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The multiplicity of roles for (bi)carbonate in photosystem II operation in the hypercarbonate-requiring cyanobacterium Arthrospira maxima

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Photosynthetica

Abstract

Arthrospira maxima is unique among cyanobacteria, growing at alkaline pH (<11) in concentrated (bi)carbonate (1.2 M saturated) and lacking carbonic anhydrases. We investigated dissolved inorganic carbon (DIC) roles within PSII of A. maxima cells oximetrically and fluorometrically, monitoring the light reactions on the donor and acceptor sides of PSII. We developed new methods for removing DIC based on a (bi)carbonate chelator and magnesium for (bi)carbonate ionpairing. We established relative affinities of three sites: the water-oxidizing complex (WOC), non-heme iron/QA–, and solvent-accessible arginines throughout PSII. Full reversibility is achieved but (bi)carbonate uptake requires light. DIC depletion at the non-heme iron site and solvent-accessible arginines greatly reduces the yield of O2 due to O2 uptake, but accelerates the PSII–WOC cycle, specifically the S2→S3 and S3→S0 transitions. DIC removal from the WOC site abolishes water oxidation and appears to influence free energy stabilization of the WOC from a site between CP43-R357 and Ca2+.

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Abbreviations

alpha:

miss

beta:

double hit

Chl:

chlorophyll

delta:

backward transition

DIC:

dissolved inorganic carbon

DMBQ:

2,5-dimethyl-p-benzoquinone

epsilon:

deactivation

F0 :

minimal fluorescence yield of the dark-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

FRRF:

fast repetition rate fluorometry

Fv :

variable fluorescence

Fv/Fm :

maximal quantum yield of PSII photochemistry

PET:

photosynthetic electron transport

PQ:

plastoquinone

S0–S4:

oxidation states of the WOC, “S-states”

VZAD (model):

Vinyard-Zachary-Ananyev-Dismukes model

WOC:

water oxidizing complex

YSS :

steady-state yield

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Authors and Affiliations

  1. The Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA

    G. Ananyev, C. Gates & G. C. Dismukes

  2. Department of Chemistry and Chemical Biology, Rutgers University, Piscataway, NJ, 08854, USA

    G. Ananyev, C. Gates & G. C. Dismukes

Authors
  1. G. Ananyev
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  2. C. Gates
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  3. G. C. Dismukes
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Correspondence to G. C. Dismukes.

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Dedicated to Prof. Govindjee on the occasion of his 85th birthday.

Acknowledgements: This work was funded by the Department of Energy, Basic Energy Sciences, Grant DE-FG02-10ER16195, and by the Stanford University Global Climate and Energy Project, activity number 96. We thank Dr. Dmitry Shevela for constructive advice and previous research, Prof. A. W. Rutherford for research which provided a foundation for our own work, and Prof. Govindjee for a long lifetime of progress on this subject and a great deal of prior advice.

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Ananyev, G., Gates, C. & Dismukes, G.C. The multiplicity of roles for (bi)carbonate in photosystem II operation in the hypercarbonate-requiring cyanobacterium Arthrospira maxima. Photosynthetica 56, 217–228 (2018). https://doi.org/10.1007/s11099-018-0781-0

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