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Photosynthesis Research

, Volume 139, Issue 1–3, pp 281–293 | Cite as

Properties and structure of a low-potential, penta-heme cytochrome c552 from a thermophilic purple sulfur photosynthetic bacterium Thermochromatium tepidum

  • Jing-Hua Chen
  • Long-Jiang Yu
  • Alain Boussac
  • Zheng-Yu Wang-Otomo
  • Tingyun Kuang
  • Jian-Ren ShenEmail author
Original Article
First Online:
  • 164 Downloads

Abstract

The thermophilic purple sulfur bacterium Thermochromatium tepidum possesses four main water-soluble redox proteins involved in the electron transfer behavior. Crystal structures have been reported for three of them: a high potential iron–sulfur protein, cytochrome c′, and one of two low-potential cytochrome c552 (which is a flavocytochrome c) have been determined. In this study, we purified another low-potential cytochrome c552 (LPC), determined its N-terminal amino acid sequence and the whole gene sequence, characterized it with absorption and electron paramagnetic spectroscopy, and solved its high-resolution crystal structure. This novel cytochrome was found to contain five c-type hemes. The overall fold of LPC consists of two distinct domains, one is the five heme-containing domain and the other one is an Ig-like domain. This provides a representative example for the structures of multiheme cytochromes containing an odd number of hemes, although the structures of multiheme cytochromes with an even number of hemes are frequently seen in the PDB database. Comparison of the sequence and structure of LPC with other proteins in the databases revealed several characteristic features which may be important for its functioning. Based on the results obtained, we discuss the possible intracellular function of this LPC in Tch. tepidum.

Keywords

Purple sulfur bacteria Electron transfer Cytochrome c Multiheme Crystal structure Thermochromatium tepidum 

Abbreviations

AMO

Ammonia monooxygenase

Cyt

Cytochrome

DaCld

Chloride dismutase

DTT

Dithiothreitol

EPR

Electron paramagnetic resonance

HAO

Hydroxylamine oxidoreductase

HiPIP

High potential iron–sulfur protein

LPC

Low-potential cytochrome

MHC

Multiheme cytochrome c

Nrf

Nitrite reductase

SAD

Single wavelength anomalous diffraction

Tch

Thermochromatium

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Notes

Acknowledgements

The authors thank Drs. M. Suga and Y. Umena for their help in the structural analysis of LPC, Dr. Y. Kashino for his help in identifying the LPC in the early stage of this work, Dr. M. T. Madigan for providing the Tch. tepidum strain, the staff members at beamlines BL41XU and BL26B1 of SPring-8 for their help in data collection, and the staff members of the Faculty of Science, Okayama University for their help in N-terminal sequencing and DNA sequencing experiments. This work was supported by the National Key R&D Program of China (2017YFA0503700), a Strategic Priority Research Program of CAS (XDB17000000), a CAS Key Research Project for Frontier Science (QYZDY-SSW-SMC003), and a JSPS KAKENHI Grant Number JP17H06433. JHC acknowledges the financial support provided by China Scholarship Council (CSC). AB was supported in part by the French Infrastructure for Integrated Structural Biology (FRISBI) ANR-10-INBS-05. The sequences were deposited in GenBank under the Accession Number MH000336, and the coordinate and the structure factors were deposited in the Protein Data Bank under Accession Number 5ZE8.

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Jing-Hua Chen
    • 1
    • 2
    • 3
  • Long-Jiang Yu
    • 2
  • Alain Boussac
    • 4
  • Zheng-Yu Wang-Otomo
    • 5
  • Tingyun Kuang
    • 1
  • Jian-Ren Shen
    • 1
    • 2
    Email author
  1. 1.Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of BotanyChinese Academy of SciencesBeijingChina
  2. 2.Research Institute for Interdisciplinary Science, Graduate School of Natural Science and TechnologyOkayama UniversityOkayamaJapan
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.I2BC, SB2SM, CNRS UMR 9198, CEA SaclayGif-sur-YvetteFrance
  5. 5.Faculty of ScienceIbaraki UniversityMitoJapan

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