Drastic Genome Reduction in an Herbivore’s Pectinolytic Symbiont

Abstract

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.

Cellulose degradation in Gastrophysa viridula (Coleoptera: Chrysomelidae): functional characterization of two CAZymes belonging to glycoside hydrolase family 45 reveals a novel enzymatic activity

“…It is also possible that the gut microbiota may contribute to the degradation of the plant cell wall in phytophagous beetles and may compensate for the reduction of the xyloglucanase and cellulase activity due to the silencing of the GH45 genes. However, examples of microbial symbionts within phytophagous beetles contributing to plant cell wall degradation are rare, and only one chrysomelid beetle is known to harbor a pectinolytic symbiont (Salem et al, ). Nonetheless, a lack of change of phenotype for GH45‐1‐silenced animals remains difficult to understand as xyloglucanases from plant pathogenic fungi were shown to be essential to insects’ ability to penetrate and infest plant cells (Ma et al, ).…”

Pectin digestion in herbivorous beetles: Impact of pseudoenzymes exceeds that of their active counterparts

“…Additionally, symbionts of herbivorous insects can encode for pectinase activity [12,36]. A remarkable example shows how a "Phytophaga" beetle host benefits from a symbiont's pectolytic activity [37]: when the pectinase-encoding symbiont is removed from its Cassida rubiginosa leaf beetle host, insect survival is highly reduced. The symbiont most likely compensates for the loss of the Cassida endogenous PG genes, and host survival depends on pectin digestion facilitated by the symbiont.…”

Horizontal gene transfer to a defensive symbiont with a reduced genome amongst a multipartite beetle microbiome

“…Second, we found little evidence that Lv-StB is capable of making metabolites of use to the host, indicating that the symbiosis is likely not based on nutrition. L. villosa ’s diet of plant leaves may be nitrogen poor, with hard to digest plant cell wall components (Salem et al, 2017), but we didn’t find polysaccharide degrading pathways or extensive biosynthesis of essential amino acids in the Lv-StB genome. Therefore, the lga BGC is the oldest remaining feature that potentially increases host fitness.…”