Structural and functional characterisation of the cyanobacterial PetC3 Rieske protein family.
The cyanobacterium Synechocystis PCC 6803 possesses three Rieske isoforms: PetC1, PetC2 and PetC3. While PetC1 and PetC2 have been identified as alternative subunits of the cytochrome b6f complex (b6f), PetC3 was localized exclusively within the plasma membrane. The spatial separation of PetC3 from the photosynthetic and respiratory protein complexes raises doubt in its involvement in bioenergetic electron transfer. Here we report a detailed structural and functional characterization of the cyanobacterial PetC3 protein family indicating that PetC3 is not a component of the b6f and the photosynthetic electron transport as implied by gene annotation. Instead PetC3 has a distinct function in cell envelope homeostasis. Especially proteomic analysis shows that deletion of petC3 in Synechocystis PCC 6803 primarily affects cell envelope proteins including many nutrient transport systems. Therefore, the observed downregulation in the photosynthetic electron transport - mainly caused by photosystem 2 inactivation - might constitute a stress adaptation. Comprehensive in silico sequence analyses revealed that PetC3 proteins are periplasmic lipoproteins tethered to the plasma membrane with a subclass consisting of soluble periplasmic proteins, i.e. their N-terminal domain is inconsistent with their integration into the b6f. For the first time, the structure of PetC3 was determined by X-ray crystallography at an atomic resolution revealing significant high similarities to non-b6f Rieske subunits in contrast to PetC1. These results suggest that PetC3 affects processes in the periplasmic compartment that only indirectly influence photosynthetic electron transport. For this reason, we suggest to rename "Photosynthetic electron transport Chain 3" (PetC3) proteins as "periplasmic Rieske proteins" (Prp).
Plant Biochemistry, Faculty of Biology & Biotechnology, Ruhr University of Bochum, 44780 Bochum, Germany.
Sebastian
S
Veit
Department of Chemistry, Graduate School of Science, Kyoto University, Kyoto, Japan.
Kazuki
K
Takeda
Division of Biology, Radioisotope Research Center, Kyoto University, Kyoto, Japan.
Yuichi
Y
Tsunoyama
BIP/UMR7281, FR3479, CNRS/AMU, Marseille, France.
Frauke
F
Baymann
Department of Biomolecular Sciences, Weizmann Institute of Science, 7610001, Rehovot, Israel.
Reinat
R
Nevo
Department of Biomolecular Sciences, Weizmann Institute of Science, 7610001, Rehovot, Israel.
Ziv
Z
Reich
Plant Biochemistry, Faculty of Biology & Biotechnology, Ruhr University of Bochum, 44780 Bochum, Germany.
Matthias
M
Rögner
Department of Chemistry, Graduate School of Science, Kyoto University, Kyoto, Japan. Electronic address: miki@kuchem.kyoto-u.ac.jp.
Kunio
K
Miki
Plant Biochemistry, Faculty of Biology & Biotechnology, Ruhr University of Bochum, 44780 Bochum, Germany. Electronic address: sascha.rexroth@ruhr-uni-bochum.de.
Sascha
S
Rexroth
D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002462:Cell Membrane / Q000378:metabolism*; D018360:Crystallography, X-Ray; D004579:Electron Transport; D045222:Electron Transport Chain Complex Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D004735:Energy Transfer; D006706:Homeostasis; D026901:Membrane Transport Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D008958:Models, Molecular; D019897:Periplasm / Q000378:metabolism; D010788:Photosynthesis; D010802:Phylogeny; D054730:Protein Interaction Domains and Motifs; D040901:Proteomics; D013050:Spectrometry, Fluorescence; D013329:Structure-Activity Relationship; D046939:Synechocystis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*
D001426:Bacterial Proteins; D045222:Electron Transport Chain Complex Proteins; D026901:Membrane Transport Proteins
Alternative Rieske subunit; Bacterial plasma membrane lipoprotein; Cyanobacteria; Cytochrome b(6)f complex; Electron transport; Photosynthesis