Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase

Proceedings of the National Academy of Sciences of the United States of America
Sara TafoyaCarlos Bustamante

Abstract

Subunits in multimeric ring-shaped motors must coordinate their activities to ensure correct and efficient performance of their mechanical tasks. Here, we study WT and arginine finger mutants of the pentameric bacteriophage φ29 DNA packaging motor. Our results reveal the molecular interactions necessary for the coordination of ADP-ATP exchange and ATP hydrolysis of the motor's biphasic mechanochemical cycle. We show that two distinct regulatory mechanisms determine this coordination. In the first mechanism, the DNA up-regulates a single subunit's catalytic activity, transforming it into a global regulator that initiates the nucleotide exchange phase and the hydrolysis phase. In the second, an arginine finger in each subunit promotes ADP-ATP exchange and ATP hydrolysis of its neighbor. Accordingly, we suggest that the subunits perform the roles described for GDP exchange factors and GTPase-activating proteins observed in small GTPases. We propose that these mechanisms are fundamental to intersubunit coordination and are likely present in other ring ATPases.

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Citations

Sep 4, 2020·The New Phytologist·Wen SongJijie Chai
Mar 11, 2021·Biochemistry·Abdullah F U H SaeedSongying Ouyang
Mar 18, 2021·Nature Reviews Physics·Robijn F BruinsmaWouter H Roos
Aug 14, 2021·The Journal of Biological Chemistry·Xiang YeS Walter Englander
Oct 30, 2019·Chemical Reviews·Sonisilpa MohapatraTaekjip Ha
Nov 14, 2021·Nature Communications·Li DaiVenigalla B Rao

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