Abstract
Cyanobacteria have versatile electron transfer pathways and many of the proteins involved are functional in both respiratory and photosynthetic electron transport. Examples of such proteins include the cytochrome b 6 f complex, NADH dehydrogenase and cytochrome oxidase complexes. In this study we have cloned and sequenced two gene clusters from the marine cyanobacterium Synechococcus sp. PCC 7002 that potentially encode heme-copper cytochrome oxidases. The ctaCIDIEI and ctaCIIDIIEII gene clusters are most similar to two related gene clusters found in the freshwater cyanobacterial strain Synechocystis sp. PCC 6803. Unlike Synechocystis sp. PCC 6803, Synechococcus sp. PCC 7002 does not have a cydAB-like gene cluster which encodes a quinol oxidase. The ctaCIDIEI and ctaCIIDIIEII gene clusters were transcribed polycistronically, although the levels of transcripts for the ctaCIIDIIEII gene cluster were lower than those of the ctaCIDIEI gene cluster. The ctaDI and ctaDII coding sequences were interrupted by interposon mutagenesis and full segregants were isolated and characterized for both single and double mutants. Growth rates, chlorophyll and carotenoid contents, oxygen consumption and oxygen evolution were examined in the wild type and mutant strains. Differences between the wild type and mutant strains observed in 77 K fluorescence spectra and in pulse-amplified modulated (PAM) fluorescence studies suggest that the cyanobacterial oxidases play a role in photoinhibition and high light tolerance in Synechococcus sp. PCC 7002.
Similar content being viewed by others
Abbreviations
- DCMU:
-
3-(3′, 4′-dichlorophyneyl)-1,1-dimethylurea
- HEPES:
-
N-(2-hydroxyethyl) piperazine-N′-(2-ethanesulfonic acid)
- PS I:
-
Photosystem I
- PS II:
-
Photosystem II
References
D Alge and GA Peschek, Characterization of a cta/CDE operon-like genomic region encoding subunits I–III of the cytochrome c oxidase of the cyanobacterium Synechocystis PCC 6803. Biochem Mol Biol Int 29 (1993a) 511-525
D Alge and GA Peschek, Identification and characterization of the ctaC (coxB) gene as part of an operon encoding subunits I, II, and III of the cytochrome c oxidase (cytochrome aa 3) in the cyanobacterium Synechocystis PCC 6803. Biochem Biophys Res Commun 191 (1993b) 9-17
FM Ausubel, R Brent, RE Kingston, DD Moore, JG Seidman, JA Smith and K Struhl, Current Protocols in Molecular Biology. New York: Wiley (1987).
S Berry, D Schneider, WF Vermaas and M Rogner, Electron transport routes in whole cells of Synechocystis sp. strain PCC 6803: the role of the cytochrome bd-type oxidase. Biochemistry 41 (2002) 3422-3429
HC Birnboim and J Doly, A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7 (1979) 1513-1523
DA Bryant and N Tandeau Marsac de, Isolation of genes encoding components of the photosynthetic apparatus. Methods Enzymol 167 (1988) 755-765
JS Buzby, RD Porter and JSE Stevens, Plasmid transformation in Agmenellum quadruplicatum PR-6: construction of biphasic plasmids and characterization of their transformation properties. J Bacteriol 154 (1983) 1446-1450
D Campbell, V Hurry, AK Clarke, P Gustafsson and G Öquist, Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62 (1998) 667-683
LM Casano, JM Zapata, M Martin and B Sabater, Chlororespiration and poising of cyclic electron transport. Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275 (2000) 942-948
JA Garcia-Horsman, B Barquera, J Rumbley, J Ma and RB Gennis, The superfamily of heme-copper respiratory oxidases. J Bacteriol 176 (1994) 5587-5600
RJ Geider and BA Osborne, Algal Photosynthesis. New York: Chapman and Hall (1992).
M Ghassemian, B Wong, F Ferriera, JL Markley and NA Straus, Cloning, sequencing and transcriptional studies of the genes for cytochrome c-553 and plastocyanin from Anabaena sp. PCC 7120. Microbiology 140 (1994) 1151-1159
SS Golden, J Brusslan and R Haselkorn, Genetic engineering of the cyanobacterial chromosome. Methods Enzymol 153 (1987) 215-231
CA Howitt and WFJ Vermaas, Quinol and cytochrome oxidasees in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37 (1998) 17944-17951
T Kaneko, S Sato, H Kotani, A Tanaka, E Asamizu, Y Nakamura, N Miyajima, M Hirosawa, M Sugiura and S Sasamoto, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3 (1996) 109-136
PC Maxwell and J Biggins, Role of cyclic electron transport in photosynthesis as measured by the photoinduced turnover of P700 in vivo. Biochemistry 15 (1976) 3975-3981
C Nomura and DA Bryant, Cytochrome c6 from Synechococcus sp. PCC 7002. In: GP Peschek, W Löffelhardt and G Schmetterer (eds.) The Phototrophic Prokaryotes. New York, USA: Kluwer Academic/Plenum Publishers (1997) pp. 269-274
C Obinger, JC Knepper, U Zimmermann and GA Peschek, Identification of a periplasmic c-type cytochrome as electron donor to the plasma membrane-bound cytochrome oxidase of the cyanobacterium Nostoc mac. Biochem Biophys Res Commun 169 (1990) 492-501
GA Peschek, M Wastyn, M Trnka, V Molitor, IV Fry and L Packer, Characterization of the cytochrome c oxidase in isolated and purified plasma membranes from the cyanobacterium Anacystis nidulans. Biochemistry 28 (1989) 3057-3063
P Prentki and HM Krisch, In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29 (1984) 303-313
T Sakamoto and DA Bryant, Temperature-regulated mRNA accumulation and stabilization for fatty acid desaturase genes in the cyanobacterium Synechococcus sp. strain PCC 7002. Mol Microbiol 23 (1997) 1281-1292
T Sakamoto and DA Bryant, Growth at low temperature causes nitrogen limitation in the cyanobacterium Synechococcus sp. PCC 7002. Arch Microbiol 169 (1998) 10-19
T Sakamoto, VB Delgazio and DA Bryant, Growth on urea can trigger death and peroxidation of the cyanobacterium Synechococcus sp. strain PCC 7002. Appl Environ Microbiol 64 (1998) 2361-2366
J Sambrook, E Fritsch and T Maniatis, Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press (1989).
LV Savitch, DP Maxwell and NPA Huner, Photosystem II excitation pressure and photosynthetic carbon metabolism in Chlorella vulgaris. Plant Physiol 111 (1996) 127-136
G Schmetterer, D Alge and W Gregor, Deletion of cytochrome c oxidase genes from the cyanobacterium Synechocystis sp. PCC6803: Evidence for alternative respiratory pathways. Photosynth Res 42 (1994) 43-50
G Schmetterer, A Valladares, D Pils, S Steinbach, M Pacher, AM Muro-Pastor, E Flores and A Herrero, The coxBAC operon encodes a cytochrome c oxidase required for heterotrophic growth in the cyanobacterium Anabaena variabilis strain ATCC 29413. J Bacteriol 183 (2001) 6429-6434
U Schreiber, U Schliwa and W Bilger, Continuous recdording of photochemical and non-photochemical chlorophyl fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10 (1986) 51-62
H Schubert, HCP Matthijs and LR Mur, In vivo assay of P700 redox changes in the cyanobacterium Fremyella diplosiphon and the role of cytochrome c oxidase in regulation of photosynthetic electron transfer. Photosynthetica 31 (1995) 517-527
Sone N, Tano H and Ishizuka M (1993) The genes in the thermophilic cyanobacterium Synechococcus vulcanus encoding cytochrome c oxidase [published erratum appears in Biochim Biophys Acta 1994 Apr 28; 1188 (2):255]. Biochim Biophys Acta 1183: 130–138
JSE Stevens, COP Patterson and J Myers, The production of hydrogen peroxide by blue green algae: a survey. J Phycol 9 (1973) 427-430
H Tano, M Ishizuka and N Sone, The cytochrome c oxidase genes in blue-green algae and characteristics of the deduced protein sequence for subunit II of the thermophilic cyanobacterium Synechococcus vulcanus. Biochem Biophys Res Commun 181 (1991) 437-442
M Trnka and GA Peschek, Immunological identification of aa3-type cytochrome oxidase in membrane preparations of the cyanobacterium Anacystis nidulans. Biochem Biophys Res Commun 136 (1986) 235-241
Yu L, Zhao J, Mühlenhoff U, Bryant DA and Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nomura, C.T., Persson, S., Shen, G. et al. Characterization of two cytochrome oxidase operons in the marine cyanobacterium Synechococcus sp. PCC 7002: Inactivation of ctaDI affects the PS I:PS II ratio. Photosynth Res 87, 215–228 (2006). https://doi.org/10.1007/s11120-005-8533-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-005-8533-y