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Identification of d-arabinan-degrading enzymes in mycobacteria

Author

Listed:
  • Omar Al-Jourani

    (Newcastle University)

  • Samuel T. Benedict

    (University of Birmingham)

  • Jennifer Ross

    (Newcastle University)

  • Abigail J. Layton

    (University of Birmingham)

  • Phillip Peet

    (University of Melbourne, Parkville)

  • Victoria M. Marando

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Nicholas P. Bailey

    (Newcastle University)

  • Tiaan Heunis

    (Newcastle University)

  • Joseph Manion

    (Newcastle University)

  • Francesca Mensitieri

    (Newcastle University)

  • Aaron Franklin

    (University of Birmingham)

  • Javier Abellon-Ruiz

    (Newcastle University)

  • Sophia L. Oram

    (Newcastle University)

  • Lauren Parsons

    (Newcastle University)

  • Alan Cartmell

    (University of Liverpool)

  • Gareth S. A. Wright

    (University of Essex)

  • Arnaud Baslé

    (Newcastle University)

  • Matthias Trost

    (Newcastle University)

  • Bernard Henrissat

    (King Abdulaziz University
    Technical University of Denmark)

  • Jose Munoz-Munoz

    (Northumbria University)

  • Robert P. Hirt

    (Newcastle University)

  • Laura L. Kiessling

    (Massachusetts Institute of Technology)

  • Andrew L. Lovering

    (University of Birmingham)

  • Spencer J. Williams

    (University of Melbourne, Parkville)

  • Elisabeth C. Lowe

    (Newcastle University)

  • Patrick J. Moynihan

    (University of Birmingham)

Abstract

Bacterial cell growth and division require the coordinated action of enzymes that synthesize and degrade cell wall polymers. Here, we identify enzymes that cleave the d-arabinan core of arabinogalactan, an unusual component of the cell wall of Mycobacterium tuberculosis and other mycobacteria. We screened 14 human gut-derived Bacteroidetes for arabinogalactan-degrading activities and identified four families of glycoside hydrolases with activity against the d-arabinan or d-galactan components of arabinogalactan. Using one of these isolates with exo-d-galactofuranosidase activity, we generated enriched d-arabinan and used it to identify a strain of Dysgonomonas gadei as a d-arabinan degrader. This enabled the discovery of endo- and exo-acting enzymes that cleave d-arabinan, including members of the DUF2961 family (GH172) and a family of glycoside hydrolases (DUF4185/GH183) that display endo-d-arabinofuranase activity and are conserved in mycobacteria and other microbes. Mycobacterial genomes encode two conserved endo-d-arabinanases with different preferences for the d-arabinan-containing cell wall components arabinogalactan and lipoarabinomannan, suggesting they are important for cell wall modification and/or degradation. The discovery of these enzymes will support future studies into the structure and function of the mycobacterial cell wall.

Suggested Citation

  • Omar Al-Jourani & Samuel T. Benedict & Jennifer Ross & Abigail J. Layton & Phillip Peet & Victoria M. Marando & Nicholas P. Bailey & Tiaan Heunis & Joseph Manion & Francesca Mensitieri & Aaron Frankli, 2023. "Identification of d-arabinan-degrading enzymes in mycobacteria," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37839-5
    DOI: 10.1038/s41467-023-37839-5
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    References listed on IDEAS

    as
    1. Fiona Cuskin & Elisabeth C. Lowe & Max J. Temple & Yanping Zhu & Elizabeth A. Cameron & Nicholas A. Pudlo & Nathan T. Porter & Karthik Urs & Andrew J. Thompson & Alan Cartmell & Artur Rogowski & Brian, 2015. "Correction: Corrigendum: Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism," Nature, Nature, vol. 520(7547), pages 388-388, April.
    2. Fiona Cuskin & Elisabeth C. Lowe & Max J. Temple & Yanping Zhu & Elizabeth A. Cameron & Nicholas A. Pudlo & Nathan T. Porter & Karthik Urs & Andrew J. Thompson & Alan Cartmell & Artur Rogowski & Brian, 2015. "Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism," Nature, Nature, vol. 517(7533), pages 165-169, January.
    3. Patrick J. Moynihan & Ian T. Cadby & Natacha Veerapen & Monika Jankute & Marialuisa Crosatti & Galina V. Mukamolova & Andrew L. Lovering & Gurdyal S. Besra, 2019. "The hydrolase LpqI primes mycobacterial peptidoglycan recycling," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

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