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Extreme parsimony in ATP consumption by 20S complexes in the global disassembly of single SNARE complexes

Changwon Kim, Min Ju Shon, Sung Hyun Kim, Gee Sung Eun, Je-Kyung Ryu, Changbong Hyeon, Reinhard Jahn and Tae-Young Yoon ()
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Changwon Kim: Seoul National University
Min Ju Shon: Seoul National University
Sung Hyun Kim: Seoul National University
Gee Sung Eun: Seoul National University
Je-Kyung Ryu: KAIST
Changbong Hyeon: Korea Institute for Advanced Study
Reinhard Jahn: Max-Planck-Institute for Biophysical Chemistry
Tae-Young Yoon: Seoul National University

Nature Communications, 2021, vol. 12, issue 1, 1-15

Abstract: Abstract Fueled by ATP hydrolysis in N-ethylmaleimide sensitive factor (NSF), the 20S complex disassembles rigid SNARE (soluble NSF attachment protein receptor) complexes in single unraveling step. This global disassembly distinguishes NSF from other molecular motors that make incremental and processive motions, but the molecular underpinnings of its remarkable energy efficiency remain largely unknown. Using multiple single-molecule methods, we found remarkable cooperativity in mechanical connection between NSF and the SNARE complex, which prevents dysfunctional 20S complexes that consume ATP without productive disassembly. We also constructed ATP hydrolysis cycle of the 20S complex, in which NSF largely shows randomness in ATP binding but switches to perfect ATP hydrolysis synchronization to induce global SNARE disassembly, minimizing ATP hydrolysis by non-20S complex-forming NSF molecules. These two mechanisms work in concert to concentrate ATP consumption into functional 20S complexes, suggesting evolutionary adaptations by the 20S complex to the energetically expensive mechanical task of SNARE complex disassembly.

Date: 2021
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DOI: 10.1038/s41467-021-23530-0

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