Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle

Abstract

While genome erosion is extensively studied in intracellular symbionts, the metabolic implications of reductive evolution in microbes subsisting extracellularly remain poorly understood. Stammera capleta—an extracellular symbiont in leaf beetles—possesses an extremely reduced genome (0.27 Mb), enabling the study of drastic reductive evolution in the absence of intracellularity. Here, we outline the genomic and transcriptomic profiles of Stammera and its host to elucidate host-symbiont metabolic interactions. Given the symbiont’s substantial demands for nutrients and membrane components, the host’s symbiotic organ shows repurposing of internal resources by upregulating nutrient transporters and cuticle-processing genes targeting epithelial chitin. Facilitated by this supplementation and its localization, Stammera exhibits a highly streamlined gene expression profile and a fermentation pathway for energy conversion, sharply contrasting the respiratory metabolism retained by most intracellular symbionts. Our results provide insights into a tightly regulated and metabolically integrated extracellular symbiosis, expanding our understanding of the minimal metabolism required to sustain life outside of a host cell.