Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

Hassan Salem, Roy Kirsch, Yannick Pauchet, Aileen Berasategui, Kayoko Fukumori, Minoru Moriyama, Michael Cripps, Donald Windsor, Takema Fukatsu, Nicole M. Gerardo

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

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. 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.
Original languageEnglish
Pages (from-to)2875-2886.e4
JournalCurrent Biology
Volume30
Issue number15
DOIs
Publication statusPublished - 3 Aug 2020
Externally publishedYes

Funding

We thank the Department of Bioorganic Chemistry at the Max Planck Institute for Chemical Ecology for contributing live Chelymorpha alternans beetles, Tobin Hammer for scientific matchmaking, and Ryuichi Koga for insightful discussions. Financial support from the Alexander von Humboldt Foundation, Smithsonian Institution, National Science Foundation, Max Planck Society, and the Wissenschaftskolleg zu Berlin is gratefully acknowledged. Specimen images from Udo Schmidt (https://www.kaefer-der-welt.de) are greatly appreciated, as are illustrations from BioRender (https://biorender.com). H.S. and N.M.G. conceived of the study. H.S. N.M.G. D.W. R.K. Y.P. T.F. and A.B. designed the experiments. H.S. A.B. K.F. and M.M. performed genome sequencing, assembly, and analysis. R.K. and Y.P. carried out transcriptome sequencing, assembly, and analysis. R.K. and Y.P. performed the enzymatic assays. M.C. contributed insect specimens for initial assays. H.S. wrote the manuscript. All authors edited and commented on the paper. The authors declare no competing interests. We thank the Department of Bioorganic Chemistry at the Max Planck Institute for Chemical Ecology for contributing live Chelymorpha alternans beetles, Tobin Hammer for scientific matchmaking, and Ryuichi Koga for insightful discussions. Financial support from the Alexander von Humboldt Foundation , Smithsonian Institution , National Science Foundation , Max Planck Society , and the Wissenschaftskolleg zu Berlin is gratefully acknowledged. Specimen images from Udo Schmidt ( https://www.kaefer-der-welt.de ) are greatly appreciated, as are illustrations from BioRender ( https://biorender.com ).

FundersFunder number
Department of Bioorganic Chemistry
National Science Foundation
Smithsonian Institution
Alexander von Humboldt-Stiftung
Wissenschaftskolleg zu Berlin
Max-Planck-Gesellschaft

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