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

Joshua S. Yuan,Peng Gao,Xin Zhou,Lantao Liu,Xueyan Chen,Nikos C. Kyrpides,Su Sun,Paul M. Richardson,Shangxian Xie,Weibing Shi,En-Gyu No

doi:10.1371/journal.pgen.1003131

Abstract

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.

Highlights

Insects represent one of the most diverse groups of organisms on the planet that can adapt to the extremely diverse ecoenvironments
Insect gut symbionts play an essential role in the insect adaptation to various food types and they have been shown to be important for lignocellulosic biomass degradation, nutrient production, compound detoxification, and environmental adaptation [2,3,4,5,6,7]
Disrupting insect gut symbionts can significantly reduce the fitness of insects and can even cause serious diseases such as CCD (Colony Collapse Disease) [8]

Summary

Introduction

Insects represent one of the most diverse groups of organisms on the planet that can adapt to the extremely diverse ecoenvironments. Insect gut symbionts were shown to be maternally inheritable from generation to generation, which suggests the symbiotic microbiota is a dynamic component of the competitive evolution between plants and herbivorous insects as well as a driving force for insect speciation [9,10]. For these reasons, insect gut symbionts have been the subject of extensive studies in recent years [10].

Author Summary

Findings

Materials and Methods