Kinetic and structural roles for the surface in guiding SAS-6 self-assembly to direct centriole architecture

Niccolò Banterle, Adrian P. Nievergelt, Svenja Buhr, Georgios N. Hatzopoulos, Charlène Brillard, Santiago Andany, Tania Hübscher, Frieda A. Sorgenfrei, Ulrich S. Schwarz, Frauke Gräter, Georg E. Fantner and Pierre Gönczy ()
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Niccolò Banterle: Swiss Federal Institute of Technology Lausanne (EPFL)
Adrian P. Nievergelt: Swiss Federal Institute of Technology Lausanne (EPFL)
Svenja Buhr: Interdisciplinary Center for Scientific Computing (IWR) Heidelberg University
Georgios N. Hatzopoulos: Swiss Federal Institute of Technology Lausanne (EPFL)
Charlène Brillard: Swiss Federal Institute of Technology Lausanne (EPFL)
Santiago Andany: Swiss Federal Institute of Technology Lausanne (EPFL)
Tania Hübscher: Swiss Federal Institute of Technology Lausanne (EPFL)
Frieda A. Sorgenfrei: Heidelberg Institute for Theoretical Studies, Heidelberg, Germany
Ulrich S. Schwarz: Interdisciplinary Center for Scientific Computing (IWR) Heidelberg University
Frauke Gräter: Interdisciplinary Center for Scientific Computing (IWR) Heidelberg University
Georg E. Fantner: Swiss Federal Institute of Technology Lausanne (EPFL)
Pierre Gönczy: Swiss Federal Institute of Technology Lausanne (EPFL)

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: Abstract Discovering mechanisms governing organelle assembly is a fundamental pursuit in biology. The centriole is an evolutionarily conserved organelle with a signature 9-fold symmetrical chiral arrangement of microtubules imparted onto the cilium it templates. The first structure in nascent centrioles is a cartwheel, which comprises stacked 9-fold symmetrical SAS-6 ring polymers emerging orthogonal to a surface surrounding each resident centriole. The mechanisms through which SAS-6 polymerization ensures centriole organelle architecture remain elusive. We deploy photothermally-actuated off-resonance tapping high-speed atomic force microscopy to decipher surface SAS-6 self-assembly mechanisms. We show that the surface shifts the reaction equilibrium by ~104 compared to solution. Moreover, coarse-grained molecular dynamics and atomic force microscopy reveal that the surface converts the inherent helical propensity of SAS-6 polymers into 9-fold rings with residual asymmetry, which may guide ring stacking and impart chiral features to centrioles and cilia. Overall, our work reveals fundamental design principles governing centriole assembly.

Date: 2021
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DOI: 10.1038/s41467-021-26329-1

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