Two KaiABC systems control circadian oscillations in one cyanobacterium

Christin Köbler, Nicolas M. Schmelling, Anika Wiegard, Alice Pawlowski, Gopal K. Pattanayak, Philipp Spät, Nina M. Scheurer, Kim N. Sebastian, Florian P. Stirba, Lutz C. Berwanger, Petra Kolkhof, Boris Maček, Michael J. Rust, Ilka M. Axmann () and Annegret Wilde ()
Additional contact information
Christin Köbler: University of Freiburg
Nicolas M. Schmelling: Heinrich Heine University Düsseldorf
Anika Wiegard: Heinrich Heine University Düsseldorf
Alice Pawlowski: Heinrich Heine University Düsseldorf
Gopal K. Pattanayak: The University of Chicago
Philipp Spät: Eberhard Karls University Tübingen
Nina M. Scheurer: University of Freiburg
Kim N. Sebastian: University of Freiburg
Florian P. Stirba: Heinrich Heine University Düsseldorf
Lutz C. Berwanger: Heinrich Heine University Düsseldorf
Petra Kolkhof: Heinrich Heine University Düsseldorf
Boris Maček: Eberhard Karls University Tübingen
Michael J. Rust: The University of Chicago
Ilka M. Axmann: Heinrich Heine University Düsseldorf
Annegret Wilde: University of Freiburg

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract The circadian clock of cyanobacteria, which predicts daily environmental changes, typically includes a standard oscillator consisting of proteins KaiA, KaiB, and KaiC. However, several cyanobacteria have diverse Kai protein homologs of unclear function. In particular, Synechocystis sp. PCC 6803 harbours, in addition to a canonical kaiABC gene cluster (named kaiAB1C1), two further kaiB and kaiC homologs (kaiB2, kaiB3, kaiC2, kaiC3). Here, we identify a chimeric KaiA homolog, named KaiA3, encoded by a gene located upstream of kaiB3. At the N-terminus, KaiA3 is similar to response-regulator receiver domains, whereas its C-terminal domain resembles that of KaiA. Homology analysis shows that a KaiA3-KaiB3-KaiC3 system exists in several cyanobacteria and other bacteria. Using the Synechocystis sp. PCC 6803 homologs, we observe circadian oscillations in KaiC3 phosphorylation in vitro in the presence of KaiA3 and KaiB3. Mutations of kaiA3 affect KaiC3 phosphorylation, leading to growth defects under both mixotrophic and chemoheterotrophic conditions. KaiC1 and KaiC3 exhibit phase-locked free-running phosphorylation rhythms. Deletion of either system (∆kaiAB1C1 or ∆kaiA3B3C3) alters the period of the cellular backscattering rhythm. Furthermore, both oscillators are required to maintain high-amplitude, self-sustained backscatter oscillations with a period of approximately 24 h, indicating their interconnected nature.

Date: 2024
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DOI: 10.1038/s41467-024-51914-5

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