Modulation of the fluorescence yield in heliobacterial cells by induction of charge recombination in the photosynthetic reaction center

Kevin Edward Redding, Iosifina Sarrou, Fabrice Rappaport, Stefano Santabarbara, Su Lin, Kiera T. Reifschneider

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Heliobacteria contain a very simple photosynthetic apparatus, consisting of a homodimeric type I reaction center (RC) without a peripheral antenna system and using the unique pigment bacteriochlorophyll (BChl) g. They are thought to use a light-driven cyclic electron transport pathway to pump protons, and thereby phosphorylate ADP, although some of the details of this cycle are yet to be worked out. We previously reported that the fluorescence emission from the heliobacterial RC in vivo was increased by exposure to actinic light, although this variable fluorescence phenomenon exhibited very different characteristics to that in oxygenic phototrophs (Collins et al. 2010). Here, we describe the underlying mechanism behind the variable fluorescence in heliobacterial cells. We find that the ability to stably photobleach P800, the primary donor of the RC, using brief flashes is inversely correlated to the variable fluorescence. Using pump-probe spectroscopy in the nanosecond timescale, we found that illumination of cells with bright light for a few seconds put them in a state in which a significant fraction of the RCs underwent charge recombination from P800 +A0 - with a time constant of ∼20 ns. The fraction of RCs in the rapidly back-reacting state correlated very well with the variable fluorescence, indicating that nearly all of the increase in fluorescence could be explained by charge recombination of P800 +A0 -, some of which regenerated the singlet excited state. This hypothesis was tested directly by time-resolved fluorescence studies in the ps and ns timescales. The major decay component in whole cells had a 20-ps decay time, representing trapping by the RC. Treatment of cells with dithionite resulted in the appearance of a ∼18-ns decay component, which accounted for ∼0.6 % of the decay, but was almost undetectable in the untreated cells. We conclude that strong illumination of heliobacterial cells can result in saturation of the electron acceptor pool, leading to reduction of the acceptor side of the RC and the creation of a back-reacting RC state that gives rise to delayed fluorescence.

Original languageEnglish
Pages (from-to)221-235
Number of pages15
JournalPhotosynthesis Research
Volume120
Issue number1-2
DOIs
Publication statusPublished - 2014

Fingerprint

photosynthetic reaction centers
Photosynthetic Reaction Center Complex Proteins
Genetic Recombination
Fluorescence
Modulation
fluorescence
deterioration
cells
Lighting
Light
lighting
Heliobacteriaceae
Bacteriochlorophylls
Dithionite
Proton Pumps
proton pump
autotrophs
Electron Transport
Excited states
Pigments

Keywords

  • Fluorescence
  • Heliobacteria
  • Type I reaction center

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology
  • Biochemistry
  • Medicine(all)

Cite this

Modulation of the fluorescence yield in heliobacterial cells by induction of charge recombination in the photosynthetic reaction center. / Redding, Kevin Edward; Sarrou, Iosifina; Rappaport, Fabrice; Santabarbara, Stefano; Lin, Su; Reifschneider, Kiera T.

In: Photosynthesis Research, Vol. 120, No. 1-2, 2014, p. 221-235.

Research output: Contribution to journalArticle

Redding, Kevin Edward ; Sarrou, Iosifina ; Rappaport, Fabrice ; Santabarbara, Stefano ; Lin, Su ; Reifschneider, Kiera T. / Modulation of the fluorescence yield in heliobacterial cells by induction of charge recombination in the photosynthetic reaction center. In: Photosynthesis Research. 2014 ; Vol. 120, No. 1-2. pp. 221-235.
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AB - Heliobacteria contain a very simple photosynthetic apparatus, consisting of a homodimeric type I reaction center (RC) without a peripheral antenna system and using the unique pigment bacteriochlorophyll (BChl) g. They are thought to use a light-driven cyclic electron transport pathway to pump protons, and thereby phosphorylate ADP, although some of the details of this cycle are yet to be worked out. We previously reported that the fluorescence emission from the heliobacterial RC in vivo was increased by exposure to actinic light, although this variable fluorescence phenomenon exhibited very different characteristics to that in oxygenic phototrophs (Collins et al. 2010). Here, we describe the underlying mechanism behind the variable fluorescence in heliobacterial cells. We find that the ability to stably photobleach P800, the primary donor of the RC, using brief flashes is inversely correlated to the variable fluorescence. Using pump-probe spectroscopy in the nanosecond timescale, we found that illumination of cells with bright light for a few seconds put them in a state in which a significant fraction of the RCs underwent charge recombination from P800 +A0 - with a time constant of ∼20 ns. The fraction of RCs in the rapidly back-reacting state correlated very well with the variable fluorescence, indicating that nearly all of the increase in fluorescence could be explained by charge recombination of P800 +A0 -, some of which regenerated the singlet excited state. This hypothesis was tested directly by time-resolved fluorescence studies in the ps and ns timescales. The major decay component in whole cells had a 20-ps decay time, representing trapping by the RC. Treatment of cells with dithionite resulted in the appearance of a ∼18-ns decay component, which accounted for ∼0.6 % of the decay, but was almost undetectable in the untreated cells. We conclude that strong illumination of heliobacterial cells can result in saturation of the electron acceptor pool, leading to reduction of the acceptor side of the RC and the creation of a back-reacting RC state that gives rise to delayed fluorescence.

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