Publikationsserver der Universitätsbibliothek Marburg
Titel:Decipering the subunit interaction in the crenarchaeal archaellum
Autor:Neiner, Tomasz Paweł
Weitere Beteiligte: Albers, Sonja-Verena (Prof. Dr.)
Veröffentlicht:2014
URI:https://archiv.ub.uni-marburg.de/diss/z2014/0481
DOI: https://doi.org/10.17192/z2014.0481
URN: urn:nbn:de:hebis:04-z2014-04819
DDC: Biowissenschaften, Biologie
Titel (trans.):Dechiffrierung von Wechselwirkungen der Untereinheiten des Archaellum von Crenarchaeota
Publikationsdatum:2015-07-15
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Archaellum, crenarchaeal archaellum, Crenarchaeota

Summary:
The archaeal motility structure, the archaellum is an intriguing hybrid of the function and architecture of two distinct motility organelles, the bacterial flagellum and the T4P, respectively. This rotating T4P is an astonishing example of evolutionary adaptation and represents indeed a unique, third way to move. This microbial structure was however for long time ignored and while many bacterial structures have been already well characterized, the knowledge about the archaellum remains still scare. The so far performed studies were restricted to motility in Euryarchaeota and included physiological and genetic analyses of few species. Here we present a detailed systematic and structural analysis of the crenarchaeal archaellum using the thermoacidophile Sulfolobus acidocaldarius as model organism. S. acidocaldarius has the most minimalistic known archaellum system, composed of only seven Fla proteins. In-frame deletion strain analysis revealed all seven fla genes to be essential for proper archaellum assembly. All these mutants were non-motile, conclusively linking the archaellum of Crenarchaeota with their swimming motility. Moreover, using immunoblot analysis we found the archaella biosynthesis to be induced under nutrient depleting conditions. We could also demonstrate that despite that all the seven fla genes are clustered in one genomic locus, they are expressed in two different transcriptional units. Thus the archaellin FlaB and the remaining structural components FlaXHGFHIJ encoding genes are expressed separately. The main focus of this work was however the structural aspect of the S. acidocaldarius archaellum. Thus we are presenting here a detailed biochemical and structural characterization of the two cytosolic components of the archaellum: the RecA family protein FlaH and the ATPase FlaI. By elucidating the interaction network of FlaH and FlaI within the archaellum, we could place them together with FlaX and FlaJ as structural components of the basal body The ATPase FlaI was successfully crystallized in hexameric form and we could solve this structure at 2.0 Å resolution. FlaI hexamer forms a crown-like structure with subunits at three different conformational states, assembled together in a rare cross-subunit interacting fashion. Further analysis revealed also that the enzymatic activity and system specificity of FlaI are structurally separated, since the ATPase is restricted to the C-terminal domain, while the functional part is represented by the N-terminal domain. We demonstrated moreover that FlaI has a dual role and is involved in generating the energy necessary for both, the archaellum assembly and its rotation. The functions of FlaI could be uncoupled by deleting the first 29 amino acids of the N-terminus, resulting in archaellated, but not motile phenotype. FlaH was characterized as an ATP-binding protein, since no ATPase activity could be detected. It has a well conserved Walker A, but an incomplete Walker B motif and as we could show with in vivo and in vitro analysis both motifs are important for ATP binding and also were essential for archaella assembly and motility. The structure of FlaH was solved at 2.3 Å resolution, revealing the presence of a bound ATP molecule, supporting the hypothesis that FlaH does not hydrolyze ATP. Structural similarities to the CII domain of KaiC and a proved auto-phosphorylation activity, suggest that FlaH plays a regulatory role and controls the archaellum assembly/function in a phosphorylation dependent manner. Taking together, all the presented here data provide insights into the role of the archaellum of S. acidocaldarius, its genomic organization and unique molecular architecture. Furthermore our structural analysis revealed differences between the motor proteins within the archaellum and the related bacterial systems, elucidating the phenomenon of the rotating type IV pilus. However, many questions regarding the archaellum remain still open and present a challenge for further motility studies in Archaea.

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