Donor strand complementation and calcium ion coordination drive the chaperone-free polymerization of archaeal cannulae

Mike Sleutel, Ravi R. Sonani, Jessalyn G. Miller, Fengbin Wang, Andres Gonzalez Socorro, Yang Chen, Reece Martin, Borries Demeler, Michael J. Rudolph, Vikram Alva, Han Remaut (), Edward H. Egelman () and Vincent P. Conticello ()
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Mike Sleutel: Vrije Universiteit Brussel
Ravi R. Sonani: University of Virginia
Jessalyn G. Miller: Emory University
Fengbin Wang: University of Virginia
Andres Gonzalez Socorro: Emory University
Yang Chen: New York Structural Biology Center
Reece Martin: University of Lethbridge
Borries Demeler: University of Lethbridge
Michael J. Rudolph: New York Structural Biology Center
Vikram Alva: Max Planck Institute for Biology Tübingen
Han Remaut: Vrije Universiteit Brussel
Edward H. Egelman: University of Virginia
Vincent P. Conticello: Emory University

Nature Communications, 2025, vol. 16, issue 1, 1-18

Abstract: Abstract Cannulae are structurally rigid tubular protein filaments that accumulate on the extracellular surface of archaea within the family Pyrodictiaceae during cell growth. These obligate anaerobes propagate under hyperthermophilic conditions in which cannulae form a biomatrix that interconnects and sustains cells. The persistence of cannulae in this environment suggests that these filaments display significant thermostability, which has attracted technological interest in their development as synthetic protein-based biomaterials. Here, we report cryoEM structural analyses of ex vivo and in vitro assembled recombinant cannulae. We demonstrate that the interactions between protomers in native and recombinant cannulae is based on donor strand complementation (DSC), a form of non-covalent polymerization previously observed for bacterial chaperone-usher pili. Unexpectedly, calcium ion coordination at the subunit interfaces reinforces the network of donor strand interactions in the cannulae. This study provides insight into the mechanism of assembly of cannulae and the structural origin of their high stability and rigidity.

Date: 2025
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DOI: 10.1038/s41467-025-64120-8

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