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Title: The nucleotide-dependent interaction of FlaH and FlaI is essential for assembly and function of the archaellum motor

Journal Article · · Molecular Microbiology
DOI:https://doi.org/10.1111/mmi.13260· OSTI ID:1378738
 [1];  [1];  [2];  [3];  [4];  [1];  [4];  [2];  [1];  [5];  [2];  [1]
  1. Univ. of Freiburg (Germany)
  2. Max Planck Inst. of Biophysics, Frankfurt (Germany)
  3. Philipps Univ. of Marburg (Germany)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Texas M. D. Anderson Cancer Center, Houston, TX (United States)

The motor of the membrane-anchored archaeal motility structure, the archaellum, contains FlaX, FlaI and FlaH. FlaX forms a 30 nm ring structure that acts as a scaffold protein and was shown to interact with the bifunctional ATPase FlaI and FlaH. However, the structure and function of FlaH has been enigmatic. Here we present structural and functional analyses of isolated FlaH and archaellum motor subcomplexes. The FlaH crystal structure reveals a RecA/Rad51 family fold with an ATP bound on a conserved and exposed surface, which presumably forms an oligomerization interface. FlaH does not hydrolyze ATP in vitro, but ATP binding to FlaH is essential for its interaction with FlaI and for archaellum assembly. FlaH interacts with the C-terminus of FlaX, which was earlier shown to be essential for FlaX ring formation and to mediate interaction with FlaI. Electron microscopy reveals that FlaH assembles as a second ring inside the FlaX ring in vitro. Collectively these data reveal central structural mechanisms for FlaH interactions in mediating archaellar assembly: FlaH binding within the FlaX ring and nucleotide-regulated FlaH binding to FlaI form the archaellar basal body core.

Research Organization:
Univ. of Freiburg (Germany); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; National Inst. of Health (NIH) (United States); Max Planck Society (Germany); European Research Council (ERC)
Grant/Contract Number:
AC02-05CH11231; GM105404; 311523
OSTI ID:
1378738
Journal Information:
Molecular Microbiology, Vol. 99, Issue 4; ISSN 0950-382X
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 31 works
Citation information provided by
Web of Science

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Cited By (19)

Salt‐dependent regulation of archaellins in Haloarcula marismortui journal October 2018
Direct observation of rotation and steps of the archaellum in the swimming halophilic archaeon Halobacterium salinarum journal August 2016
CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus journal December 2016
The structure of the periplasmic FlaG–FlaF complex and its essential role for archaellar swimming motility journal December 2019
Motor torque measurement of Halobacterium salinarum archaellar suggests a general model for ATP-driven rotary motors journal May 2019
Taxis in archaea journal November 2018
Archaeal cell surface biogenesis journal June 2018
Structure of the archaeal chemotaxis protein CheY in a domain-swapped dimeric conformation journal August 2019
Tree of motility – A proposed history of motility systems in the tree of life journal January 2020
Versatile cell surface structures of archaea: Cell surface structures of archaea journal December 2017
Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction journal May 2017
Evolution of the Stator Elements of Rotary Prokaryote Motors journal October 2019
Twitch or swim: towards the understanding of prokaryotic motion based on the type IV pilus blueprint journal June 2018
Diversity and Evolution of Type IV pili Systems in Archaea journal May 2016
Proteomic Analysis of Methanonatronarchaeum thermophilum AMET1, a Representative of a Putative New Class of Euryarchaeota, “Methanonatronarchaeia” journal January 2018
Structure and in situ organisation of the Pyrococcus furiosus archaellum machinery journal June 2017
Structure of the archaeal chemotaxis protein CheY in a domain-swapped dimeric conformation text January 2019
Structure and in situ organisation of the Pyrococcus furiosus archaellum machinery text January 2017
Cross-kymography analysis to simultaneously quantify the function and morphology of the archaellum journal January 2018