Abstract
Functional organization of the photosynthetic apparatus in the unique chlorophyll d-predominating prokaryote, Acaryochloris marina, was studied using polarographic measurements of single-turnover flash yields, action spectra and optical cross sections for PS-specific reactions. O2 evolution was indicative of PS II activity, while reversible photoinhibition of respiratory O2 uptake under aerobic conditions in the presence of DCMU and H2 photoevolution by anaerobically adapted cells were the indicatives of PS I activity. O2 evolution in the cells upon single-turnover flashes followed the normal S-state cycle with a period-4 oscillation. Analysis of action spectra for the partial reactions of photosynthesis revealed that: (1) distinct spectral forms of Chl d are nonuniformly distributed between PS I and PS II, e.g. Chl d-695 and Chl d-735 are preferentially located in PS II and PS I, respectively; (2) a minor fraction of Chl a in the cells belongs mostly to PS II; (3) biliproteins transfer excitation energy both to PS II and, with a lower efficiency, PS I; (4) the efficiency of energy transfer from biliproteins to PS II depends on the light quality growth conditions and is larger in white light (WL)-grown cells compared to the red light (RL)-grown cells. Content of functional O2 evolving PS II centers decreases 2 times in the RL-grown cells relative to the WL-grown cells, whereas content of competent PS I centers involved in photoinhibition of respiration remains almost the same in both the cultures. The effective antenna size of PS I was estimated to be 80–90 Chl d including 3–10 molecules absorbing at 735 nm. The effective optical cross-section of PS II corresponded to 90–100 Chl d and, presumably, 4 Chl a + 2 Pheo a [Mimuro et al. (1999) Biochim Biophys Acta 1412: 37–46]. Optical cross-section measurements indicated that the functional PS II units of A. marina attach one rod of four hexameric units of biliproteins.
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References
Appel J and Schultz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis: Hydrogenases as important regulatory devices for a proper redox poising? J Photochem Photobiol B47: 1–11
Bald D, Kruíp J and Rögner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems? Photosynth Res 49: 103–118
Boekema EJ, Hankamer B, Bald D, Kruip J, Niedl J, Boonstra AF, Barber J and Rögner M (1995) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92: 175–179
Boichenko VA (1998) Action spectra and functional antenna sizes of Photosystems I and II in relation to the thylakoid membrane organization and pigment composition. Photosynth Res 58: 163–174
Boichenko VA and Bader KP (1998) Verification of the Z-scheme in Chlamydomonas mutants with Photosystem I deficiency. Photosynth Res 56: 113–115
Boichenko VA and Hoffmann P (1994) Photosynthetic hydrogen production in prokaryotes and eukaryotes: Occurrence, mechanism and functions. Photosynthetica 30: 527–552
Boichenko VA, Wiessner W, Klimov VV, Mende D and Demeter S (1992) Hydrogen photoevolution indicates an increase in the antenna size of Photosystem I in Chlamydobotrys stellata during transition from autotrophic to photoheterotrophic nutrition. Plant Physiol 100: 518–524
Boichenko VA, Klimov VV, Mayes SR and Barber J (1993) Characterization of the light-induced oxygen gas exchange from the IC2 mutant of Synechocystis sp PCC 6803 lacking the Photosystem II 33 kDa extrinsic protein. Z Naturforcsh 48c: 224–233
Gantt E (1996) Pigment protein complexes and the concept of the photosynthetic unit: Chlorophyll complexes and phycobilisomes. Photosynth Res 48: 47–53
Gobets B, Van Amerongen H, Monshouwer R, Kruip J, Rögner M, van Grondelle R and Dekker JP (1994) Polarized site-selected fluorescence spectroscopy of isolated Photosystem I particles. Biochim Biophys Acta 1118: 75–85
Dubinsky Z, Falkowski PG and Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27: 1335–1349
Elanskaya IV, Allakhverdiev SI, Boichenko VA, Klimov VV, Demeter S, Timofeev KN and Shestakov SV (1994) Photochemical characterization of cyanobacterium Synechocystis sp. PCC 6803 mutants with impaired photosystem II proteins. Biochemistry (Moscow) — Engl Tr 59: 929–934
Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: Accomplishments and problems for future studies. Photosynth Res 53: 83–93
Hastings G, Hoshina S, Webber AN and Blankenship RE (1995) Universality of energy and electron transfer processes in Photosystem I. Biochemistry 34: 15512–15522
Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M and Itoh S (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci USA 95: 13319–13323
Hu Q, Marquardt J, Iwasaki I, Miyashita H, Kurano N, Mörschel E and Miyachi S (1999) Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochim Biophys Acta 1412: 250–261
Koehne B and Trissl H-W (1998) The cyanobacterium Spirulina platensis contains a long wavelength-absorbing pigment C738(F 77K 760) at room temperature. Biochemistry 37: 5494–550
Lewin RA and Whithers NW (1975) Extraordinary pigment composition of a prokaryotic alga. Nature 256: 735–737
Marquardt J, Senger H, Miyashita H, Miyachi S and Mörschel E (1997) Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 410: 428–432
Meunier PC, Burnap RL and Sherman LA (1995) Interaction of the photosynthetic and respiratory electron transport chains producing slow O2 signals under flashing light in Synechocystis sp. PCC 6803. Photosynth Res 45: 31–40
Meunier PC, Colon-Lopez MS and Sherman LA (1998) Photosystem II cyclic heterogeneity and photoactivation in the diazotrophic, unicellular cyanobacterium Cyanothece species ATCC 51142. Plant Physiol 116: 1551–1562
Mimuro M, Akimoto S, Yamazaki I, Miyashita H and Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga, Acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412: 37–46
Mimuro M, Hirayama K, Uezono K, Miyashita H and Miyachi S (2000) Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, Acaryochloris marina. Biochim Biophys Acta 1456: 27–34
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M and Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383: 402
Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M and Miyachi S (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major pigment. Plant Cell Physiol 38: 274–281
Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to Photosystem I in a cyanobacterium. Biochim Biophys Acta 1100: 285–292
Mullineaux CW (1994) Excitation energy transfer from phycobilisomes to Photosystem I in a cyanobacterial mutant lacking Photosystem 2. Biochim Biophys Acta 1184: 71–77
Myers J and Graham JR (1971) The photosynthetic unit in Chlorella measured by repetitive short flashes. Plant Physiol 48: 282–286
Pølsson L-O, Dekker JP, Schlodder E, Monshouwer R and Van Grondelle R (1996) Polarized site-selected fluorescence spectroscopy of the long-wavelength emitting chlorophylls in isolated Photosystem I particles of Synechococcus elongatus. Photosynth Res 48: 239–246
Pølsson L-O, Flemming C, Gobets B, Van Grondelle R, Dekker JP and Schlodder E (1998) Energy transfer and charge separation in Photosystem I: P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus. Biophys J 74: 2611–2622
Pfannschmidt T, Nilsson A and Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625–628
Porra RJ, Thompson WA and Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384–394
Rögner M, Nixon PJ and Diner BA (1990) Purification and characterization of Photosystem I and Photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 265: 6189–6196
Satoh K (1996) Introduction to the Photsystem II center—isolation and biochemical and biophysical characterization. In: Ort DR and Yocum CF (eds) Oxygenic Photosynthesis: The Light Reactions, pp 193–211. Kluwer Academic Publishers, Dordrecht, The Netherlands
Schiller H, Senger H, Miyashita H, Miyachi S and Dau H (1997) Light-harvesting in Acaryochloris marina — spectroscopic characterization of a chlorophyll d-dominated photosynthetic antenna system. FEBS Lett 410: 433–436
Shubin VV, Bezsmertnaya IN and Karapetyan NV (1995) Efficient energy transfer from the long-wavelength antenna chlorophylls to P700 in Photosystem I complexes from Spirulina platensis. J Photochem Photobiol B 30: 153–160
Sidler WA (1994) Phycobilisome and phycobiliprotein structures. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 139–216. Kluwer Academic Publishers, Dordrecht, The Netherlands
Soukoulis V, Savikhin S, Xu W, Chitnis PR and Struve WS (1999) Electronic spectra of PS I mutants: The peripheral subunits do not bind red chlorophylls in Synechocystis sp. PCC 6803. Biophys J 76: 2711–2715
Trissl H-W (1993) Long-wavelength absorbing antenna pigments and heterogeneous absorption bands concentrate excitons and increase absorption cross section. Photosynth Res 35: 247–263
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Boichenko, V.A., Klimov, V.V., Miyashita, H. et al. Functional characteristics of chlorophyll d-predominating photosynthetic apparatus in intact cells of Acaryochloris marina. Photosynthesis Research 65, 269–277 (2000). https://doi.org/10.1023/A:1010637631417
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DOI: https://doi.org/10.1023/A:1010637631417