Drastic Genome Reduction in an Herbivore's Pectinolytic Symbiont

Hassan Salem, Eugen Bauer, Roy Kirsch, Aileen Berasategui, Michael Cripps, Benjamin Weiss, Ryuichi Koga, Kayoko Fukumori, Heiko Vogel, Takema Fukatsu, Martin Kaltenpoth

Research output: Contribution to JournalArticleAcademicpeer-review

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. A proteobacterial symbiont with the smallest known genome of an extracellular bacterium provides its host beetle with key enzymes to break down pectin in plant-based food, giving a striking example of symbiosis and evolutionary adaptation.
Original languageEnglish
Pages (from-to)1520-1531.e13
JournalCell
Volume171
Issue number7
DOIs
Publication statusPublished - 14 Dec 2017
Externally publishedYes

Funding

We thank Yannick Pauchet for insightful discussions on the experimental set-up and Nicole Gerardo, Amanda Gibson, Wen-Hao Tan, and Jaap de Roode for helpful comments on an earlier draft of the manuscript. We thank Sarah Jackman for her assistance in beetle collection and maintenance. Financial support from the Max Planck Society , the Alexander von Humboldt Foundation , and the German Science Foundation ( KI1917/1-1 ) is gratefully acknowledged.

FundersFunder number
Alexander von Humboldt-Stiftung
Deutsche ForschungsgemeinschaftKI1917/1-1
Japan Society for the Promotion of Science25221107
Max-Planck-Gesellschaft

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