Comparative Genomic Analysis of the Endosymbionts of Herbivorous Insects Reveals Eco-Environmental Adaptations: Biotechnology Applications

摘要

Metagenome analysis of the gut symbionts of three different insects was conducted as a means of comparing taxonomic and metabolic diversity of gut microbiomes to diet and life history of the insect hosts. A second goal was the discovery of novel biocatalysts for biorefinery applications. Grasshopper and cutworm gut symbionts were sequenced and compared with the previously identified metagenome of termite gut microbiota. These insect hosts represent three different insect orders and specialize on different food types. The comparative analysis revealed dramatic differences among the three insect species in the abundance and taxonomic composition of the symbiont populations present in the gut. The composition and abundance of symbionts was correlated with their previously identified capacity to degrade and utilize the different types of food consumed by their hosts. The metabolic reconstruction revealed that the gut metabolome of cutworms and grasshoppers was more enriched for genes involved in carbohydrate metabolism and transport than wood-feeding termite, whereas the termite gut metabolome was enriched for glycosyl hydrolase (GH) enzymes relevant to lignocellulosic biomass degradation. Moreover, termite gut metabolome was more enriched with nitrogen fixation genes than those of grasshopper and cutworm gut, presumably due to the termite's adaptation to the high fiber and less nutritious food types. In order to evaluate and exploit the insect symbionts for biotechnology applications, we cloned and further characterized four biomass-degrading enzymes including one endoglucanase and one xylanase from both the grasshopper and cutworm gut symbionts. The results indicated that the grasshopper symbiont enzymes were generally more efficient in biomass degradation than the homologous enzymes from cutworm symbionts. Together, these results demonstrated a correlation between the composition and putative metabolic functionality of the gut microbiome and host diet, and suggested that this relationship could be exploited for the discovery of symbionts and biocatalysts useful for biorefinery applications. Author Summary The symbiotic gut microbiome of herbivorous insects is vital for their ability to utilize and specialize on plants with very different nutrient qualities. Moreover, the gut microbiome is a significant resource for the discovery of biocatalysts and microbes with applications to various biotechnologies. We compared the gut symbionts from three different insect species to examine whether there was a relationship between the diversity and metabolic capability of the symbionts and the diet of their hosts, with the goal of using such a relationship for the discovery of biocatalysts for biofuel applications. The study revealed that the metabolic capabilities of the insect gut symbionts correlated with insect adaptation to different food types and life histories at the levels of species, metabolic pathway, and individual gene. Moreover, we showed that the grasshopper cellulase and xylanase enzymes generally exhibited higher activities than those of cutworm, demonstrating differences in capabilities even at the protein level. Together, our findings confirmed our previous research and suggested that the grasshopper might be a good target for biocatalyst discovery due to their high gut cellulytic enzyme activities.