Larvae of longhorned beetles (Coleoptera; Cerambycidae) have evolved a diverse and phylogenetically conserved array of plant cell wall degrading enzymes

Abstract

Longhorned beetles (Cerambycidae) are the most diverse group of predominantly wood‐feeding (xylophagous) insects on Earth. Larvae of most species feed within tissues of plants made up of large amounts of plant cell wall (PCW), which is notoriously difficult to digest. To efficiently access nutrients from their food source, cerambycid larvae have to deconstruct PCW polysaccharides – such as cellulose, hemicelluloses and pectin – requiring them to possess a diversity of plant cell wall degrading enzymes (PCWDEs) in their digestive tract. Genomic data for Cerambycidae are mostly limited to notorious forest pests and are lacking for most of the taxonomic groups. Consequently, our understanding of the distribution and evolution of cerambycid PCWDEs is quite limited. We addressed the numbers, kinds and evolution of cerambycid PCWDEs by surveying larval midgut transcriptomes from 23 species representing six of the eight recognized subfamilies of Cerambycidae and each with very diverse host types (i.e., gymnosperms, angiosperms, xylem, phloem, fresh or dead plant tissues). Using these data, we identified 340 new putative PCWDEs belonging to ten carbohydrate active enzyme families, including two gene families (GH7 and GH53) not previously reported from insects. The remarkably wide range of PCWDEs expressed by Cerambycidae should allow them to break down most PCW polysaccharides. Moreover, the observed distribution of PCWDEs encoded in cerambycid genomes agreed more with phylogenetic relationship of the species studied than with the taxonomic origin or quality of the host plant tissues.

Cuticle supplementation and nitrogen recycling by a dual bacterial symbiosis in a family of xylophagous beetles (Coleoptera: Bostrichidae)

“…Additionally, we generated a second (codon-based) nucleotide alignment based on Benchmarking Universal Single-Copy Orthologs (BUSCO) using a custom pipeline (Waterhouse et al, 2018) to extract the genes from the metagenome datasets. BUSCO analysis was performed for each dataset using the insecta_odb10 database (1,658 genes) to extract BUSCO genes that were found across all species (Shin et al, 2021). The corresponding nucleotide sequences were then extracted and aligned with MAFFT (Katoh & Standley, 2013) with --auto and default options.…”

Genome sequencing provides insights into the evolution of gene families encoding plant cell wall‐degrading enzymes in longhorned beetles

“…We previously investigated the structure of GH5_8-encoding genes in the two highly fragmented draft genomes of Phymatodes lengi and X. colonus (Shin et al, 2021). Their structure comprises two exons and a single intron with a conserved position and phase between gh5_8…”

“…In addition, the fact that all the PCWDE-encoding genes we previously identified in the gut transcriptomes of the corresponding species (Shin et al, 2021) were present in these draft genomes, provided extra evidence that we could use these assemblies for subsequent analyses. On the one hand, we recognise that the suitability of our assemblies for analyses dealing with chromosome synteny and whole genome comparisons is limited.…”

“…Cerambycinae (McKenna et al, 2019;Shin et al, 2021), we identified new families of PCWDEs, such as GH5_8, GH43_26, GH53, and GH7, none of which were present in previous transcriptome analyses (Pauchet et al, 2014;Scully et al, 2013) or in the reference genome of A. glabripennis (McKenna et al, 2016). Using phylogenetic analyses, we hypothesized that these genes were acquired from various microbial donors through several independent HGT events (Shin et al, 2021). Here, we confirmed their integration into the Cerambycidae genomes in regions containing known insect-derived genes and showed that the genes acquired introns after their original integration.…”

Dynamic changes of gut bacterial communities present in larvae of Anoplophora glabripennies collected at different developmental stages

“…Wood‐boring beetles live on nutritional imbalanced diet with low nitrogen environments (0.03%−0.1% nitrogen) (Mattson, 1980). The majority of the woody tissue is plant cell wall, mostly polysaccharides, including lignin, cellulose, hemicellulose, and pectin (Shin et al, 2021). Wood‐feeding insects thus have evolved a variety of survival strategies to liberate carbohydrates from intractable plant tissues to overcome extreme nutritional obstacles (Ayayee et al, 2014; Mattson, 1980).…”