Flavodoxin with an air-stable flavin semiquinone in a green sulfur bacterium

Abstract

Flavodoxins are small proteins with a non-covalently bound FMN that can accept two electrons and accordingly adopt three redox states: oxidized (quinone), one-electron reduced (semiquinone), and two-electron reduced (quinol). In iron-deficient cyanobacteria and algae, flavodoxin can substitute for ferredoxin as the electron carrier in the photosynthetic electron transport chain. Here, we demonstrate a similar function for flavodoxin from the green sulfur bacterium Chlorobium phaeovibrioides (cp-Fld). The expression of the cp-Fld gene, found in a close proximity with the genes for other proteins associated with iron transport and storage, increased in a low-iron medium. cp-Fld produced in Escherichia coli exhibited the optical, ERP, and electron-nuclear double resonance spectra that were similar to those of known flavodoxins. However, unlike all other flavodoxins, cp-Fld exhibited unprecedented stability of FMN semiquinone to oxidation by air and difference in midpoint redox potentials for the quinone–semiquinone and semiquinone–quinol couples (− 110 and − 530 mV, respectively). cp-Fld could be reduced by pyruvate:ferredoxin oxidoreductase found in the membrane-free extract of Chl. phaeovibrioides cells and photo-reduced by the photosynthetic reaction center found in membrane vesicles from these cells. The green sulfur bacterium Chl. phaeovibrioides appears thus to be a new type of the photosynthetic organisms that can use flavodoxin as an alternative electron carrier to cope with iron deficiency.

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Abbreviations

cp-Fld, cp-Fldox, cp-Fldsq, cp-Fldred :

Flavodoxin from Chl. phaeovibrioides and its oxidized, semiquinone, and completely reduced forms, respectively

E m :

Midpoint redox potential

ENDOR:

Electron-nuclear double resonance

GSB:

Green sulfur bacteria

PFOR:

Pyruvate:ferredoxin oxidoreductase

RC:

Photosynthetic reaction center

RT-qPCR:

Quantitative reverse transcription polymerase chain reaction

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Acknowledgements

This work was supported by the Russian Science Foundation research project 19-14-00063. We are indebted to Prof. R.N. Ivanovsky for helpful discussions.

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Correspondence to Alexander V. Bogachev.

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Bertsova, Y.V., Kulik, L.V., Mamedov, M.D. et al. Flavodoxin with an air-stable flavin semiquinone in a green sulfur bacterium. Photosynth Res 142, 127–136 (2019). https://doi.org/10.1007/s11120-019-00658-1

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Keywords

  • Flavodoxin
  • Green sulfur bacteria
  • Redox titration
  • Electron transport
  • Iron deficiency
  • ENDOR