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Structural insights into ATP hydrolysis by the MoxR ATPase RavA and the LdcI-RavA cage-like complex.

<div class='caption-title'>Cryo-EM structure of the LdcI–RavA cage-like complex.</div>
<div class='caption-title'>Comparison between a RavA hexamer generated from the RavA crystal structure and a fit in the cryo-EM map of the LdcI–RavA complex.</div>
<div class='caption-title'>Cryo-EM analysis of free RavA in the presence of nucleotide (ADP).</div>
Jessop M, Arragain B, Miras R, Fraudeau A, Huard K, Bacia-Verloop M, Catty P, Felix J, Malet H, Gutsche I
OpenAccess logo Commun Biol 3 46 (2020)
Related entries: 6q7l, 6sza, 6szb

Cited: 14 times
EuropePMC logo PMID: 31992852

Abstract

The hexameric MoxR AAA+ ATPase RavA and the decameric lysine decarboxylase LdcI form a 3.3 MDa cage, proposed to assist assembly of specific respiratory complexes in E. coli. Here, we show that inside the LdcI-RavA cage, RavA hexamers adopt an asymmetric spiral conformation in which the nucleotide-free seam is constrained to two opposite orientations. Cryo-EM reconstructions of free RavA reveal two co-existing structural states: an asymmetric spiral, and a flat C2-symmetric closed ring characterised by two nucleotide-free seams. The closed ring RavA state bears close structural similarity to the pseudo two-fold symmetric crystal structure of the AAA+ unfoldase ClpX, suggesting a common ATPase mechanism. Based on these structures, and in light of the current knowledge regarding AAA+ ATPases, we propose different scenarios for the ATP hydrolysis cycle of free RavA and the LdcI-RavA cage-like complex, and extend the comparison to other AAA+ ATPases of clade 7.

Reviews citing this publication (1)

  1. AAA+ ATPases: structural insertions under the magnifying glass. Jessop M, Felix J, Gutsche I. Curr Opin Struct Biol 66 119-128 (2021)

Articles citing this publication (13)

  1. Structural asymmetry governs the assembly and GTPase activity of McrBC restriction complexes. Niu Y, Suzuki H, Hosford CJ, Walz T, Chappie JS. Nat Commun 11 5907 (2020)
  2. Congress AAA+ proteins: converging mechanisms, diverging functions. Glynn SE, Kardon JR, Mueller-Cajar O, Cho C. Nat Struct Mol Biol 27 515-518 (2020)
  3. Discovery of ancestral L-ornithine and L-lysine decarboxylases reveals parallel, pseudoconvergent evolution of polyamine biosynthesis. Li B, Liang J, Hanfrey CC, Phillips MA, Michael AJ. J Biol Chem 297 101219 (2021)
  4. Conformational variability of cyanobacterial ChlI, the AAA+ motor of magnesium chelatase involved in chlorophyll biosynthesis. Shvarev D, Scholz AI, Moeller A. mBio 14 e0189323 (2023)
  5. Coupling of distant ATPase domains in the circadian clock protein KaiC. Swan JA, Sandate CR, Chavan AG, Freeberg AM, Etwaru D, Ernst DC, Palacios JG, Golden SS, LiWang A, Lander GC, Partch CL. Nat Struct Mol Biol 29 759-766 (2022)
  6. Cryo-EM Structure of the Type IV Pilus Extension ATPase from Enteropathogenic Escherichia coli. Nayak AR, Singh PK, Zhao J, Samsó M, Donnenberg MS. mBio e0227022 (2022)
  7. Insights into the structure-function relationship of the NorQ/NorD chaperones from Paracoccus denitrificans reveal shared principles of interacting MoxR AAA+/VWA domain proteins. Kahle M, Appelgren S, Elofsson A, Carroni M, Ädelroth P. BMC Biol 21 47 (2023)
  8. Mechanistic insights into sulfur source-driven physiological responses and metabolic reorganization in the fuel-biodesulfurizing Rhodococcus qingshengii IGTS8. Zumsteg J, Hirschler A, Carapito C, Maurer L, Villette C, Heintz D, Dahl C, El Nayal A, Sangal V, Mahmoud H, Van Dorsselaer A, Ismail W. Appl Environ Microbiol 89 e0082623 (2023)
  9. Structural and functional analysis of the Francisella lysine decarboxylase as a key actor in oxidative stress resistance. Felix J, Siebert C, Ducassou JN, Nigou J, Garcia PS, Fraudeau A, Huard K, Mas C, Brochier-Armanet C, Couté Y, Gutsche I, Renesto P. Sci Rep 11 972 (2021)
  10. Supramolecular assembly of the Escherichia coli LdcI upon acid stress. Jessop M, Liesche C, Felix J, Desfosses A, Baulard M, Adam V, Fraudeau A, Huard K, Effantin G, Kleman JP, Bacia-Verloop M, Bourgeois D, Gutsche I. Proc Natl Acad Sci U S A 118 (2021)
  11. The AAA+ ATPase RavA and its binding partner ViaA modulate E. coli aminoglycoside sensitivity through interaction with the inner membrane. Felix J, Bumba L, Liesche C, Fraudeau A, Rébeillé F, El Khoury JY, Huard K, Gallet B, Moriscot C, Kleman JP, Duhoo Y, Jessop M, Kandiah E, Barras F, Jouhet J, Gutsche I. Nat Commun 13 5502 (2022)
  12. The RavA-ViaA chaperone complex modulates bacterial persistence through its association with the fumarate reductase enzyme. Bhandari V, Reichheld SE, Houliston S, Lemak A, Arrowsmith CH, Sharpe S, Houry WA. J Biol Chem 299 105199 (2023)
  13. Translation Fidelity and Respiration Deficits in CLPP-Deficient Tissues: Mechanistic Insights from Mitochondrial Complexome Profiling. Key J, Gispert S, Koepf G, Steinhoff-Wagner J, Reichlmeir M, Auburger G. Int J Mol Sci 24 17503 (2023)


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