Metabolic and immunological effects of gut microbiota in leaf beetles at the local and systemic levels

Abstract

Insects' intestinal microbes have profound effects on the host's physiological traits, which can impact their physiology at both the local (gut) and systemic (body) levels. Nevertheless, the molecular mechanisms underlying host-microbiota interactions, especially in non-model insects, remain elusive. Recently, tissue-specific transcriptomic analysis has been highlighted as a robust tool in studying host-microbe interactions. Plagiodera versicolora is a worldwide leaf-eating pest that primarily feeds on willows and poplar. The interplay between gut microflora and this host beetle has yet to be studied. Herein, we investigate the effects of the gut microbiota on the body mass of P. versicolora larvae, compare the nutrition status of larvae in absence and presence of gut microbiota, and profile gut bacterial loads throughout its developmental larval stages. We then perform comparative transcriptomic analysis of gut and body tissues in axenic and non-axenic larvae. Finally, we confirm the expression patterns of representative genes in nutritional metabolism and immunity. Results show that weight growth is retarded in conventional larvae, with a concomitant increase of total bacterial load by the 5^th development day, and germ-free larvae have a higher glucose content than conventional-reared larvae. Both nutritional and immunological analyses indicate that gut bacteria are a burden in the beetle's larval development. These findings elucidate the impacts of gut microbiota on P. versicolora, and provide insight into tissue-specific responses to gut microflora in this pest at the genetic level, boosting our understanding of the molecular mechanisms underlying host-microbe interactions in leaf beetles and beyond.

Keywords: Plagiodera versicolora; RNA-seq; gut bacteria; insect immunity; nutritional metabolism.