Skip to main content
Log in

Effect of the respiratory activity on photoinhibition of the cyanobacterium Synechocystis sp.

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The influence of respiratory activity on photosynthesis in Synechocystis cells that had been exposed to high light intensity was studied using distinct conditions of nitrogen supply. The photoinhibitory rate of N-sufficient cells was not influenced by the presence of different nitrogen sources. In contrast, when N-starved cells were resupplied with ammonium, they were protected from photoinhibition. Although N-starved cells presented a higher rate of dark O2 uptake than N-sufficient ones, the photoinhibitory rate increased in both cases after addition of sodium azide or sodium azide plus salicylhydroxamic acid in the photoinhibitory treatment. In the absence of the D1 protein repair mechanism, photodamage to Photosystem II was faster in N-sufficient cells than in N-starved ones. Mitigation of photodamage disappeared when the respiratory activity of N-starved cells was partially suppressed by the addition of sodium azide or sodium azide and salicylhydroxamic acid. Our results suggest that electron flow through cyanobacterial terminal oxidases can assist Photosystem I in removing electrons from the reduced plastoquinone pool, thus contributing to both reopening of Photosystem II reaction centers and avoiding photogeneration of reactive oxygen species under photoinhibitory conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen MM, Law A and Evans EH (1990) Control of photosynthesis during nitrogen depletion and recovery in a non-nitrogen-fixing cyanobacterium. Arch Microbiol 153: 428–431

    Article  CAS  Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 129–142. Bios Scientific Publications, Oxford

    Google Scholar 

  • Asada K, Kiso K and Yoshikawa K (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J Biol Chem 249: 2175–2181

    PubMed  CAS  Google Scholar 

  • Bader KP and Schmid A (1989) Photosynthetic and respiratory oxygen gas exchange measured by mass spectrometry in the filamentous cyanobacterium Oscillatoria chalibea in dependence on the nitrogen source in the growth medium. Biochim Biophys Acta 974: 303–310

    CAS  Google Scholar 

  • Berges JA, Charlebois DO, Mauzerall DC and Falkowsky PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of Photosystems I and II in microalgae. Plant Physiol 10: 689–696

    Google Scholar 

  • Büchel C, Zsiros O and Garab G (1998) Alternative cyanidesensitive oxidase interacting with photosynthesis in Synechocystis PCC 6803. Ancestor of the terminal oxidase of chlororespiration? Photosynthetica 35: 223–231

    Article  Google Scholar 

  • Campbell D and Öquist G (1996) Predicting light acclimation in cyanobacteria from non-photochemical quenching of Photosystem II fluorescence, which reflects state transitions in these organisms. Plant Physiol 111: 1293–1298

    PubMed  CAS  Google Scholar 

  • Florencio FJ, Chávez S, Muro-Pastor MI, Reyes JC, Marqués S, Mérida A and Candau P (1994) Interaction between photosynthesis and nitrogen assimilating enzymes in cyanobacteria. In: Barber J, Guerrero MG and Medrano H (eds) Trends in Photosynthesis Research, pp231–340. Intercept, Andover, UK

    Google Scholar 

  • Fresnedo O and Serra JL (1992) Effect of nitrogen starvation on the biochemistry of Phormidium laminosum (Cyanophyceae). J Phycol 28: 786–793

    Article  CAS  Google Scholar 

  • Hideg E, Spetea C and Vass I (1994) Singlet oxygen and free radical production during acceptor-and donor-side-induced photoinhibition studies with spin trapping EPR spectroscopy. Biochim Biophys Acta 1186: 143–152

    Article  CAS  Google Scholar 

  • Garbisu C, Hall DO and Serra JL (1992) Nitrate and nitrite uptake by free-living and immobilized N-starved cells of Phormidium laminosum. J Appl Phycol 4: 139–148

    Article  CAS  Google Scholar 

  • Gorham PR, Mclachlan JR, Hammer VT and Kim WK (1964) Isolation and cultures of toxics strains of Anabaena flos-aquae (Lyngb.) de Bréb. Verh-Int. Verein Theor Angew Limnol 15: 796–804

    Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG and Collier JL (1993) Environmental effects on the light-harvesting complex of cyanobacteria. J Bacteriol 175: 575–582

    PubMed  CAS  Google Scholar 

  • Guerrero MG and Lara C (1987) Assimilation of inorganic nitrogen. In: Fay P and van Baalen C (eds) The Cyanobacteria, pp 163–186. Elsevier, Amsterdam

    Google Scholar 

  • Howitt CA, Smith GD and Day DA (1993) Cyanide-insensitive oxygen uptake and pyridine nucleotide dehydrogenases in the cyanobacterium Anabaena PCC7120. Biochim Biophys Acta 1141: 313–320

    Article  CAS  Google Scholar 

  • Krause GH (1994) The role of oxygen in photoinhibition of photosynthesis. In: Foyer CH and Mullineaux PM (eds) Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, pp 43–76. CRC Press, Boca Raton, Florida

    Google Scholar 

  • Lajkó F, Kadioglu A, Borbély G and Garab G (1997) Competition between the photosynthetic and the (chloro)respiratory electron transport chains in cyanobacteria, green algae and higher plants. Effect of heat stress. Photosynthetica 33: 217–226

    Article  Google Scholar 

  • Leverenz JW, Falk S, Pilström C-M and Samuelsson G (1990) The effects of photoinhibition on the photosynthetic light-response curve of green plant cells (Chlamydomonas reinhardtii). Planta 182: 161–168

    Article  CAS  Google Scholar 

  • Macpherson AN, Telfer A, Barber J and Truscott, TG (1993) Direct detection of singlet oxygen from isolated Photosystem II reaction centers. Biochim Biophys Acta 1143: 301–309

    Article  CAS  Google Scholar 

  • McKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140: 315–322

    Google Scholar 

  • Montesinos ML, Muro-Pastor AM, Herrero A and Flores E (1998) Ammonium/methyl-ammonium permeases of cyanobacteria.J Biol Chem 273: 31463–31470

    Article  PubMed  CAS  Google Scholar 

  • Myao M (1994) Involvement of active oxygen species in degradation of the D1 protein under strong illumination in isolated sub-complexes of Photosystem II. Biochemistry 3: 9722–9730

    Article  Google Scholar 

  • Ochoa de Alda JAG, Tapia MI, Llama MJ and Serra JL (1996a) Bioenergetics processes are modified during nitrogen starvation and recovery in Phormidium laminosum (Cyanophyceae). J Phycol 32: 258–265

    Article  Google Scholar 

  • Ochoa de Alda JAG, Tapia MI, Franck F, Llama MJ and Serra JL (1996b) Changes in nitrogen source modify distribution of excitation energy in the cyanobacterium Phormidium laminosum. Physiol Plant 97: 69–78

    Article  CAS  Google Scholar 

  • Ohmori M, Oh-hama T, Furihata K and Miyachi S (1986) Effect of ammonia on cellular pH of Anabaena cylindrica determined with 31P NMR spectroscopy. Plant Cell Physiol 27: 563–566

    CAS  Google Scholar 

  • Peschek GA (1980) Electron transport reactions in respiratory particles of hydrogenase-induced Anacistis nidulans. Arch Microbiol 125: 123–131

    Article  CAS  Google Scholar 

  • Peschek GA (1987) Respiratory electron transport In: Fay P and van Baalen C (eds) The Cyanobacteria, pp 119–161. Elsevier, Amsterdam

    Google Scholar 

  • Pills D, Gregor W and Schmetterer G (1997) Evidence for in vivo activity of three distinct respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Lett 152: 83–88

    Article  Google Scholar 

  • Sandman G and Malkin R (1983) NADH and NADPH as electron donors to respiratory and photosynthetic electron transport in the blue-green alga Aphanocapsa. Biochim Biophys Acta 725:221–224

    Article  Google Scholar 

  • Scherer S, Alpes I, Sadowsky H and Böger P (1988) Ferredoxin-NAD+ oxidoreductase is the respiratory NADPH dehydrogenase of the cyanobacterium Anabaena variabilis. Arch Biochem Biophys 267: 228–235

    Article  PubMed  CAS  Google Scholar 

  • Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 409–435. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Schonbaum GR, Bonner WD, Storey BT and Bahr JT (1971) Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol 47: 124–128

    Article  PubMed  CAS  Google Scholar 

  • Schubert H, Matthijs HCP and Mur LR (1995) In vivo assay of P700 redox changes in the cyanobacterium. Fremyella diplosiphon and role of cytochrome c oxidase in regulation of photosynthetic electron transfer. Photosynthetica 31: 517–527

    CAS  Google Scholar 

  • Shyam R, Raghavendra AS and Sane PV (1993) Role of dark respiration in photoinhibition of photosynthesis and its reactivation in the cyanobacterium Anacystis nidulans. Physiol Plant 88: 446–452

    Article  CAS  Google Scholar 

  • Skillman JB and Osmond CB (1998) Influence of nitrogen supply and growth irradiance on photoinhibition and recovery in Heuchera americana (Saxifraceae). Physiol Plant 103: 567–573

    Article  CAS  Google Scholar 

  • Tapia MI, Ochoa de Alda JAG, Llama MJ and Serra JL (1996) Changes in intracellular amino acids and organic acids induced by nitrogen starvation and nitrate and ammonium resupply in the cyanobacterium Phormidium laminosum. Planta 198: 526–531

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo M. Chaloub.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Silva, L.M.T., Dos Santos, C.P. & Chaloub, R.M. Effect of the respiratory activity on photoinhibition of the cyanobacterium Synechocystis sp.. Photosynthesis Research 68, 61–69 (2001). https://doi.org/10.1023/A:1011890200229

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011890200229

Navigation