Abstract
Wood is a highly intractable food source, yet many insects successfully colonize and thrive in this challenging niche. Overcoming the lignin barrier of wood is a key challenge in nutrient acquisition, but full depolymerization of intact lignin polymers has only been conclusively demonstrated in fungi and is not known to occur by enzymes produced by insects or bacteria. Previous research validated that lignocellulose and hemicellulose degradation occur within the gut of the wood boring insect, Anoplophora glabripennis (Asian longhorned beetle), and that a fungal species, Fusarium solani (ATCC MYA 4552), is consistently associated with the larval stage. While the nature of this relationship is unresolved, we sought to assess this fungal isolate's ability to degrade lignocellulose and cell wall polysaccharides and to extract nutrients from woody tissue. This gut-derived fungal isolate was inoculated onto a wood-based substrate and shotgun proteomics using Multidimensional Protein Identification Technology (MudPIT) was employed to identify 400 expressed proteins. Through this approach, we detected proteins responsible for plant cell wall polysaccharide degradation, including proteins belonging to 28 glycosyl hydrolase families and several cutinases, esterases, lipases, pectate lyases, and polysaccharide deacetylases. Proteinases with broad substrate specificities and ureases were observed, indicating that this isolate has the capability to digest plant cell wall proteins and recycle nitrogenous waste under periods of nutrient limitation. Additionally, several laccases, peroxidases, and enzymes involved in extracellular hydrogen peroxide production previously implicated in lignin depolymerization were detected. In vitro biochemical assays were conducted to corroborate MudPIT results and confirmed that cellulases, glycosyl hydrolases, xylanases, laccases, and Mn- independent peroxidases were active in culture; however, lignin- and Mn- dependent peroxidase activities were not detected While little is known about the role of filamentous fungi and their associations with insects, these findings suggest that this isolate has the endogenous potential to degrade lignocellulose and extract nutrients from woody tissue.
Highlights
Most beetles in the family Cerambycidae develop deep in woody tissues where access to sugar monomers present in plant cell wall polysaccharides is impeded by the presence of a recalcitrant lignin barrier and other essential nutritional resources, including proteins, lipids, sterols, and vitamins, are deficient or absent altogether [1]
Some evidence indicates that cell wall proteins present in xylem elements are cross-linked with lignin and other cell wall polysaccharides, protecting them from proteolysis, suggesting that lignocellulose and hemicellulose degradation may be required for protein acquisition [11]
We demonstrated that lignin, cellulose, and hemicellulose degradation occur in the guts of larval A. glabripennis [22,23,24]
Summary
Most beetles in the family Cerambycidae develop deep in woody tissues where access to sugar monomers present in plant cell wall polysaccharides is impeded by the presence of a recalcitrant lignin barrier and other essential nutritional resources, including proteins, lipids, sterols, and vitamins, are deficient or absent altogether [1]. The Asian longhorned beetle (Anoplophora glabripennis, Coleoptera: Cerambycidae), an exotic insect native to China first detected in the U.S in the early 1990’s, attacks both weakened [4] and healthy [5] deciduous trees in the absence of external wood-degrading fungi. This beetle enjoys a broad host range, which includes over 21 deciduous tree species [6,7]. Its lack of stereoregularity and periodicity and its condensed, insoluble properties make lignin resistant to most forms of enzymatic attack [13]
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