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Insights into phosphoethanolamine cellulose synthesis and secretion across the Gram-negative cell envelope

Author

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  • Preeti Verma

    (University of Virginia School of Medicine)

  • Ruoya Ho

    (University of Virginia School of Medicine)

  • Schuyler A. Chambers

    (Stanford University)

  • Lynette Cegelski

    (Stanford University)

  • Jochen Zimmer

    (University of Virginia School of Medicine
    Howard Hughes Medical Institute)

Abstract

Phosphoethanolamine (pEtN) cellulose is a naturally occurring modified cellulose produced by several Enterobacteriaceae. The minimal components of the E. coli cellulose synthase complex include the catalytically active BcsA enzyme, a hexameric semicircle of the periplasmic BcsB protein, and the outer membrane (OM)-integrated BcsC subunit containing periplasmic tetratricopeptide repeats (TPR). Additional subunits include BcsG, a membrane-anchored periplasmic pEtN transferase associated with BcsA, and BcsZ, a periplasmic cellulase of unknown biological function. While cellulose synthesis and translocation by BcsA are well described, little is known about its pEtN modification and translocation across the cell envelope. We show that the N-terminal cytosolic domain of BcsA positions three BcsG copies near the nascent cellulose polymer. Further, the semicircle’s terminal BcsB subunit tethers the N-terminus of a single BcsC protein in a trans-envelope secretion system. BcsC’s TPR motifs bind a putative cello-oligosaccharide near the entrance to its OM pore. Additionally, we show that only the hydrolytic activity of BcsZ but not the subunit itself is necessary for cellulose secretion, suggesting a secretion mechanism based on enzymatic removal of translocation incompetent cellulose. Lastly, protein engineering introduces cellulose pEtN modification in orthogonal cellulose biosynthetic systems. These findings advance our understanding of pEtN cellulose modification and secretion.

Suggested Citation

  • Preeti Verma & Ruoya Ho & Schuyler A. Chambers & Lynette Cegelski & Jochen Zimmer, 2024. "Insights into phosphoethanolamine cellulose synthesis and secretion across the Gram-negative cell envelope," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51838-0
    DOI: 10.1038/s41467-024-51838-0
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    References listed on IDEAS

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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Jacob L. W. Morgan & Joanna Strumillo & Jochen Zimmer, 2013. "Crystallographic snapshot of cellulose synthesis and membrane translocation," Nature, Nature, vol. 493(7431), pages 181-186, January.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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    1. Itxaso Anso & Samira Zouhir & Thibault Géry Sana & Petya Violinova Krasteva, 2024. "Structural basis for synthase activation and cellulose modification in the E. coli Type II Bcs secretion system," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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