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Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles

MPS-Authors
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Busch,  André
Department of Entomology, Prof. D. G. Heckel, MPI for Chemical Ecology, Max Planck Society;
IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society;

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Pauchet,  Yannick
Department of Entomology, Prof. D. G. Heckel, MPI for Chemical Ecology, Max Planck Society;

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Citation

Busch, A., Danchin, E. G. J., & Pauchet, Y. (2019). Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles. BMC Evolutionary Biology, 19: 100. doi:10.1186/s12862-019-1429-9.


Cite as: https://hdl.handle.net/21.11116/0000-0003-9626-9
Abstract
Background: Cellulose, a major polysaccharide of the plant cell wall, consists of β-1,4-linked glucose moieties
forming a molecular network recalcitrant to enzymatic breakdown. Although cellulose is potentially a rich source of
energy, the ability to degrade it is rare in animals and was believed to be present only in cellulolytic microbes.
Recently, it has become clear that some animals encode endogenous cellulases belonging to several glycoside
hydrolase families (GHs), including GH45. GH45s are distributed patchily among the Metazoa and, in insects, are
encoded only by the genomes of Phytophaga beetles. This study aims to understand both the enzymatic functions
and the evolutionary history of GH45s in these beetles.
Results: To this end, we biochemically assessed the enzymatic activities of 37 GH45s derived from five species of
Phytophaga beetles and discovered that beetle-derived GH45s degrade three different substrates: amorphous
cellulose, xyloglucan and glucomannan. Our phylogenetic and gene structure analyses indicate that at least one
gene encoding a putative cellulolytic GH45 was present in the last common ancestor of the Phytophaga, and that
GH45 xyloglucanases evolved several times independently in these beetles. The most closely related clade to
Phytophaga GH45s was composed of fungal sequences, suggesting this GH family was acquired by horizontal gene
transfer from fungi. Besides the insects, other arthropod GH45s do not share a common origin and appear to have
emerged at least three times independently.
Conclusion: The rise of functional innovation from gene duplication events has been a fundamental process in the
evolution of GH45s in Phytophaga beetles. Both, enzymatic activity and ancestral origin suggest that GH45s were
likely an essential prerequisite for the adaptation allowing Phytophaga beetles to feed on plants.