Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp. strain PCC 6803

In cyanobacteria, photorespiratory 2-phosphoglycolate (2PG) metabolism is mediated by three different routes, including one route involving the glycine decarboxylase complex (Gcv). It has been suggested that, in addition to conversion of 2PG into non-toxic intermediates, this pathway is important for acclimation to high-light. The photoreduction of O2 (Mehler reaction), which is mediated by two flavoproteins Flv1 and Flv3 in cyanobacteria, dissipates excess reductants under high-light by the four electron-reduction of oxygen to water. Single and double mutants defective in these processes were constructed to investigate the relation between photorespiratory 2PG-metabolism and the photoreduction of O2 in the cyanobacterium Synechocystis sp. PCC 6803. The single mutants Δflv1, Δflv3, and ΔgcvT, as well as the double mutant Δflv1/ΔgcvT, were completely segregated but not the double mutant Δflv3/ΔgcvT, suggesting that the T-protein subunit of the Gcv (GcvT) and Flv3 proteins cooperate in an essential process. This assumption is supported by the following results: (1) The mutant Δflv3/ΔgcvT showed a considerable longer lag phase and sometimes bleached after shifts from slow (low light, air CO2) to rapid (standard light, 5% CO2) growing conditions. (2) Photoinhibition experiments indicated a decreased ability of the mutant Δflv3/ΔgcvT to cope with high-light. (3) Fluorescence measurements showed that the photosynthetic electron chain is reduced in this mutant. Our data suggest that the photorespiratory 2PG-metabolism and the photoreduction of O2, particularly that catalyzed by Flv3, cooperate during acclimation to high-light stress in cyanobacteria.

[1]  W. Martin,et al.  Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. , 2008, Molecular biology and evolution.

[2]  G. Krause,et al.  Chlorophyll Fluorescence and Photosynthesis: The Basics , 1991 .

[3]  R. Leegood,et al.  Photorespiration: metabolic pathways and their role in stress protection. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  A. Mehler.  Studies on reactions of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. , 1951, Archives of biochemistry and biophysics.

[5]  W. Ogren.  Photorespiration: Pathways, Regulation, and Modification , 1984 .

[6]  M. Kanehisa,et al.  Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp. PCC 6803. , 2004, Plant & cell physiology.

[7]  K. Asada,et al.  Quenching Analysis of Chlorophyll Fluorescence by the Saturation Pulse Method: Particular Aspects Relating to the Study of Eukaryotic Algae and Cyanobacteria , 1995 .

[8]  H. Bauwe,et al.  Genetic manipulation of glycine decarboxylation. , 2003, Journal of experimental botany.

[9]  D. Casamatta.  The Cyanobacteria: Molecular Biology, Genomics and Evolution. , 2008 .

[10]  Hong-liang Wang,et al.  Polymerase chain reaction‐based mutageneses identify key transporters belonging to multigene families involved in Na+ and pH homeostasis of Synechocystis sp. PCC 6803 , 2002, Molecular microbiology.

[11]  D. Campbell,et al.  Chlorophyll Fluorescence Analysis of Cyanobacterial Photosynthesis and Acclimation , 1998, Microbiology and Molecular Biology Reviews.

[12]  Y. Jouanneau,et al.  A family of flavoproteins in the domains Archaea and Bacteria. , 1998, European journal of biochemistry.

[13]  Aaron Kaplan,et al.  Supplementary Experimental Procedures Organisms and Growth Conditions , 2022 .

[14]  J. Raven,et al.  CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. , 2005, Annual review of plant biology.

[15]  B. Ibelings,et al.  Long-Term Response toward Inorganic Carbon Limitation in Wild Type and Glycolate Turnover Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 68031[W] , 2007, Plant Physiology.

[16]  E. Aro,et al.  Flavodiiron Proteins in Oxygenic Photosynthetic Organisms: Photoprotection of Photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803 , 2009, PloS one.

[17]  T. Ogawa,et al.  Two Types of Functionally Distinct NAD(P)H Dehydrogenases inSynechocystis sp. Strain PCC6803* , 2000, The Journal of Biological Chemistry.

[18]  M. Hagemann,et al.  The glycine decarboxylase complex is not essential for the cyanobacterium Synechocystis sp. strain PCC 6803. , 2005, Plant biology.

[19]  A. Kozaki,et al.  Photorespiration protects C3 plants from photooxidation , 1996, Nature.

[20]  J. Snel,et al.  The use of chlorophyll fluorescence nomenclature in plant stress physiology , 1990, Photosynthesis Research.

[21]  Peter Lindblad,et al.  An AbrB-Like Protein Regulates the Expression of the Bidirectional Hydrogenase in Synechocystis sp. Strain PCC 6803 , 2007, Journal of bacteriology.

[22]  Aaron Kaplan,et al.  The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants , 2008, Proceedings of the National Academy of Sciences.

[23]  H. Scheller,et al.  Photoinhibition of photosystem I , 2005, Planta.

[24]  D. Kirilovsky.  Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism , 2007, Photosynthesis Research.

[25]  H. Matthijs,et al.  The chlorophyll‐binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress , 2005, FEBS letters.

[26]  A. Kaplan,et al.  The Plant-Like C 2 Glycolate Cycle and the Bacterial-Like Glycerate Pathway Cooperate in Phosphoglycolate Metabolism in Cyanobacteria 1 , 2006 .

[27]  E. Flores,et al.  The cyanobacteria : molecular biology, genomics, and evolution , 2008 .

[28]  Y. Hihara,et al.  DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light , 2001, Plant Cell.

[29]  Aaron Kaplan,et al.  Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings , 2004, Photosynthesis Research.

[30]  M. Badger,et al.  Journal of Experimental Botany Advance Access published October 10, 2005 Journal of Experimental Botany, Page 1 of 17 Phenotypic Plasticity and the Changing Environment Special Issue , 2005 .

[31]  L. Sherman,et al.  Microarray Analysis of the Genome-Wide Response to Iron Deficiency and Iron Reconstitution in the Cyanobacterium Synechocystis sp. PCC 68031[w] , 2003, Plant Physiology.

[32]  B. Colman.  Photosynthetic carbon assimilation and the suppression of photorespiration in the cyanobacteria , 1989 .

[33]  A. Kaplan,et al.  The Plant-Like C2 Glycolate Cycle and the Bacterial-Like Glycerate Pathway Cooperate in Phosphoglycolate Metabolism in Cyanobacteria1 , 2006, Plant Physiology.

[34]  C. Osmond.  Photorespiration and photoinhibition: Some implications for the energetics of photosynthesis , 1981 .

[35]  M. Badger,et al.  Impairment of the Photorespiratory Pathway Accelerates Photoinhibition of Photosystem II by Suppression of Repair But Not Acceleration of Damage Processes in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[36]  Miguel Teixeira,et al.  Structure of a dioxygen reduction enzyme from Desulfovibrio gigas , 2000, Nature Structural Biology.

[37]  J. B. Vicente,et al.  Biochemical, spectroscopic, and thermodynamic properties of flavodiiron proteins. , 2008, Methods in enzymology.

[38]  S. Allakhverdiev,et al.  Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery , 2001, The EMBO journal.

[39]  J. Appel,et al.  LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator , 2005, Molecular microbiology.

[40]  Hong-liang Wang,et al.  Alterations in Global Patterns of Gene Expression in Synechocystis sp. PCC 6803 in Response to Inorganic Carbon Limitation and the Inactivation of ndhR, a LysR Family Regulator* , 2004, Journal of Biological Chemistry.

[41]  J. Waterbury,et al.  Generic assignments, strain histories, and properties of pure cultures of cyanobacteria , 1979 .

[42]  Aaron Kaplan,et al.  Fractionation of the Three Stable Oxygen Isotopes by Oxygen-Producing and Oxygen-Consuming Reactions in Photosynthetic Organisms1[w] , 2005, Plant Physiology.

[43]  J. B. Vicente,et al.  Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. , 2002, Biochemical and biophysical research communications.

[44]  C. Kerfeld,et al.  A Soluble Carotenoid Protein Involved in Phycobilisome-Related Energy Dissipation in Cyanobacteria , 2006, The Plant Cell Online.

[45]  S. Ruuska,et al.  Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  E. Aro,et al.  Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. , 1993, Biochimica et biophysica acta.

[47]  N. Tolbert.  THE C2 OXIDATIVE PHOTOSYNTHETIC CARBON CYCLE. , 1997, Annual review of plant physiology and plant molecular biology.

[48]  Expression of two nblA-homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803. , 2001, FEMS microbiology letters.

[49]  J. Moroney,et al.  CO2 Concentrating Mechanisms , 2007 .

[50]  K. Forchhammer,et al.  Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors. , 2000, Microbiology.

[51]  A. Kaplan,et al.  CO2 CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS. , 1999, Annual review of plant physiology and plant molecular biology.

[52]  K. Asada,et al.  THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. , 1999, Annual review of plant physiology and plant molecular biology.

[53]  E. Zuther,et al.  The stpA gene form synechocystis sp. strain PCC 6803 encodes the glucosylglycerol-phosphate phosphatase involved in cyanobacterial osmotic response to salt shock , 1997, Journal of bacteriology.