Photoresponse Mechanism in Cyanobacteria: Key Factor in Photoautotrophic Chassis

  • Jiao Zhan
  • Qiang Wang
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1080)


As the oldest oxygenic photoautotrophic prokaryotes, cyanobacteria have outstanding advantages as the chassis cell in the research field of synthetic biology. Cognition of photosynthetic mechanism, including the photoresponse mechanism under high-light (HL) conditions, is important for optimization of the cyanobacteria photoautotrophic chassis for synthesizing biomaterials as “microbial cell factories.” Cyanobacteria are well-established model organisms for the study of oxygenic photosynthesis and have evolved various acclimatory responses to HL conditions to protect the photosynthetic apparatus from photodamage. Here, we reviewed the latest progress in the mechanism of HL acclimation in cyanobacteria. The subsequent acclimatory responses and the corresponding molecular mechanisms are included: (1) acclimatory responses of PSII and PSI; (2) the degradation of phycobilisome; (3) induction of the photoprotective mechanisms such as state transitions, OCP-dependent non-photochemical quenching, and the induction of HLIP family; and (4) the regulation mechanisms of the gene expression under HL.


Synthetic biology Chassis Photosynthesis Cyanobacteria High light 


  1. 1.
    Akulinkina DV, Bolychevtseva YV, Elanskaya IV, Karapetyan NV, Yurina NP (2015) Association of high light-inducible HliA/HliB stress proteins with photosystem 1 trimers and monomers of the cyanobacterium Synechocystis PCC 6803. Biochem Biokhim 80:1254–1261. CrossRefGoogle Scholar
  2. 2.
    Allen JF, Sanders CE, Holmes NG (1985) Correlation of membrane-protein phosphorylation with excitation-energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193:271–275. CrossRefGoogle Scholar
  3. 3.
    Baier K, Nicklisch S, Grundner C, Reinecke J, Lockau W (2001) Expression of two nblA-homologous genes is required for phycobilisome degradation in nitrogen-starved Synechocystis sp. PCC6803. FEMS Microbiol Lett 195:35–39CrossRefPubMedGoogle Scholar
  4. 4.
    Barker M, de Vries R, Nield J, Komenda J, Nixon PJ (2006) The Deg proteases protect Synechocystis sp PCC 6803 during heat and light stresses but are not essential for removal of damaged D1 protein during the photosystem two repair cycle. J Biol Chem 281:30347–30355. CrossRefPubMedGoogle Scholar
  5. 5.
    Berera R, van Stokkum IH, Gwizdala M, Wilson AI, Kirilovsky D, van Grondelle R (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem B 116:2568–2574CrossRefPubMedGoogle Scholar
  6. 6.
    Bienert R, Baier K, Volkmer R, Lockau W, Heinemann U (2006) Crystal structure of NblA from Anabaena sp PCC 7120, a small protein playing a key role in phycobilisome degradation. J Biol Chem 281:5216–5223. CrossRefPubMedGoogle Scholar
  7. 7.
    Billis K, Billini M, Tripp HJ, Kyrpides NC, Mavromatis K (2014) Comparative transcriptomics between Synechococcus PCC 7942 and Synechocystis PCC 6803 provide insights into mechanisms of stress acclimation. PLoS One 9:e109738CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Boehm M et al (2012) Subunit organization of a synechocystis hetero-oligomeric thylakoid FtsH complex involved in photosystem II repair. Plant Cell 24:3669–3683. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Boulay C, Wilson A, D'Haene S, Kirilovsky D (2010) Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci 107:11620–11625CrossRefPubMedGoogle Scholar
  10. 10.
    Canaani O (1986) Photoacoustic detection of oxygen evolution and state 1–state 2 transitions in cyanobacteria. Biochim Biophys Acta (BBA)-Bioenerg 852:74–80CrossRefGoogle Scholar
  11. 11.
    Chen Z, Zhan J, Chen Y, Yang M, He C, Ge F, Wang Q (2015) Effects of phosphorylation of beta subunits of phycocyanins on state transition in the model cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 56:1997–2013. CrossRefPubMedGoogle Scholar
  12. 12.
    Chidgey JW et al (2014) A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC/Alb3 insertase. Plant Cell 26:1267–1279. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Collier JL, Grossman A (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Crawford TS, Hanning KR, Chua JP, Eaton-Rye JJ, Summerfield TC (2016) Comparison of D1′-and D1-containing PS II reaction centre complexes under different environmental conditions in Synechocystis sp. PCC 6803. Plant Cell Environ 39:1715–1726CrossRefPubMedGoogle Scholar
  15. 15.
    Czarnecki O, Grimm B (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63:1675–1687. CrossRefPubMedGoogle Scholar
  16. 16.
    Daddy S, Zhan J, Jantaro S, He C, He Q, Wang Q (2015a) A novel high light-inducible carotenoid-binding protein complex in the thylakoid membranes of Synechocystis PCC 6803. Sci Rep 5:9480. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Deamer D (2005) A giant step towards artificial life? Trends Biotechnol 23:336–338CrossRefPubMedGoogle Scholar
  18. 18.
    Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485. CrossRefPubMedGoogle Scholar
  19. 19.
    Dines M, Sendersky E, David L, Schwarz R (2008) Structural, functional, and mutational analysis of the NblA protein provides insight into possible modes of interaction with the phycobilisome. J Biol Chem 283(44):30330–30340Google Scholar
  20. 20.
    Dolganov N, Bhaya D, Grossman AR (1995) Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc Natl Acad Sci 92:636–640CrossRefPubMedGoogle Scholar
  21. 21.
    Dühring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci 103:7054–7058CrossRefPubMedGoogle Scholar
  22. 22.
    Eriksson J, Salih GF, Ghebramedhin H, Jansson C (2000) Deletion mutagenesis of the 5′ psbA2 region in Synechocystis 6803: identification of a putative cis element involved in photoregulation. Mol Cell Biol Res Commun 3:292–298CrossRefPubMedGoogle Scholar
  23. 23.
    Folea IM, Zhang P, Aro E-M, Boekema EJ (2008) Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett 582:1749–1754. CrossRefPubMedGoogle Scholar
  24. 24.
    Fujimori T, Hihara Y, Sonoike K (2005) PsaK2 subunit in photosystem I is involved in state transition under high light condition in the cyanobacterium Synechocystis sp PCC 6803. J Biol Chem 280:22191–22197. CrossRefPubMedGoogle Scholar
  25. 25.
    Funk C, Vermaas W (1999) A cyanobacterial gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants. Biochemistry 38:9397–9404CrossRefPubMedGoogle Scholar
  26. 26.
    Gao X, Gao F, Liu D, Zhang H, Nie XQ, Yang C (2016) Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO2. Energy Environ Sci 9:1400–1411CrossRefGoogle Scholar
  27. 27.
    Gao ZX, Zhao H, Li ZM, Tan XM, Lu XF (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5:9857–9865CrossRefGoogle Scholar
  28. 28.
    Georg J et al (2014) The small regulatory RNA SyR1/PsrR1 controls photosynthetic functions in cyanobacteria. Plant Cell 26:3661–3679. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Golden SS, Brusslan J, Haselkorn R (1987) [12] Genetic engineering of the cyanobacterial chromosome. Methods Enzymol 153:215–231CrossRefPubMedGoogle Scholar
  30. 30.
    Grossman AR, Bhaya D, He Q (2001) Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 276:11449–11452. CrossRefPubMedGoogle Scholar
  31. 31.
    Gwizdala M, Wilson A, Kirilovsky D (2011) In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the orange carotenoid protein in Synechocystis PCC 6803. Plant Cell 23:2631–2643CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Gwizdala M, Wilson A, Omairi-Nasser A, Kirilovsky D (2013) Characterization of the Synechocystis PCC 6803 fluorescence recovery protein involved in photoprotection. BBA-Bioenergetics 1827:348–354. CrossRefPubMedGoogle Scholar
  33. 33.
    Hanaoka M, Tanaka K (2008) Dynamics of RpaB–promoter interaction during high light stress, revealed by chromatin immunoprecipitation (ChIP) analysis in Synechococcus elongatus PCC 7942. Plant J 56:327–335CrossRefPubMedGoogle Scholar
  34. 34.
    Havaux M, Guedeney G, He QF, Grossman AR (2003) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. BBA-Bioenergetics 1557:21–33. CrossRefPubMedGoogle Scholar
  35. 35.
    He Q, Dolganov N, Bjorkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314. CrossRefPubMedGoogle Scholar
  36. 36.
    Hernandez-Prieto MA, Tibiletti T, Abasova L, Kirilovsky D, Vass I, Funk C (2011) The small CAB-like proteins of the cyanobacterium Synechocystis sp. PCC 6803: their involvement in chlorophyll biogenesis for photosystem II. Biochim Biophys Acta (BBA)-Bioenerg 1807:1143–1151CrossRefGoogle Scholar
  37. 37.
    Hihara Y, Sonoike K, Ikeuchi M (1998) A novel gene, pmgA, specifically regulates photosystem stoichiometry in the cyanobacterium Synechocystis species PCC 6803 in response to high light. Plant Physiol 117:1205–1216CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548. CrossRefPubMedGoogle Scholar
  39. 39.
    Hsiao HY, He QF, van Waasbergen LG, Grossman AR (2004) Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J Bacteriol 186:3882–3888. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Hu J, Li T, Xu W, Zhan J, Chen H, He C, Wang Q (2017) Small antisense RNA RblR positively regulates RuBisCo in Synechocystis sp. PCC 6803. Front Microbiol 8:231PubMedPubMedCentralGoogle Scholar
  41. 41.
    Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231CrossRefPubMedGoogle Scholar
  42. 42.
    Jallet D, Thurotte A, Leverenz RL, Perreau F, Kerfeld CA, Kirilovsky D (2014) Specificity of the cyanobacterial orange carotenoid protein: influences of orange carotenoid protein and phycobilisome structures. Plant Physiol 164:790–804CrossRefPubMedGoogle Scholar
  43. 43.
    Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917CrossRefPubMedGoogle Scholar
  44. 44.
    Kadowaki T, Nagayama R, Georg J, Nishiyama Y, Wilde A, Hess WR, Hihara Y (2016) A feed-forward loop consisting of the response regulator RpaB and the small RNA PsrR1 controls light acclimation of photosystem I gene expression in the cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol 57:813–823. CrossRefPubMedGoogle Scholar
  45. 45.
    Kappell AD, Bhaya D, van Waasbergen LG (2006) Negative control of the high light-inducible hliA gene and implications for the activities of the NblS sensor kinase in the cyanobacterium Synechococcus elongatus strain PCC 7942. Arch Microbiol 186:403–413CrossRefPubMedGoogle Scholar
  46. 46.
    Kappell AD, van Waasbergen LG (2007) The response regulator RpaB binds the high light regulatory 1 sequence upstream of the high-light-inducible hliB gene from the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 187:337–342CrossRefPubMedGoogle Scholar
  47. 47.
    Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Karradt A, Sobanski J, Mattow J, Lockau W, Baier K (2008) NblA, a key protein of phycobilisome degradation, interacts with ClpC, a HSP100 chaperone partner of a cyanobacterial Clp protease. J Biol Chem 283:32394–32403. CrossRefPubMedGoogle Scholar
  49. 49.
    Kato H et al (2011) Interactions between histidine kinase NblS and the response regulators RpaB and SrrA are involved in the bleaching process of the cyanobacterium Synechococcus elongatus PCC 7942. Plant Cell Physiol 52:2115–2122CrossRefPubMedGoogle Scholar
  50. 50.
    Kettunen R, Pursiheimo S, Rintamaki E, VanWijk KJ, Aro EM (1997) Transcriptional and translational adjustments of psbA gene expression in mature chloroplasts during photoinhibition and subsequent repair of photosystem II. Eur J Biochem 247:441–448. CrossRefPubMedGoogle Scholar
  51. 51.
    Kirilovsky D (2015) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126:3–17. CrossRefPubMedGoogle Scholar
  52. 52.
    Kirilovsky D, Kerfeld CA (2016) Cyanobacterial photoprotection by the orange carotenoid protein. Nat Plants 2:16180CrossRefPubMedGoogle Scholar
  53. 53.
    Knoppova J et al (2014) Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant Cell 26:1200–1212. CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Komenda J, Barker M, Kuvikova S, de Vries R, Mullineaux CW, Tichy M, Nixon PJ (2006) The FtsH protease slr0228 is important for quality control of photosystem II in the thylakoid membrane of Synechocystis sp PCC 6803. J Biol Chem 281:1145–1151. CrossRefPubMedGoogle Scholar
  55. 55.
    Komenda J, Sobotka R (2016) Cyanobacterial high-light-inducible proteins—protectors of chlorophyll–protein synthesis and assembly. Biochim Biophys Acta (BBA)-Bioenerg 1857:288–295CrossRefGoogle Scholar
  56. 56.
    Kopecna J, Komenda J, Bucinska L, Sobotka R (2012) Long-term acclimation of the cyanobacterium Synechocystis sp. PCC 6803 to high light is accompanied by an enhanced production of chlorophyll that is preferentially channeled to trimeric photosystem I. Plant Physiol 160:2239–2250. CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kopf M, Hess WR (2015) Regulatory RNAs in photosynthetic cyanobacteria. FEMS Microbiol Rev 39:301–315. CrossRefPubMedGoogle Scholar
  58. 58.
    Krynicka V et al (2014) Two essential FtsH proteases control the level of the Fur repressor during iron deficiency in the cyanobacterium Synechocystis sp PCC 6803. Mol Microbiol 94:609–624. CrossRefPubMedGoogle Scholar
  59. 59.
    Kulkarni RD, Golden SS (1994) Adaptation to high light-intensity in Synechococcus sp strain PCC7942 – regulation of 3 psbA genes and 2 forms of the D1 protein. J Bacteriol 176:959–965CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Legewie S, Dienst D, Wilde A, Herzel H, Axmann IM (2008) Small RNAs establish delays and temporal thresholds in gene expression. Biophys J 95:3232–3238. CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Li H, Li DH, Yang SZ, Xie H, Zhao JQ (2006) The state transition mechanism – simply depending on light-on and -off in Spirulina platensis. BBA-Bioenergetics 1757:1512–1519. CrossRefPubMedGoogle Scholar
  62. 62.
    Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260. CrossRefPubMedGoogle Scholar
  63. 63.
    Longoni P, Douchi D, Cariti F, Fucile G, Goldschmidt-Clermont M (2015) Phosphorylation of the Lhcb2 isoform of light harvesting complex II is central to state transitions. Plant Physiol :pp.01498.02015
  64. 64.
    Ma F et al (2016) Dynamic changes of IsiA-containing complexes during long-term iron deficiency in Synechocystis sp. PCC 6803. Mol Plant.
  65. 65.
    Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C (2000) Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp PCC 6803. FEBS Lett 479:72–77. CrossRefPubMedGoogle Scholar
  66. 66.
    Marin K et al (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp PCC 6803. Proc Natl Acad Sci U S A 100:9061–9066. CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Biol 50:67–95CrossRefGoogle Scholar
  68. 68.
    Mehta P, Goyal S, Wingreen NS (2008) A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 4:221CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46:905–915CrossRefPubMedGoogle Scholar
  70. 70.
    Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008a) Identification of two homologous genes, chlAI and chlA(II), that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp PCC 6803. J Biol Chem 283:2684–2692. CrossRefPubMedGoogle Scholar
  71. 71.
    Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008b) Identification of two homologous genes, chlAI and chlAII, that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283:2684–2692CrossRefPubMedGoogle Scholar
  72. 72.
    Mitschke J et al (2011a) An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp PCC6803. Proc Natl Acad Sci U S A 108:2124–2129. CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Mitschke J, Vioque A, Haas F, Hess WR, Muro-Pastor AM (2011b) Dynamics of transcriptional start site selection during nitrogen stress-induced cell differentiation in Anabaena sp. PCC7120. Proc Natl Acad Sci 108:20130–20135CrossRefPubMedGoogle Scholar
  74. 74.
    Mukhopadhyay A, Kennelly PJ (2011) A low molecular weight protein tyrosine phosphatase from Synechocystis sp strain PCC 6803: enzymatic characterization and identification of its potential substrates. J Biochem 149:551–562. CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393. CrossRefPubMedGoogle Scholar
  76. 76.
    Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424CrossRefGoogle Scholar
  77. 77.
    Mulo P, Sicora C, Aro E-M (2009) Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697–3710. CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Murakami A, Fujita Y (1991) Regulation of photosystem stoichiometry in the photosynthetic system of the cyanophyte Synechocystis PCC 6714 in response to light-intensity. Plant Cell Physiol 32:223–230CrossRefGoogle Scholar
  79. 79.
    Muramatsu M, Hihara Y (2012) Acclimation to high-light conditions in cyanobacteria: from gene expression to physiological responses. J Plant Res 125:11–39. CrossRefPubMedGoogle Scholar
  80. 80.
    Muramatsu M, Sonoike K, Hihara Y (2009) Mechanism of downregulation of photosystem I content under high-light conditions in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 155:989–996CrossRefPubMedGoogle Scholar
  81. 81.
    Nakamura Y et al (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids (supplement). DNA Res 10:181–201CrossRefPubMedGoogle Scholar
  82. 82.
    Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635. CrossRefPubMedGoogle Scholar
  83. 83.
    Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Olive J, Mbina I, Vernotte C, Astier C, Wollman FA (1986) Randomization of the EF particles in thylakoid membranes of Synechocystis-6714 upon transition from state-I to state-II. FEBS Lett 208:308–312. CrossRefGoogle Scholar
  85. 85.
    Osbourn AE, O’Maille PE, Rosser SJ, Lindsey K (2012) Synthetic biology. New Phytol 196:671–677CrossRefPubMedGoogle Scholar
  86. 86.
    Pojidaeva E, Zinchenko V, Shestakov SV, Sokolenko A (2004) Involvement of the SppA1 peptidase in acclimation to saturating light intensities in Synechocystis sp strain PCC 6803. J Bacteriol 186:3991–3999. CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Polívka T, Kerfeld CA, Pascher T, Sundström V (2005) Spectroscopic properties of the carotenoid 3′-Hydroxyechinenone in the orange carotenoid protein from the cyanobacterium Arthrospira maxima. Biochemistry 44:3994–4003CrossRefPubMedGoogle Scholar
  88. 88.
    Rakhimberdieva MG, Elanskaya IV, Vermaas WF, Karapetyan NV (2010) Carotenoid-triggered energy dissipation in phycobilisomes of Synechocystis sp. PCC 6803 diverts excitation away from reaction centers of both photosystems. Biochim Biophys Acta (BBA)-Bioenerg 1797:241–249CrossRefGoogle Scholar
  89. 89.
    Sakurai I, Stazic D, Eisenhut M, Vuorio E, Steglich C, Hess WR, Aro EM (2012) Positive regulation of psbA gene expression by cis-encoded antisense RNAs in Synechocystis sp. PCC 6803. Plant Physiol 160:1000–1010. CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Seino Y, Takahashi T, Hihara Y (2009) The response regulator RpaB binds to the upstream element of photosystem I genes to work for positive regulation under low-light conditions in Synechocystis sp. strain PCC 6803. J Bacteriol 191:1581–1586CrossRefPubMedGoogle Scholar
  91. 91.
    Sendersky E, Kozer N, Levi M, Garini Y, Shav-Tal Y, Schwarz R (2014) The proteolysis adaptor, NblA, initiates protein pigment degradation by interacting with the cyanobacterial light-harvesting complexes. Plant J 79:118–126. CrossRefPubMedGoogle Scholar
  92. 92.
    Sendersky E, Kozer N, Levi M, Moizik M, Garini Y, Shav-Tal Y, Schwarz R (2015) The proteolysis adaptor, NblA, is essential for degradation of the core pigment of the cyanobacterial light-harvesting complex. Plant J: Cell Mol Biol 83:845–852. CrossRefGoogle Scholar
  93. 93.
    Shen J, Wang G (1998) State transition in blue-green alga Synechocystis PCC 6803. Chin Sci Bull 43:2087–2091CrossRefGoogle Scholar
  94. 94.
    Sicora CI, Ho FM, Salminen T, Styring S, Aro E-M (2009) Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. Biochim Biophys Acta (BBA)-Bioenerg 1787:105–112CrossRefGoogle Scholar
  95. 95.
    Silva P et al (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. Plant Cell 15:2152–2164. CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Singh AK, Elvitigala T, Bhattacharyya-Pakrasi M, Aurora R, Ghosh B, Pakrasi HB (2008) Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the cyanobacterium Synechocystis. Plant Physiol 148:467–478. CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Sokolenko A (2005) SppA peptidases: family diversity from heterotrophic bacteria to photoautotrophic eukaryotes. Physiol Plant 123:391–398. CrossRefGoogle Scholar
  98. 98.
    Staleva H, Komenda J, Shukla MK, Slouf V, Kana R, Polivka T, Sobotka R (2015) Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol 11:287–291. CrossRefPubMedGoogle Scholar
  99. 99.
    Summerfield TC, Toepel J, Sherman LA (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47:12939–12941. CrossRefPubMedGoogle Scholar
  100. 100.
    Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235–244. CrossRefPubMedGoogle Scholar
  101. 101.
    Tamary E et al (2012) Structural and functional alterations of cyanobacterial phycobilisomes induced by high-light stress. BBA-Bioenergetics 1817:319–327. CrossRefPubMedGoogle Scholar
  102. 102.
    Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60CrossRefPubMedGoogle Scholar
  103. 103.
    van der Woude AD, Angermayr SA, Puthan VV, Osnato A, Hellingwerf KJ (2014) Carbon sink removal: increased photosynthetic production of lactic acid by Synechocystis sp. PCC6803 in a glycogen storage mutant. J Biotechnol 184:100–102CrossRefPubMedGoogle Scholar
  104. 104.
    van Waasbergen LG, Dolganov N, Grossman AR (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184:2481–2490. CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Vavilin D, Yao D, Vermaas W (2007) Small cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp PCC 6803 – kinetic analysis of pigment labeling with N-15 AND C-13. J Biol Chem 282:37660–37668. CrossRefPubMedGoogle Scholar
  106. 106.
    Voigt K, Sharma CM, Mitschke J, Lambrecht SJ, Voß B, Hess WR, Steglich C (2014) Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J 8:2056–2068CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Wang B, Pugh S, Nielsen DR, Zhang W, Meldrum DR (2013) Engineering cyanobacteria for photosynthetic production of 3-hydroxybutyrate directly from CO2. Metab Eng 16:68–77CrossRefPubMedGoogle Scholar
  108. 108.
    Wang Q, Hall CL, Al-Adami MZ, He Q (2010) IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in synechocystis PCC 6803. Plos One 5:e10432. CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Wang Q, Jantaro S, Lu B, Majeed W, Bailey M, He Q (2008a) The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147:1239–1250. CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Wang Y, Sun T, Gao X, Shi M, Wu L, Chen L, Zhang W (2016) Biosynthesis of platform chemical 3-hydroxypropionic acid (3-HP) directly from CO2 in cyanobacterium Synechocystis sp. PCC 6803. Metab Eng 34:60CrossRefPubMedGoogle Scholar
  111. 111.
    Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116:265–276. CrossRefPubMedGoogle Scholar
  112. 112.
    Wilde A, Hihara Y (2016) Transcriptional and posttranscriptional regulation of cyanobacterial photosynthesis. Biochim Biophys Acta 1857:296–308. CrossRefPubMedGoogle Scholar
  113. 113.
    Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Wilson A et al (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci 105:12075–12080CrossRefPubMedGoogle Scholar
  115. 115.
    Xiong W, Morgan JA, Ungerer J, Wang B, Maness PC, Yu J (2015) Erratum: the plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene. Nat Plants 1:15053CrossRefGoogle Scholar
  116. 116.
    Xu H, Vavilin D, Funk C, Vermaas W (2004) Multiple deletions of small cab-like proteins in the cyanobacterium Synechocystis sp PCC 6803 – consequences for pigment biosynthesis and accumulation. J Biol Chem 279:27971–27979. CrossRefPubMedGoogle Scholar
  117. 117.
    Xu W, Chen H, He CL, Wang Q (2014) Deep sequencing-based identification of small regulatory RNAs in Synechocystis sp. PCC 6803. PLoS One 9:e92711. CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Xu X, Yang S, Xie J, Zhao J (2012) Kinetics and dynamics for light state transition in cyanobacterium Spirulina platensis cells. Biochem Biophys Res Commun 422:233–237. CrossRefPubMedGoogle Scholar
  119. 119.
    Xue Y, Zhang Y, Cheng D, Daddy S, He QF (2014) Genetically engineering Synechocystis sp Pasteur culture collection 6803 for the sustainable production of the plant secondary metabolite p-coumaric acid. Proc Natl Acad Sci U S A 111:9449–9454CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Yao D et al (2007) Localization of the small CAB-like proteins in photosystem II. J Biol Chem 282:267–276. CrossRefPubMedGoogle Scholar
  121. 121.
    Yao DC, Brune DC, Vavilin D, Vermaas WF (2012) Photosystem II component lifetimes in the cyanobacterium Synechocystis sp. strain PCC 6803 small cab-like proteins stabilize biosynthesis intermediates and affect early steps in chlorophyll synthesis. J Biol Chem 287:682–692CrossRefPubMedGoogle Scholar
  122. 122.
    Yeremenko N et al (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313. CrossRefPubMedGoogle Scholar
  123. 123.
    Yoshioka-Nishimura M, Yamamoto Y (2014) Quality control of photosystem II: the molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes. J Photochem Photobiol B-Biol 137:100–106. CrossRefGoogle Scholar
  124. 124.
    Yukako Hihara, AK, Minoru Kanehisa, Aaron Kaplan, Masahiko Ikeuchib (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806CrossRefGoogle Scholar
  125. 125.
    Zavafer A, Cheah MH, Hillier W, Chow WS, Takahashi S (2015) Photodamage to the oxygen evolving complex of photosystem II by visible light. Sci Rep 5:16363. CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2013) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53:13–19CrossRefPubMedPubMedCentralGoogle Scholar
  127. 127.
    Zhao C, Li Z, Li T, Zhang Y, Bryant DA, Zhao J (2015) High-yield production of extracellular type-I cellulose by the cyanobacterium Synechococcus sp. PCC 7002. Cell Discov 1:15004. CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Zilinskas BA, Greenwald LS (1986) Phycobilisome structure and function. Photosynth Res 10:7–35. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Algal Biology, Institute of HydrobiologyThe Chinese Academy of SciencesWuhanChina

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