A concerted ATPase cycle of the protein transporter AAA-ATPase Bcs1

Yangang Pan, Jingyu Zhan, Yining Jiang, Di Xia and Simon Scheuring ()
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Yangang Pan: Weill Cornell Medical College
Jingyu Zhan: National Cancer Institute, National Institutes of Health
Yining Jiang: Weill Cornell Medical College
Di Xia: National Cancer Institute, National Institutes of Health
Simon Scheuring: Weill Cornell Medical College

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Bcs1, a homo-heptameric transmembrane AAA-ATPase, facilitates folded Rieske iron-sulfur protein translocation across the inner mitochondrial membrane. Structures in different nucleotide states (ATPγS, ADP, apo) provided conformational snapshots, but the kinetics and structural transitions of the ATPase cycle remain elusive. Here, using high-speed atomic force microscopy (HS-AFM) and line scanning (HS-AFM-LS), we characterized single-molecule Bcs1 ATPase cycling. While the ATP conformation had ~5600 ms lifetime, independent of the ATP-concentration, the ADP/apo conformation lifetime was ATP-concentration dependent and reached ~320 ms at saturating ATP-concentration, giving a maximum turnover rate of 0.17 s−1. Importantly, Bcs1 ATPase cycle conformational changes occurred in concert. Furthermore, we propose that the transport mechanism involves opening the IMS gate through energetically costly straightening of the transmembrane helices, potentially driving rapid gate resealing. Overall, our results establish a concerted ATPase cycle mechanism in Bcs1, distinct from other AAA-ATPases that use a hand-over-hand mechanism.

Date: 2023
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DOI: 10.1038/s41467-023-41806-5

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