrial ethanol production is the presence of lignin [2], a stereotypically irregular, aromatic biopolymer comprised of phenylpropanoid aryl alcohol subunits and articulated by over 12 types of chemical bonds [3]. Wood-feeding insects, in collaboration with their gut microbial communities, have the capacity to produce enzymes that facilitate the degradation of lignocellulosic material [4,5]. These microbial communities constitute unique ecosystems that may serve as reservoirs of novel proteins and enzymes that could be exploited to enhance the efficiency of industrial biomass pre-treatment processes, decoupling lignin from wood polysaccharides and facilitating access to fermentable sugars in cellulose and hemicellulose. The assemblage of microbes associated with the A. glabripennis midgut represents an excellent candidate for mining novel lignocellulose degrading enzymes for biofuel applications
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