Pectin, an integral component of the plant cell wall, is a recalcitrant substrate against enzymatic challenges by most animals. In characterizing the source of a leaf beetle's (Cassida rubiginosa) pectin-degrading phenotype, we demonstrate its dependency on an extracellular bacterium housed in specialized organs connected to the foregut. Despite possessing the smallest genome (0.27 Mb) of any organism not subsisting within a host cell, the symbiont nonetheless retained a functional pectinolytic metabolism targeting the polysaccharide's two most abundant classes: homogalacturonan and rhamnogalacturonan I. Comparative transcriptomics revealed pectinase expression to be enriched in the symbiotic organs, consistent with enzymatic buildup in these structures following immunostaining with pectinase-targeting antibodies. Symbiont elimination results in a drastically reduced host survivorship and a diminished capacity to degrade pectin. Collectively, our findings highlight symbiosis as a strategy for an herbivore to metabolize one of nature's most complex polysaccharides and a universal component of plant tissues.

Highlights d Stammera genomes are structurally conserved across Cassidinae species d Symbiont pectinases complement the host's endogenous cellulases and xylanases d Stammera differentially encode pectinases in their reduced genomes d Symbiont pectinolytic range reflects host plant breadth

Insects represent the biodiversity of the terrestrial ecosystem, and their prosperity is attributable to their association with symbiotic microorganisms. By sequestering microbial functionality into their bodies, organs, tissues, or cells, diverse insects have successfully exploited otherwise inaccessible ecological niches and resources, including herbivory enabled by utilization of indigestible plant cell wall components. In leaf beetles of the subfamily Cassininae, an ancient symbiont lineage, Stammera , whose genome is extremely reduced and specialized for encoding pectin-degrading enzymes, is hosted in gut-associated symbiotic organs and contributes to the host’s food plant digestion.

Symbiotic microbes can enable their host to access untapped nutritional resources but may also constrain niche space by promoting specialization. Here, we reconstruct functional changes in the evolutionary history of the symbiosis between a group of (semi-)aquatic herbivorous insects and mutualistic bacteria. Sequencing the symbiont genomes across 26 species of reed beetles (Chrysomelidae, Donaciinae) spanning four genera indicates that the genome-eroded mutualists provide life stage-specific benefits to larvae and adults, respectively. In the plant sap-feeding larvae, the symbionts are inferred to synthesize most of the essential amino acids as well as the B vitamin riboflavin. The adult reed beetles' folivory is likely supported by symbiont-encoded pectinases that complement the host-encoded set of cellulases, as revealed by transcriptome sequencing. However, mapping the occurrence of the symbionts' pectinase genes and the hosts' food plant preferences onto the beetles' phylogeny reveals multiple independent losses of pectinase genes in lineages that switched to feeding on pectin-poor plants, presumably constraining their hosts' subsequent adaptive potential.