Crystal structure and redox properties of a novel cyanobacterial heme protein with a His/Cys heme axial ligation and a Per-Arnt-Sim (PAS)-like domain

Taiki Motomura, Michihiro Suga, Rainer Hienerwadel, Akiko Nakagawa, Thanh Lan Lai, Wolfgang Nitschke, Takahiro Kuma, Miwa Sugiura, Alain Boussac, Jian-Ren Shen

Research output: Contribution to journalArticle

Abstract

Photosystem II catalyzes light-induced water oxidation leading to the generation of dioxygen indispensable for sustaining aerobic life on Earth. The Photosystem II reaction center is composed of D1 and D2 proteins encoded by psbA and psbD genes, respectively. In cyanobacteria, different psbA genes are present in the genome. The thermophilic cyanobacterium Thermosynechococcus elongatus contains three psbA genes: psbA1, psbA2, and psbA3, and a new c-type heme protein, Tll0287, was found to be expressed in a strain expressing the psbA2 gene only, but the structure and function of Tll0287 are unknown. Here we solved the crystal structure of Tll0287 at a 2.0 Å resolution. The overall structure of Tll0287 was found to be similar to some kinases and sensor proteins with a Per-Arnt-Sim-like domain rather than to other c-type cytochromes. The fifth and sixth axial ligands for the heme were Cys and His, instead of the His/ Met or His/His ligand pairs observed for most of the c-type hemes. The redox potential, E12, of Tll0287 was 255 ± 20 mV versus normal hydrogen electrode at pH values above 7.5. Below this pH value, the E12 increased by ≈57 mV/pH unit at 15 °C, suggesting the involvement of a protonatable group with a pKred 7.2 ± 0.3. Possible functions of Tll0287 as a redox sensor under microaerobic conditions or a cytochrome subunit of an H2S-oxidizing system are discussed in view of the environmental conditions in which psbA2 is expressed, as well as phylogenetic analysis, structural, and sequence homologies.

Original languageEnglish
Pages (from-to)9599-9612
Number of pages14
JournalJournal of Biological Chemistry
Volume292
Issue number23
DOIs
Publication statusPublished - 2017

Fingerprint

Hemeproteins
Heme
Oxidation-Reduction
Ligation
Genes
Crystal structure
Photosystem II Protein Complex
Cyanobacteria
Cytochrome c Group
Ligands
Cytochromes
Sequence Homology
Protein Kinases
Sensors
Hydrogen
Electrodes
Structural analysis
Genome
Oxygen
Light

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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Crystal structure and redox properties of a novel cyanobacterial heme protein with a His/Cys heme axial ligation and a Per-Arnt-Sim (PAS)-like domain. / Motomura, Taiki; Suga, Michihiro; Hienerwadel, Rainer; Nakagawa, Akiko; Lai, Thanh Lan; Nitschke, Wolfgang; Kuma, Takahiro; Sugiura, Miwa; Boussac, Alain; Shen, Jian-Ren.

In: Journal of Biological Chemistry, Vol. 292, No. 23, 2017, p. 9599-9612.

Research output: Contribution to journalArticle

Motomura, Taiki ; Suga, Michihiro ; Hienerwadel, Rainer ; Nakagawa, Akiko ; Lai, Thanh Lan ; Nitschke, Wolfgang ; Kuma, Takahiro ; Sugiura, Miwa ; Boussac, Alain ; Shen, Jian-Ren. / Crystal structure and redox properties of a novel cyanobacterial heme protein with a His/Cys heme axial ligation and a Per-Arnt-Sim (PAS)-like domain. In: Journal of Biological Chemistry. 2017 ; Vol. 292, No. 23. pp. 9599-9612.
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abstract = "Photosystem II catalyzes light-induced water oxidation leading to the generation of dioxygen indispensable for sustaining aerobic life on Earth. The Photosystem II reaction center is composed of D1 and D2 proteins encoded by psbA and psbD genes, respectively. In cyanobacteria, different psbA genes are present in the genome. The thermophilic cyanobacterium Thermosynechococcus elongatus contains three psbA genes: psbA1, psbA2, and psbA3, and a new c-type heme protein, Tll0287, was found to be expressed in a strain expressing the psbA2 gene only, but the structure and function of Tll0287 are unknown. Here we solved the crystal structure of Tll0287 at a 2.0 {\AA} resolution. The overall structure of Tll0287 was found to be similar to some kinases and sensor proteins with a Per-Arnt-Sim-like domain rather than to other c-type cytochromes. The fifth and sixth axial ligands for the heme were Cys and His, instead of the His/ Met or His/His ligand pairs observed for most of the c-type hemes. The redox potential, E12, of Tll0287 was 255 ± 20 mV versus normal hydrogen electrode at pH values above 7.5. Below this pH value, the E12 increased by ≈57 mV/pH unit at 15 °C, suggesting the involvement of a protonatable group with a pKred 7.2 ± 0.3. Possible functions of Tll0287 as a redox sensor under microaerobic conditions or a cytochrome subunit of an H2S-oxidizing system are discussed in view of the environmental conditions in which psbA2 is expressed, as well as phylogenetic analysis, structural, and sequence homologies.",
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AU - Lai, Thanh Lan

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AB - Photosystem II catalyzes light-induced water oxidation leading to the generation of dioxygen indispensable for sustaining aerobic life on Earth. The Photosystem II reaction center is composed of D1 and D2 proteins encoded by psbA and psbD genes, respectively. In cyanobacteria, different psbA genes are present in the genome. The thermophilic cyanobacterium Thermosynechococcus elongatus contains three psbA genes: psbA1, psbA2, and psbA3, and a new c-type heme protein, Tll0287, was found to be expressed in a strain expressing the psbA2 gene only, but the structure and function of Tll0287 are unknown. Here we solved the crystal structure of Tll0287 at a 2.0 Å resolution. The overall structure of Tll0287 was found to be similar to some kinases and sensor proteins with a Per-Arnt-Sim-like domain rather than to other c-type cytochromes. The fifth and sixth axial ligands for the heme were Cys and His, instead of the His/ Met or His/His ligand pairs observed for most of the c-type hemes. The redox potential, E12, of Tll0287 was 255 ± 20 mV versus normal hydrogen electrode at pH values above 7.5. Below this pH value, the E12 increased by ≈57 mV/pH unit at 15 °C, suggesting the involvement of a protonatable group with a pKred 7.2 ± 0.3. Possible functions of Tll0287 as a redox sensor under microaerobic conditions or a cytochrome subunit of an H2S-oxidizing system are discussed in view of the environmental conditions in which psbA2 is expressed, as well as phylogenetic analysis, structural, and sequence homologies.

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