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, Tae Young Yoon

Research output: Contribution to journalArticleScientificpeer-review

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.

Original languageEnglish
Article number3206
Number of pages15
JournalNature Communications
Volume12
Issue number1
DOIs
Publication statusPublished - 2021
Externally publishedYes

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