An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion

Sabbadin, Federico; Hemsworth, Glyn R.; Ciano, Luisa; Henrissat, Bernard; Dupree, Paul; Tryfona, Theodora; Marques, Rita D. S.; Sweeney, Sean T.; Besser, Katrin; Elias, Luisa; Pesante, Giovanna; Li, Yi; Dowle, Adam A.; Bates, Rachel; Gomez, Leonardo D.; Simister, Rachael; Davies, Gideon J.; Walton, Paul H.; Bruce, Neil C.; McQueen-Mason, Simon J.

Abstract

Thermobia domestica belongs to an ancient group of insects and has a remarkable ability to digest crystalline cellulose without microbial assistance. By investigating the digestive proteome of Thermobia, we have identified over 20 members of an uncharacterized family of lytic polysaccharide monooxygenases (LPMOs). We show that this LPMO family spans across several clades of the Tree of Life, is of ancient origin, and was recruited by early arthropods with possible roles in remodeling endogenous chitin scaffolds during development and metamorphosis. Based on our in-depth characterization of Thermobia's LPMOs, we propose that diversification of these enzymes toward cellulose digestion might have endowed ancestral insects with an effective biochemical apparatus for biomass degradation, allowing the early colonization of land during the Paleozoic Era. The vital role of LPMOs in modern agricultural pests and disease vectors offers new opportunities to help tackle global challenges in food security and the control of infectious diseases.

Citation

Sabbadin, F., Hemsworth, G. R., Ciano, L., Henrissat, B., Dupree, P., Tryfona, T., Marques, R. D. S., Sweeney, S. T., Besser, K., Elias, L., Pesante, G., Li, Y., Dowle, A. A., Bates, R., Gomez, L. D., Simister, R., Davies, G. J., Walton, P. H., Bruce, N. C., & McQueen-Mason, S. J. (2018). An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nature Communications, 9, Article 756. https://doi.org/10.1038/s41467-018-03142-x

• Journal Article Type: Article
• Acceptance Date: Jan 22, 2018
• Online Publication Date: Feb 22, 2018
• Publication Date: 2018-12
• Deposit Date: Feb 13, 2020
• Publicly Available Date: Feb 18, 2020
• Journal: Nature Communications
• Electronic ISSN: 2041-1723
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 9
• Article Number: 756
• DOI: https://doi.org/10.1038/s41467-018-03142-x
• Keywords: General Biochemistry, Genetics and Molecular Biology; General Physics and Astronomy; General Chemistry
• Public URL: https://nottingham-repository.worktribe.com/output/3829618
• Publisher URL: https://www.nature.com/articles/s41467-018-03142-x
• Additional Information: Received: 11 July 2017; Accepted: 22 January 2018; First Online: 22 February 2018; : The authors declare no competing financial interests.