Abstract
Cyanobacteria, as well as green algae and higher plants, have highly conserved photosynthetic machinery. Cyanothece sp. ATCC 51142 is a unicellular, aerobic, diazotrophic cyanobacterium that fixes N2 in the dark. In Cyanothece, the psbA gene family is composed of five members, encoding different isoforms of the D1 protein. A new D1 protein has been postulated in the literature, which blocks PSII during the night and allows the fixation of nitrogen. We present data showing changes in PSII function in cells grown in cycles alternating between 12 h of light and dark, respectively, at Cyanothece sp. ATCC 51142. Cyanothece sp. ATCC 51142 uses intrinsic mechanisms to protect its nitrogenase activity in a two-stage process. In Stage I, immediately after the onset of darkness, the cells lose photosynthetic activity in a reversible process, probably by dissociation of water oxidation complex from photosystem II via a mechanism that does not require de novo protein synthesis. In Stage II, a more severe disruption of photosystem II function occurs is in part protein synthesis dependent and it could be a functional signature of the presence of sentinel D1 in a limited number of reaction centers still active or not yet inactivated by the mechanism described in Stage I. This process of inhibition uses light as a triggering signal for both the inhibition of photosynthetic activity and recovery when light returns. The intrinsic mechanism of photosynthetic inactivation during darkness with the interplay of the two mechanisms requires further studies.
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References
Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. BBA 1143(2):113–134. https://doi.org/10.1016/0005-2728(93)90134-2
Brown CM, MacKinnon JD, Cockshutt AM, Villareal TA, Campbell DA (2008) Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Mar Biol 154(3):413–422. https://doi.org/10.1007/s00227-008-0933-z
Campbell D, Eriksson MJ, Öquist G, Gustafsson P, Clarke A (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci 95:364–369. https://doi.org/10.1073/pnas.95.1.364
Clarke AK, Soitamo A, Gustafsson P, Oquist G (1993) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci USA 90(21):9973–9977. https://doi.org/10.1073/pnas.90.21.9973
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. https://doi.org/10.1126/science.1093087
Gallon JR (1992) Reconciling the incompatible: N2 fixation and O2. New Phytol 22(4):571–609. https://doi.org/10.1111/j.1469-8137.1992.tb00087.x
Golden SS, Brusslan J, Haselkorn R (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5(11):2789–2798
Huang L, McCluskey MP, Ni H, LaRossa RA (2002) Global gene expression profiles of the cyanobacterium Synechocystis sp. PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol 184(24):6845–6858. https://doi.org/10.1128/JB.184.24.6845-6858.2002
Kos PB, Deak Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777:74–83. https://doi.org/10.1016/j.bbabio.2007.10.015
Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37(50):17339–17344. https://doi.org/10.1021/bi9822628
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage 438 T4. Nature 227(5259):680–685. https://doi.org/10.1038/227680a0
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044. https://doi.org/10.1038/nature04224
Masuda T, Bernat G, Beckova M, Kotabova E, Lawrenz E, Lukes M, Komenda J, Prasil O (2018) Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ Microbiol 20(2):546–560. https://doi.org/10.1111/1462-2920.13963
Mate Z, Sass L, Szekeres M, Vass I, Nagy F (1998) UV-B-induced differential transcription of psbA genes encoding the D1 protein of photosystem II in the cyanobacterium Synechocystis 6803. J Biol Chem 273:17439–17444. https://doi.org/10.1074/jbc.273.28.17439
Meunier PC, Colon-Lopez MS, Sherman LA (1998) Photosystem II cyclic heterogeneity and photoactivation in the diazotrophic, unicellular cyanobacterium Cyanothece species ATCC 51142. Plant Physiol 116:1551–1562. https://doi.org/10.1104/pp.116.4.1551
Mohamed A, Jansson C (1989) Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13:693–700. https://doi.org/10.1007/BF00016024
Mohamed A, Jansson C (1991) Photosynthetic electron transport controls degradation but not production of psbA transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 16:891–897. https://doi.org/10.1007/BF00015080
Mulo P, Sicora CI, Aro EM (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66(23):3697–3710. https://doi.org/10.1007/s00018-009-0103-6
Murray JW (2012) Sequence variation at the oxygen-evolving centre of photosystem II: a new class of ‘rogue’ cyanobacterial D1 proteins. Photosynth Res 110:177–184. https://doi.org/10.1007/s11120-011-9714-5
Nanba O, Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci 84(1):109–112. https://doi.org/10.1073/pnas.84.1.109
Nixon PJ, Trost JT, Diner BA (1992) Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC6803: assembly requires a free carboxyl group a tC-terminal position 344. Biochemistry 31:10859–10871
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16. https://doi.org/10.1093/aob/mcq059
Öquist G, Campbell D, Clarke AK, Gustafsson P (1995) The cyanobacterium Synechococcus modulates photosystem II function in response to excitation stress through D1 exchange. Photosynth Res 46:151–158. https://doi.org/10.1007/BF00020425
Reddy KJ, Haskell JB, Sherman DM, Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175:1284–1292. https://doi.org/10.1128/jb.175.5.1284-1292.1993
Salih GF, Jansson C (1997) Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp strain 6803 produces a nove1 and functional D1 protein. Plant Cell 9:869–878. https://doi.org/10.1105/tpc.9.6.869
Sander J, Nowaczyk M, Kopczak M, Rögner M (2008) Role of the psbA gene family of PSII from the thermophilic cyanobacterium Thermosynechococcus elongatus. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the Sun. Springer, Dordrecht, pp 745–748
Sane PV, Ivanov AG, Sveshnikov D, Huner NP, Öquist G (2002) A transient exchange of the photosystem II reaction center protein D1:1 with D1:2 during low temperature stress of Synechococcus sp. PCC 7942 in the light lowers the redox potential of Q(B). J Biol Chem 277(36):32739–32745. https://doi.org/10.1074/jbc.M200444200
Sherman LA, Meunier P, Colon-Lopez MS (1998) Diurnal rhythms in metabolism: a day in the life of a unicellular, diazotrophic cyanobacterium. Photosynth Res 58:25–42. https://doi.org/10.1023/A:1006137605802
Sicora CI, Máté Z, Vass I (2003) The interaction of visible and UV-B light during photodamage and repair of photosystem II. Photosynth Res 75:127–137. https://doi.org/10.1023/A:1022852631339
Sicora CI, Appleton SE, Brown CM, Chung J, Chandler J, Cockshutt AM, Vass I, Campbell DA (2006) Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. BBA 1:47–56. https://doi.org/10.1016/j.bbabio.2005.11.002
Sicora CI, Brown CM, Cheregi O, Vass I, Campbell DA (2008) The psbA gene family responds differentially to light and UVB stress in Gloeobacter violaceus PCC 7421, a deeply divergent cyanobacterium. Biochim Biophys Acta 1777:130–139. https://doi.org/10.1016/j.bbabio.2007.09.001
Sicora CI, Ho F, Salminen T, Styring S, Aro EM (2009) Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. Biochim Biophys Acta 1787:105–112. https://doi.org/10.1016/j.bbabio.2008.12.002
Sippola K, Aro EM (1999) Thiol redox state regulates expression of psbA genes in Synechococcus sp. PCC 7942. Plant Mol Biol 41:425–433. https://doi.org/10.1023/A:1006347808475
Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen JR (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517(7532):99–103. https://doi.org/10.1038/nature13991
Summerfield TC, Toepel J, Sherman LA (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47:11294–12939. https://doi.org/10.1021/bi8018916
Tichý M, Lupınková L, Sicora C, Vass I, Kuvikova S, Prášil O, Komenda J (2003) Synechocystis 6803 mutants expressing distinct forms of the photosystem II D1 protein from Synechococcus 7942: relationship between the psbA coding region and sensitivity to visible and UV-B radiation. BBA 1605(1–3):55–66. https://doi.org/10.1016/S0005-2728(03)00064-1
Toepel J, Welsh E, Summerfield TC, Pakrasi HB, Sherman LA (2008) Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J Bacteriol 190:3904–3913. https://doi.org/10.1128/JB.00206-08
Tyystjarvi T, Tuominen I, Herranen M, Aro EM, Tyystjarvi E (2002) Action spectrum of psbA gene transcription is similar to that of photoinhibition in Synechocystis sp. PCC 6803. FEBS Lett 516(1–3):167–171. https://doi.org/10.1016/S0014-5793(02)02537-1
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473(7345):55–60. https://doi.org/10.1038/nature09913
Vass I, Kirilovsky D, Etienne A-L (1999) UV-B radiation-induced donor-and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 38:12786–12794. https://doi.org/10.1021/bi991094w
Vazquez D (1974) Inhibitors of protein synthesis. FEBS Lett 40:S48–S62. https://doi.org/10.1016/0014-5793(74)80689-7
Wegener KM, Nagarajan A, Pakrasi HB (2015) An atypical psbA gene encodes a sentinel D1 protein to form a physiologically relevant inactive photosystem II complex in cyanobacteria. J Biol Chem 290:3764–3774. https://doi.org/10.1074/jbc.M114.604124
Whitmarsh J, Govindjee (1999) The photosynthetic process. In: Singhal GS, Renger R, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology. Springer, Dordrecht, pp 11–51
Williams RJP, da Silva JJRF (1997) The natural selection of the chemical elements: the environment and life’s chemistry. Claredon Press, Gloucestershire
Zhang X, Sherman LA (2012) Alternate copies of D1 are used by cyanobacteria under different environmental conditions. Photosynth Res 114:133–135. https://doi.org/10.1007/s11120-012-9783-0
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The project was partially funded by the Romanian National Authority for Scientific Research, CNCS-UEFISCDI, project number: PN-II-IDPCE-2011-3-0765 and the Executive Unit for Financing Higher Education, Research, Development and Innovation (UEFISCDI), Romania, project code PN-II-RU-PD-2011-3-0255.
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Sicora, C.I., Chiș, I., Chiș, C. et al. Regulation of PSII function in Cyanothece sp. ATCC 51142 during a light–dark cycle. Photosynth Res 139, 461–473 (2019). https://doi.org/10.1007/s11120-018-0598-5
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DOI: https://doi.org/10.1007/s11120-018-0598-5