Abstract
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.
Highlights
Symbiotic microbes can enable their host to access untapped nutritional resources but may constrain niche space by promoting specialization
Microbial symbionts are pervasive in herbivorous insects and often aid in alleviating the challenges associated with a plant-based feeding ecology[1]
While the subunits of NADH-ubiquinone oxidoreductase and cytochrome d ubiquinol oxidase are retained in all of the symbionts, the ATP synthase complex is only present in symbionts of the host genus Plateumaris, but absent in Donacia, Macroplea, and Neohaemonia, suggesting that the symbionts of these taxa use the proton gradient generated by the respiratory complex for secondary transport reactions and meet their ATP demands by substrate-level phosphorylation alone or obtain additional ATP from the host
Summary
Symbiotic microbes can enable their host to access untapped nutritional resources but may constrain niche space by promoting specialization. In addition to the amino acid and riboflavin biosynthesis pathways that supplement the hosts’ nutrition, the genomes of some reed beetle symbionts encode a polygalacturonase (PG, i.e., GH28) in the chromosome and/or on the plasmid.
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