Photosynthetica

, Volume 56, Issue 1, pp 217–228 | Cite as

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

Article

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+.

Additional key words

bicarbonate depletion dissolved inorganic carbon oxygen-evolving complex redox tuning water-oxidizing complex 

Abbreviation

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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Supplementary material

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11099_2018_781_MOESM5_ESM.pdf (162 kb)
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11099_2018_781_MOESM6_ESM.pdf (155 kb)
Supplementary material, approximately 155 KB.

References

  1. Ananyev G., Dismukes G.C.: How fast can Photosystem II split water? Kinetic performance at high and low frequencies.–Photosynth. Res. 84: 355–365, 2005.CrossRefPubMedGoogle Scholar
  2. Ananyev G., Gates C., Dismukes G.C.: The oxygen quantum yield in diverse algae and cyanobacteria is controlled by partitioning of flux between linear and cyclic electron flow within photosystem II.–BBA-Bioenergetics 1857: 1380–1391, 2016.CrossRefPubMedGoogle Scholar
  3. Ananyev G., Gates C., Dismukes G.C.: Biogenesis and assembly of the CaMn4O5 core of photosynthetic water oxidases and inorganic mutants.–In: Scott R. (ed.): Metalloprotein Active Site Assembly. John Wiley & Sons, Chichester 2017.Google Scholar
  4. Ananyev G., Nguyen T., Putnam-Evans C., Dismukes G.C.: Mutagenesis of CP43-arginine-357 to serine reveals new evidence for (bi) carbonate functioning in the water oxidizing complex of photosystem II.–Photoch. Photobio. Sci. 4: 991–998, 2005.CrossRefGoogle Scholar
  5. Armstrong C.T., Mason P.E., Anderson J.R., Dempsey C.E.: Arginine side chain interactions and the role of arginine as a gating charge carrier in voltage sensitive ion channels.–Sci. Rep. 6: 21759, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Askerka M., Vinyard D.J., Brudvig G.W., Batista V.S.: NH3 Binding to the S2 state of the O2-evolving complex of photosystem II: Analogue to H2O binding during the S2→ S3 transition.–Biochemistry 54: 5783–5786, 2015.CrossRefPubMedGoogle Scholar
  7. Babcock G.T., Barry B.A., Debus R.J. et al.: Water oxidation in photosystem II: from radical chemistry to multielectron chemistry.–Biochemistry 28: 9557–9565, 1989.CrossRefPubMedGoogle Scholar
  8. Baranov S., Tyryshkin A., Katz D. et al.: Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex. Kinetics of reconstitution of O2 evolution by photoactivation.–Biochemistry 43: 2070–2079, 2004.CrossRefPubMedGoogle Scholar
  9. Brinkert K., De Causmaecker S., Krieger-Liszkay A. et al.: Bicarbonate-induced redox tuning in photosystem II for regulation and protection.–P. Natl. Acad. Sci. USA 113: 12144–12149, 2016.CrossRefGoogle Scholar
  10. Capone M., Narzi D., Bovi D., Guidoni L.: Mechanism of water delivery to the active site of photosystem II along the S2 to S3 transition.–J. Phys. Chem. Lett. 7: 592–596, 2016.CrossRefPubMedGoogle Scholar
  11. Carrieri D., Ananyev G., Brown T., Dismukes G.C.: In vivo bicarbonate requirement for water oxidation by photosystem II in the hypercarbonate-requiring cyanobacterium Arthrospira maxima.–J. Inorg. Biochem. 101: 1865–1874, 2007.CrossRefPubMedGoogle Scholar
  12. Clausen J., Beckmann K., Junge W., Messinger J.: Evidence that bicarbonate is not the substrate in photosynthetic oxygen evolution.–Plant Physiol. 139: 1444–1450, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dasgupta J., Ananyev G.M., Dismukes G.C.: Photoassembly of the water-oxidizing complex in photosystem II.–Coordin. Chem. Rev. 252: 347–360, 2008.CrossRefGoogle Scholar
  14. Dasgupta J., Tyryshkin A.M., Baranov S.V., Dismukes G.C.: Bicarbonate coordinates to Mn3+ during photo-assembly of the catalytic Mn4Ca core of photosynthetic water oxidation: EPR characterization.–Appl. Magn. Reson. 37: 137–150, 2010.CrossRefGoogle Scholar
  15. Diner B.A., Petrouleas V., Wendoloski J.J.: The iron-quinone electron-acceptor complex of photosystem II.–Physiol. Plantarum 81: 423–436, 1991.CrossRefGoogle Scholar
  16. Drake B.G., Gonzàlez-Meler M.A., Long S.P.: More efficient plants: a consequence of rising atmospheric CO2?–Annu. Rev. Plant Phys. 48: 609–639, 1997.CrossRefGoogle Scholar
  17. Ferreira K.N., Iverson T.M., Maghlaoui K. et al.: Architecture of the photosynthetic oxygen-evolving center.–Science 303: 1831–1838, 2004.CrossRefPubMedGoogle Scholar
  18. Gates C., Ananyev G., Dismukes G.C.: The strontium inorganic mutant of the water oxidizing center (CaMn4O5) of PSII improves WOC efficiency but slows electron flux through the terminal acceptors.–BBA-Bioenergetics 1857: 1550–1560, 2016.CrossRefPubMedGoogle Scholar
  19. Govindjee, van Rensen J.: Photosystem II reaction centers and bicarbonate.–In: Deisenhofer j. (ed.): Photosynthetic Reaction Centers. Pp. 357–389, Academic Press, San Diego 1993.CrossRefGoogle Scholar
  20. Hillier W., McConnell I., Badger M.R. et al.: Quantitative assessment of intrinsic carbonic anhydrase activity and the capacity for bicarbonate oxidation in photosystem II.–Biochemistry 45: 2094–2102, 2006.CrossRefPubMedGoogle Scholar
  21. Hunger J., Neueder R., Buchner R., Apelblat A.: A conductance study of guanidinium chloride, thiocyanate, sulfate, and carbonate in dilute aqueous solutions: ion-association and carbonate hydrolysis effects.–J. Phys. Chem. B 117: 615–622, 2013.CrossRefPubMedGoogle Scholar
  22. Hwang H.J., Dilbeck P., Debus R.J., Burnap R.L.: Mutation of arginine 357 of the CP43 protein of photosystem II severely impairs the catalytic S-state cycle of the H2O oxidation complex.–Biochemistry 46: 11987–11997, 2007.CrossRefPubMedGoogle Scholar
  23. Ippolito J.A., Alexander R.S., Christianson D.W.: Hydrogen bond stereochemistry in protein structure and function.–J. Mol. Biol. 215: 457–471, 1990.CrossRefPubMedGoogle Scholar
  24. Khorobrykh A., Dasgupta J., Kolling D.R. et al.: Evolutionary origins of the photosynthetic water oxidation cluster: bicarbonate permits Mn2+ photo-oxidation by anoxygenic bacterial reaction centers.–Chem. Bio. Chem. 14: 1725–1731, 2013.CrossRefPubMedGoogle Scholar
  25. Klimov V.V., Allakhverdiev S.I., Feyziev Y.M., Baranov S.V.: Bicarbonate requirement for the donor side of photosystem II.–FEBS Lett. 363: 251–255, 1995.CrossRefPubMedGoogle Scholar
  26. Klimov V., Baranov S.: Bicarbonate requirement for the wateroxidizing complex of photosystem II.–BBA-Bioenergetics 1503: 187–196, 2001.CrossRefPubMedGoogle Scholar
  27. Kolber Z.S., Prášil O., Falkowski P.G.: Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols.–BBABioenergetics 1367: 88–106, 1998.CrossRefGoogle Scholar
  28. Koroidov S., Shevela D., Shutova T. et al.: Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation.–P. Natl. Acad. Sci. USA 111: 6299–6304, 2014.CrossRefGoogle Scholar
  29. Kuriata A.M., Chakraborty M., Henderson J.N. et al: ATP and magnesium promote cotton short-form ribulose-1, 5- bisphosphate carboxylase/oxygenase (Rubisco) activase hexamer formation at low micromolar concentrations.–Biochemistry 53: 7232–7246, 2014.CrossRefPubMedGoogle Scholar
  30. Lubitz W., Cox N., Rapatskiy L. et al.: Light-induced water oxidation in photosynthesis.–J. Biol. Inorg. Chem. 19: S350–S350, 2014.Google Scholar
  31. Roach T., Sedoud A., Krieger-Liszkay A.: Acetate in mixotrophic growth medium affects photosystem II in Chlamydomonas reinhardtii and protects against photoinhibition.–BBABioenergetics 1827: 1183–1190, 2013.CrossRefGoogle Scholar
  32. Rutherford A.W., Govindjee, Inoue Y.: Charge accumulation and photochemistry in leaves studied by thermo-luminescence and delayed light-emission.–P. Natl. Acad. Sci. USA 81: 1107–1111, 1984.CrossRefGoogle Scholar
  33. Shen J.-R.: The structure of photosystem II and the mechanism of water oxidation in photosynthesis.–Annu. Rev. Plant Biol. 66: 23–48, 2015.CrossRefPubMedGoogle Scholar
  34. Shevela D., Eaton-Rye J.J., Shen J.-R., Govindjee: Photosystem II and the unique role of bicarbonate: A historical perspective.–BBA-Bioenergetics 1817: 1134–1151, 2012.CrossRefPubMedGoogle Scholar
  35. Shevela D., Su J.-H., Klimov V., Messinger J.: Hydrogencarbonate is not a tightly bound constituent of the wateroxidizing complex in photosystem II.–BBA-Bioenergetics 1777: 532–539, 2008.CrossRefPubMedGoogle Scholar
  36. Snel J.F.H., van Rensen J.J.S.: Reevaluation of the role of electron flow in broken chloroplasts.–Plant Physiol. 75: 146–150, 1984.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Stemler A.: Inhibition of photosystem II by formate. Possible evidence for a direct bicarbonate and formate in the regulation of photosynthetic role of bicarbonate in photosynthetic oxygen evolution.–BBA-Bioenergetics 593: 103–112, 1980.CrossRefPubMedGoogle Scholar
  38. Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient.–J. Photoch. Photobio. B 104: 236–257, 2011.CrossRefGoogle Scholar
  39. van Rensen J.J.S., Tonk W.J.M., de Bruijn S.M.: Involvement of bicarbonate in the protonation of the secondary quinone electron acceptor of photosystem II via the non-haem iron of the quinone-iron acceptor complex.–FEBS Lett. 226: 347–351, 1988.CrossRefGoogle Scholar
  40. van Rensen J.J.S., Xu C., Govindjee: Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis.–Physiol. Plantarum 105: 585–592, 1999.CrossRefGoogle Scholar
  41. Vermaas W.F., Rutherford A.W.: EPR measurements on the effects of bicarbonate and triazine resistance on the acceptor side of photosystem II.–FEBS Lett. 175: 243–248, 1984.CrossRefGoogle Scholar
  42. Vinyard D.J., Zachary C.E., Ananyev G., Dismukes G.C.: Thermodynamically accurate modeling of the catalytic cycle of photosynthetic oxygen evolution: A mathematical solution to asymmetric Markov chains.–BBA-Bioenergetics 1827: 861–868, 2013.CrossRefPubMedGoogle Scholar
  43. Vogt L., Ertem M.Z., Pal R. et al.: Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca2+ or Ca2+ substituted by Sr2+.–Biochemistry 54: 820–825, 20CrossRefPubMedGoogle Scholar
  44. Vonshak A., Tomaselli L.: Arthrospira (Spirulina): systematics and ecophysiology.–In: Whitton B.A.(ed.): The Ecology of Cyanobacteria. Pp. 505–522. Springer, Dordrecht 2000Google Scholar
  45. Wincencjusz H., van Gorkom H.J., Yocum C.F.: The photosynthetic oxygen evolving complex requires chloride for its redox state S2→ S3 and S3→ S0 transitions but not for S0→ S1 or S1→ S2 transitions.–Biochemistry 36: 3663–3670, 1997.CrossRefPubMedGoogle Scholar
  46. Wydrzynski T., Govindjee: A new site of bicarbonate effect in photosystem II of photosynthesis: Evidence from chlorophyll fluorescence transients in spinach chloroplasts.–BBABioenergetics 387: 403–408, 1975.CrossRefGoogle Scholar
  47. Zarrouk C.: [Contribution to the study of Cyanophyceae, influence of various physical and chemical factors on growth and photosynthesis of Spirulina maxima (Setch and Gardner) Geitler.]–J. Univ de Paris, 1966. [In French]Google Scholar
  48. Zhang H., Joseph J., Gurney M., et al.: Bicarbonate enhances peroxidase activity of Cu, Zn-superoxide dismutase role of carbonate anion radical and scavenging of carbonate anion radical by metalloporphyrin antioxidant enzyme mimetics.–J. Biol. Chem. 277: 1013–1020, 2002.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.The Waksman Institute of MicrobiologyRutgers UniversityPiscatawayUSA
  2. 2.Department of Chemistry and Chemical BiologyRutgers UniversityPiscatawayUSA

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