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

Author

Listed:
  • Federico Sabbadin

    (University of York)

  • Glyn R. Hemsworth

    (University of Leeds
    University of Leeds)

  • Luisa Ciano

    (University of York)

  • Bernard Henrissat

    (Université Aix-Marseille
    INRA, USC 1408 AFMB
    King Abdulaziz University)

  • Paul Dupree

    (University of Cambridge)

  • Theodora Tryfona

    (University of Cambridge)

  • Rita D. S. Marques

    (University of Cambridge)

  • Sean T. Sweeney

    (University of York)

  • Katrin Besser

    (University of York)

  • Luisa Elias

    (University of York)

  • Giovanna Pesante

    (University of York)

  • Yi Li

    (University of York)

  • Adam A. Dowle

    (University of York)

  • Rachel Bates

    (University of York)

  • Leonardo D. Gomez

    (University of York)

  • Rachael Simister

    (University of York)

  • Gideon J. Davies

    (University of York)

  • Paul H. Walton

    (University of York)

  • Neil C. Bruce

    (University of York)

  • Simon J. McQueen-Mason

    (University of York)

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.

Suggested Citation

  • Federico Sabbadin & Glyn R. Hemsworth & Luisa Ciano & Bernard Henrissat & Paul Dupree & Theodora Tryfona & Rita D. S. Marques & Sean T. Sweeney & Katrin Besser & Luisa Elias & Giovanna Pesante & Yi Li, 2018. "An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-03142-x
    DOI: 10.1038/s41467-018-03142-x
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    Cited by:

    1. Wen-Xin Jiang & Ping-Yi Li & Xiu-Lan Chen & Yi-Shuo Zhang & Jing-Ping Wang & Yan-Jun Wang & Qi Sheng & Zhong-Zhi Sun & Qi-Long Qin & Xue-Bing Ren & Peng Wang & Xiao-Yan Song & Yin Chen & Yu-Zhong Zhan, 2022. "A pathway for chitin oxidation in marine bacteria," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Iván Ayuso-Fernández & Tom Z. Emrich-Mills & Julia Haak & Ole Golten & Kelsi R. Hall & Lorenz Schwaiger & Trond S. Moe & Anton A. Stepnov & Roland Ludwig & George E. Cutsail III & Morten Sørlie & Åsmu, 2024. "Mutational dissection of a hole hopping route in a lytic polysaccharide monooxygenase (LPMO)," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Ho Ta Giap & Ngo Nguyen Vu & Vu Van Van, 2023. "Isolation and identification of Vibrio spp. with potential ability to produce polysaccharide monooxygenase from diseased Penaeus monodon," HO CHI MINH CITY OPEN UNIVERSITY JOURNAL OF SCIENCE - ENGINEERING AND TECHNOLOGY, HO CHI MINH CITY OPEN UNIVERSITY JOURNAL OF SCIENCE, HO CHI MINH CITY OPEN UNIVERSITY, vol. 13(1), pages 24-32.

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