Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

• Published in: Current biology Vol. 30; no. 15; pp. 2875 - 2886.e4
• Main Authors: Salem, Hassan, Kirsch, Roy, Pauchet, Yannick, Berasategui, Aileen, Fukumori, Kayoko, Moriyama, Minoru, Cripps, Michael, Windsor, Donald, Fukatsu, Takema, Gerardo, Nicole M.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 03.08.2020
• Subjects: adaptation; beetles; co-evolution; herbivore-microbe interactions; herbivory; symbiosis; herbivore-microbe interactions; herbivory; adaptation; beetles; symbiosis; co-evolution
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2020.05.043

Numerous adaptations are gained in light of a symbiotic lifestyle. Here, we investigated the obligate partnership between tortoise leaf beetles (Chrysomelidae: Cassidinae) and their pectinolytic Stammera symbionts to detail how changes to the bacterium’s streamlined metabolic range can shape the digestive physiology and ecological opportunity of its herbivorous host. Comparative genomics of 13 Stammera strains revealed high functional conservation, highlighted by the universal presence of polygalacturonase, a primary pectinase targeting nature’s most abundant pectic class, homogalacturonan (HG). Despite this conservation, we unexpectedly discovered a disparate distribution for rhamnogalacturonan lyase, a secondary pectinase hydrolyzing the pectic heteropolymer, rhamnogalacturonan I (RG-I). Consistent with the annotation of rhamnogalacturonan lyase in Stammera, cassidines are able to depolymerize RG-I relative to beetles whose symbionts lack the gene. Given the omnipresence of HG and RG-I in foliage, Stammera that encode pectinases targeting both substrates allow their hosts to overcome a greater diversity of plant cell wall polysaccharides and maximize access to the nutritionally rich cytosol. Possibly facilitated by their symbionts’ expanded digestive range, cassidines additionally endowed with rhamnogalacturonan lyase appear to utilize a broader diversity of angiosperms than those beetles whose symbionts solely supplement polygalacturonase. Our findings highlight how symbiont metabolic diversity, in concert with host adaptations, may serve as a potential source of evolutionary innovations for herbivorous lineages. [Display omitted] •Stammera genomes are structurally conserved across Cassidinae species•Symbiont pectinases complement the host’s endogenous cellulases and xylanases•Stammera differentially encode pectinases in their reduced genomes•Symbiont pectinolytic range reflects host plant breadth Tortoise leaf beetles rely on the symbiotic bacterium, Stammera, to digest foliage rich in pectin. Salem et al. reveal that Stammera varies in the pectinases it encodes and supplements. Stammera encoding a more dynamic digestive range allows its host to overcome a greater diversity of plant polysaccharides, corresponding to a wider ecological distribution.