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Abstract

Widespread phytochrome photoreceptors use photoisomerization of linear tetrapyrrole (bilin) chromophores to measure the ratio of red to far-red light. Cyanobacteria also contain distantly related cyanobacteriochrome (CBCR) proteins that share the bilin-binding GAF domain of phytochromes but sense other colors of light. CBCR photocycles are extremely diverse, ranging from the near-UV to the near-IR. Photoisomerization of the bilin triggers photoconversion of the CBCR input, thereby modulating the biochemical signaling state of output domains such as histidine kinase bidomains that can interface with cellular signal transduction pathways. CBCRs thus can regulate several aspects of cyanobacterial photobiology, including phototaxis, metabolism of cyclic nucleotide second messengers, and optimization of the cyanobacterial light-harvesting apparatus. This review examines spectral tuning, photoconversion, and photobiology of CBCRs and recent developments in understanding their evolution and in applying them in synthetic biology.

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2024-11-20
2025-02-11
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Literature Cited

  1. 1.
    Altmayer S, Köhler L, Bielytskyi P, Gärtner W, Matysik J, et al. 2022.. Light- and pH-dependent structural changes in cyanobacteriochrome AnPixJg2. . Photochem. Photobiol. Sci. 21::44769
    [Crossref] [Google Scholar]
  2. 2.
    Badary A, Abe K, Ferri S, Kojima K, Sode K. 2015.. The development and characterization of an exogenous green-light-regulated gene expression system in marine cyanobacteria. . Mar. Biotechnol. 17::24551
    [Crossref] [Google Scholar]
  3. 3.
    Bandara S, Rockwell NC, Zeng X, Ren Z, Wang C, et al. 2021.. Crystal structure of a far-red-sensing cyanobacteriochrome reveals an atypical bilin conformation and spectral tuning mechanism. . PNAS 118::e2025094118
    [Crossref] [Google Scholar]
  4. 4.
    Bhaya D, Takahashi A, Grossman AR. 2001.. Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. . PNAS 98::754045
    [Crossref] [Google Scholar]
  5. 5.
    Blain-Hartung M, Rockwell NC, Lagarias JC. 2017.. Light-regulated synthesis of cyclic-di-GMP by a bidomain construct of the cyanobacteriochrome Tlr0924 (SesA) without stable dimerization. . Biochemistry 56::614554
    [Crossref] [Google Scholar]
  6. 6.
    Blain-Hartung M, Rockwell NC, Lagarias JC. 2021.. Natural diversity provides a broad spectrum of cyanobacteriochrome-based diguanylate cyclases. . Plant Physiol. 187::63245
    [Crossref] [Google Scholar]
  7. 7.
    Blain-Hartung M, Rockwell NC, Moreno MV, Martin SS, Gan F, et al. 2018.. Cyanobacteriochrome-based photoswitchable adenylyl cyclases (cPACs) for broad spectrum light regulation of cAMP levels in cells. . J. Biol. Chem. 293::847383
    [Crossref] [Google Scholar]
  8. 8.
    Bryant DA. 1981.. The photoregulated expression of multiple phycocyanin species. A general mechanism for the control of phycocyanin synthesis in chromatically adapting cyanobacteria. . Eur. J. Biochem. 119::42529
    [Crossref] [Google Scholar]
  9. 9.
    Bryant DA, Canniffe DP. 2018.. How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. . J. Phys. B 51::033001
    [Crossref] [Google Scholar]
  10. 10.
    Burgie ES, Walker JM, Phillips GN Jr., Vierstra RD. 2013.. A photo-labile thioether linkage to phycoviolobilin provides the foundation for the blue/green photocycles in DXCF-cyanobacteriochromes. . Structure 21::8897
    [Crossref] [Google Scholar]
  11. 11.
    Bussell AN, Kehoe DM. 2013.. Control of a four-color sensing photoreceptor by a two-color sensing photoreceptor reveals complex light regulation in cyanobacteria. . PNAS 110::1283439
    [Crossref] [Google Scholar]
  12. 12.
    Campbell EL, Hagen KD, Chen R, Risser DD, Ferreira DP, Meeks JC. 2015.. Genetic analysis reveals the identity of the photoreceptor for phototaxis in hormogonium filaments of Nostoc punctiforme. . J. Bacteriol. 197::78291
    [Crossref] [Google Scholar]
  13. 13.
    Chang CW, Gottlieb SM, Kim PW, Rockwell NC, Lagarias JC, Larsen DS. 2013.. Reactive ground-state pathways are not ubiquitous in red/green cyanobacteriochromes. . J. Phys. Chem. B 117::1122938
    [Crossref] [Google Scholar]
  14. 14.
    Chen KN, Ma BG. 2023.. OptoCRISPRi-hd: engineering a bacterial green-light-activated CRISPRi system with a high dynamic range. . ACS Synth. Biol. 12::170815
    [Crossref] [Google Scholar]
  15. 15.
    Chen Y, Zhang J, Luo J, Tu JM, Zeng XL, et al. 2012.. Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics. . FEBS J. 279::4054
    [Crossref] [Google Scholar]
  16. 16.
    Cho SM, Jeoung SC, Song JY, Kupriyanova EV, Pronina NA, et al. 2015.. Genomic survey and biochemical analysis of recombinant candidate cyanobacteriochromes reveals enrichment for near UV/violet sensors in the halotolerant and alkaliphilic cyanobacterium Microcoleus IPPAS B353. . J. Biol. Chem. 290::2850214
    [Crossref] [Google Scholar]
  17. 17.
    Cho SM, Jeoung SC, Song JY, Song JJ, Park YI. 2017.. Hydrophobic residues near the bilin chromophore-binding pocket modulate spectral tuning of insert-Cys subfamily cyanobacteriochromes. . Sci. Rep. 7::40576
    [Crossref] [Google Scholar]
  18. 18.
    Clinger JA, Chen E, Kliger DS, Phillips GN Jr. 2021.. Pump-probe circular dichroism spectroscopy of cyanobacteriochrome TePixJ yields: insights into its photoconversion. . J. Phys. Chem. B 125::20210
    [Crossref] [Google Scholar]
  19. 19.
    Cornilescu CC, Cornilescu G, Burgie ES, Markley JL, Ulijasz AT, Vierstra RD. 2013.. Dynamic structural changes underpin photoconversion of a blue/green cyanobacteriochrome between its dark and photoactivated states. . J. Biol. Chem. 289::305565
    [Crossref] [Google Scholar]
  20. 20.
    Enomoto G, Ikeuchi M. 2020.. Blue-/green-light-responsive cyanobacteriochromes are cell shade sensors in red-light replete niches. . iScience 23::100936
    [Crossref] [Google Scholar]
  21. 21.
    Enomoto G, Win NN, Narikawa R, Ikeuchi M. 2015.. Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. . PNAS 112::808287
    [Crossref] [Google Scholar]
  22. 22.
    Enomoto G, Nomura R, Shimada T, Win NN, Narikawa R, Ikeuchi M. 2014.. Cyanobacteriochrome SesA is a diguanylate cyclase that induces cell aggregation in Thermosynechococcus. . J. Biol. Chem. 289::248019
    [Crossref] [Google Scholar]
  23. 23.
    Enomoto G, Wallner T, Wilde A. 2023.. Control of light-dependent behaviour in cyanobacteria by the second messenger cyclic di-GMP. . Microlife 4::uqad019
    [Crossref] [Google Scholar]
  24. 24.
    Essen LO, Mailliet J, Hughes J. 2008.. The structure of a complete phytochrome sensory module in the Pr ground state. . PNAS 105::1470914
    [Crossref] [Google Scholar]
  25. 25.
    Fischer AJ, Rockwell NC, Jang AY, Ernst LA, Waggoner AS, et al. 2005.. Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44::1520315
    [Crossref] [Google Scholar]
  26. 26.
    Freer LH, Kim PW, Corley SC, Rockwell NC, Zhao L, et al. 2012.. Chemical inhomogeneity in the ultrafast dynamics of the DXCF cyanobacteriochrome Tlr0924. . J. Phys. Chem. B 116::1057181
    [Crossref] [Google Scholar]
  27. 27.
    Fushimi K, Enomoto G, Ikeuchi M, Narikawa R. 2017.. Distinctive properties of dark reversion kinetics between two red/green-type cyanobacteriochromes and their application in the photoregulation of cAMP synthesis. . Photochem. Photobiol. 93::68191
    [Crossref] [Google Scholar]
  28. 28.
    Fushimi K, Hasegawa M, Ito T, Rockwell NC, Enomoto G, et al. 2020.. Evolution-inspired design of multicolored photoswitches from a single cyanobacteriochrome scaffold. . PNAS 117::1557380
    [Crossref] [Google Scholar]
  29. 29.
    Fushimi K, Hoshino H, Shinozaki-Narikawa N, Kuwasaki Y, Miyake K, et al. 2020.. The cruciality of single amino acid replacement for the spectral tuning of biliverdin-binding cyanobacteriochromes. . Int. J. Mol. Sci. 21::6278
    [Crossref] [Google Scholar]
  30. 30.
    Fushimi K, Ikeuchi M, Narikawa R. 2017.. The expanded red/green cyanobacteriochrome lineage: an evolutionary hot spot. . Photochem. Photobiol. 93::9036
    [Crossref] [Google Scholar]
  31. 31.
    Fushimi K, Miyazaki T, Kuwasaki Y, Nakajima T, Yamamoto T, et al. 2019.. Rational conversion of chromophore selectivity of cyanobacteriochromes to accept mammalian intrinsic biliverdin. . PNAS 116::83019
    [Crossref] [Google Scholar]
  32. 32.
    Fushimi K, Narikawa R. 2019.. Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum. . Curr. Opin. Struct. Biol. 57::3946
    [Crossref] [Google Scholar]
  33. 33.
    Fushimi K, Narikawa R. 2021.. Unusual ring D fixation by three crucial residues promotes phycoviolobilin formation in the DXCF-type cyanobacteriochrome without the second Cys. . Biochem. J. 478::104359
    [Crossref] [Google Scholar]
  34. 34.
    Fushimi K, Rockwell NC, Enomoto G, Win NN, Martin SS, et al. 2016.. Cyanobacteriochrome photoreceptors lacking the canonical Cys residue. . Biochemistry 55::698195
    [Crossref] [Google Scholar]
  35. 35.
    Gaidukov N. 1902.. Über den Einfluss farbigen Lichts auf die Färbung lebender Oscillarien. Berlin:: Abhandlung Königlich Preuss. Akad. Wiss.
    [Google Scholar]
  36. 36.
    Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA. 2014.. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. . Science 345::131217
    [Crossref] [Google Scholar]
  37. 37.
    Glazer AN. 1985.. Light harvesting by phycobilisomes. . Annu. Rev. Biophys. 14::4777
    [Crossref] [Google Scholar]
  38. 38.
    Gottlieb SM, Chang CW, Martin SS, Rockwell NC, Lagarias JC, Larsen DS. 2014.. Optically guided photoactivity: coordinating tautomerization, photoisomerization, inhomogeneity, and reactive intermediates within the RcaE cyanobacteriochrome. . J. Phys. Chem. Lett. 5::152733
    [Crossref] [Google Scholar]
  39. 39.
    Gottlieb SM, Kim PW, Chang CW, Hanke SJ, Hayer RJ, et al. 2015.. Conservation and diversity in the primary forward photodynamics of red/green cyanobacteriochromes. . Biochemistry 54::102842
    [Crossref] [Google Scholar]
  40. 40.
    Gottlieb SM, Kim PW, Corley SC, Madsen D, Hanke SJ, et al. 2014.. Primary and secondary photodynamics of the violet/orange dual-cysteine NpF2164g3 cyanobacteriochrome domain from Nostoc punctiforme. . Biochemistry 53::102940
    [Crossref] [Google Scholar]
  41. 41.
    Gottlieb SM, Kim PW, Rockwell NC, Hirose Y, Ikeuchi M, et al. 2013.. Primary photodynamics of the green/red-absorbing photoswitching regulator of the chromatic adaptation E domain from Fremyella diplosiphon. . Biochemistry 52::8198208
    [Crossref] [Google Scholar]
  42. 42.
    Grebert T, Nguyen AA, Pokhrel S, Joseph KL, Ratin M, et al. 2021.. Molecular bases of an alternative dual-enzyme system for light color acclimation of marine Synechococcus cyanobacteria. . PNAS 118::e2019715118
    [Crossref] [Google Scholar]
  43. 43.
    Greenswag AR, Li X, Borbat PP, Samanta D, Watts KJ, et al. 2015.. Preformed soluble chemoreceptor trimers that mimic cellular assembly states and activate CheA autophosphorylation. . Biochemistry 54::345468
    [Crossref] [Google Scholar]
  44. 44.
    Hasegawa M, Fushimi K, Miyake K, Nakajima T, Oikawa Y, et al. 2018.. Molecular characterization of DXCF cyanobacteriochromes from the cyanobacterium Acaryochloris marina identifies a blue-light power sensor. . J. Biol. Chem. 293::171327
    [Crossref] [Google Scholar]
  45. 45.
    Hirose Y, Chihong S, Watanabe M, Yonekawa C, Murata K, et al. 2019.. Diverse chromatic acclimation processes regulating phycoerythrocyanin and rod-shaped phycobilisome in cyanobacteria. . Mol. Plant 12::71525
    [Crossref] [Google Scholar]
  46. 46.
    Hirose Y, Narikawa R, Katayama M, Ikeuchi M. 2010.. Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. . PNAS 107::885459
    [Crossref] [Google Scholar]
  47. 47.
    Hirose Y, Rockwell NC, Nishiyama K, Narikawa R, Ukaji Y, et al. 2013.. Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. . PNAS 110::497479
    [Crossref] [Google Scholar]
  48. 48.
    Hirose Y, Shimada T, Narikawa R, Katayama M, Ikeuchi M. 2008.. Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. . PNAS 105::952833
    [Crossref] [Google Scholar]
  49. 49.
    Hoshino H, Narikawa R. 2023.. Novel cyanobacteriochrome photoreceptor with the second Cys residue showing atypical orange/blue reversible photoconversion. . Photochem. Photobiol. Sci. 22::25161
    [Crossref] [Google Scholar]
  50. 50.
    Hu JH, Chang JW, Xu T, Wang J, Wang X, et al. 2021.. Structural basis of bilin binding by the chlorophyll biosynthesis regulator GUN4. . Protein Sci. 30::208391
    [Crossref] [Google Scholar]
  51. 51.
    Hu P-P, Hou J-Y, Guo R, Jiang S-P, Zhou M, Zhao K-H. 2018.. Conversion of phycocyanobilin-binding GAF domain to biliverdin-binding domain. . J. Porphyr. Phthalocyanines 22::398405
    [Crossref] [Google Scholar]
  52. 52.
    Ikeuchi M, Ishizuka T. 2008.. Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. . Photochem. Photobiol. Sci. 7::115967
    [Crossref] [Google Scholar]
  53. 53.
    Ishizuka T, Kamiya A, Suzuki H, Narikawa R, Noguchi T, et al. 2011.. The cyanobacteriochrome, TePixJ, isomerizes its own chromophore by converting phycocyanobilin to phycoviolobilin. . Biochemistry 50::95361
    [Crossref] [Google Scholar]
  54. 54.
    Ishizuka T, Narikawa R, Kohchi T, Katayama M, Ikeuchi M. 2007.. Cyanobacteriochrome TePixJ of Thermosynechococcus elongatus harbors phycoviolobilin as a chromophore. . Plant Cell Physiol. 48::138590
    [Crossref] [Google Scholar]
  55. 55.
    Jang J, Reed PMM, Rauscher S, Woolley GA. 2022.. Point (S-to-G) mutations in the W(S/G)GE motif in red/green cyanobacteriochrome GAF domains enhance thermal reversion rates. . Biochemistry 61::144455
    [Crossref] [Google Scholar]
  56. 56.
    Jang J, Tang K, Youn J, McDonald S, Beyer HM, et al. 2023.. Engineering of bidirectional, cyanobacteriochrome-based light-inducible dimers (BICYCL)s. . Nat. Methods 20::43241
    [Crossref] [Google Scholar]
  57. 57.
    Jenkins AJ, Gottlieb SM, Chang CW, Hayer RJ, Martin SS, et al. 2019.. Conservation and diversity in the secondary forward photodynamics of red/green cyanobacteriochromes. . Photochem. Photobiol. Sci. 18::253952
    [Crossref] [Google Scholar]
  58. 58.
    Jenkins AJ, Gottlieb SM, Chang CW, Kim PW, Hayer RJ, et al. 2020.. Conservation and diversity in the primary reverse photodynamics of the canonical red/green cyanobacteriochrome family. . Biochemistry 59::401528
    [Crossref] [Google Scholar]
  59. 59.
    Kashimoto T, Miyake K, Sato M, Maeda K, Matsumoto C, et al. 2020.. Acclimation process of the chlorophyll d-bearing cyanobacterium Acaryochloris marina to an orange light environment revealed by transcriptomic analysis and electron microscopic observation. . J. Gen. Appl. Microbiol. 66::10615
    [Crossref] [Google Scholar]
  60. 60.
    Kehoe DM, Grossman AR. 1996.. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. . Science 273::140912
    [Crossref] [Google Scholar]
  61. 61.
    Kehoe DM, Gutu A. 2006.. Responding to color: the regulation of complementary chromatic adaptation. . Annu. Rev. Plant Biol. 57::12750
    [Crossref] [Google Scholar]
  62. 62.
    Kianianmomeni A, ed. 2016.. Optogenetics: Methods and Protocols. New York:: Springer. 402 pp.
    [Google Scholar]
  63. 63.
    Kim PW, Freer LH, Rockwell NC, Martin SS, Lagarias JC, Larsen DS. 2012.. Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 1. Forward dynamics. . Biochemistry 51::60818
    [Crossref] [Google Scholar]
  64. 64.
    Kim PW, Freer LH, Rockwell NC, Martin SS, Lagarias JC, Larsen DS. 2012.. Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 2. Reverse dynamics. . Biochemistry 51::61930
    [Crossref] [Google Scholar]
  65. 65.
    Kim PW, Freer LH, Rockwell NC, Martin SS, Lagarias JC, Larsen DS. 2012.. Second-chance initiation dynamics of the cyanobacterial photocycle in the NpR6012 GAF4 domain of Nostoc punctiforme. . J. Am. Chem. Soc. 134::13033
    [Crossref] [Google Scholar]
  66. 66.
    Kim PW, Rockwell NC, Martin SS, Lagarias JC, Larsen DS. 2014.. Dynamic inhomogeneity in the photodynamics of cyanobacterial phytochrome Cph1. . Biochemistry 53::281826
    [Crossref] [Google Scholar]
  67. 67.
    Kirpich JS, Chang CW, Franse J, Yu Q, Escobar FV, et al. 2021.. Comparison of the forward and reverse photocycle dynamics of two highly similar canonical red/green cyanobacteriochromes reveals unexpected differences. . Biochemistry 60::27488
    [Crossref] [Google Scholar]
  68. 68.
    Kirpich JS, Chang CW, Madsen D, Gottlieb SM, Martin SS, et al. 2018.. Noncanonical photodynamics of the orange/green cyanobacteriochrome power sensor NpF2164g7 from the PtxD phototaxis regulator of Nostoc punctiforme. . Biochemistry 57::263648
    [Crossref] [Google Scholar]
  69. 69.
    Kumarapperuma I, Joseph KL, Wang C, Biju LM, Tom IP, et al. 2022.. Crystal structure and molecular mechanism of an E/F type bilin lyase-isomerase. . Structure 30::56474.e3
    [Crossref] [Google Scholar]
  70. 70.
    Kuwasaki Y, Miyake K, Fushimi K, Takeda Y, Ueda Y, et al. 2019.. Protein engineering of dual-Cys cyanobacteriochrome AM1_1186g2 for biliverdin incorporation and far-red/blue reversible photoconversion. . Int. J. Mol. Sci. 20::2935
    [Crossref] [Google Scholar]
  71. 71.
    Larsen B, Hofmann R, Camacho IS, Clarke RW, Lagarias JC, et al. 2023.. Highlighter: an optogenetic system for high-resolution gene expression control in plants. . PLOS Biol. 21::e3002303
    [Crossref] [Google Scholar]
  72. 72.
    Ledermann B, Schwan M, Sommerkamp JA, Hofmann E, Beja O, Frankenberg-Dinkel N. 2018.. Evolution and molecular mechanism of four-electron reducing ferredoxin-dependent bilin reductases from oceanic phages. . FEBS J. 285::33956
    [Crossref] [Google Scholar]
  73. 73.
    Li X, Fleetwood AD, Bayas C, Bilwes AM, Ortega DR, et al. 2013.. The 3.2 Å resolution structure of a receptor: CheA:CheW signaling complex defines overlapping binding sites and key residue interactions within bacterial chemosensory arrays. . Biochemistry 52::385265
    [Crossref] [Google Scholar]
  74. 74.
    Lim S, Rockwell NC, Martin SS, Dallas JL, Lagarias JC, Ames JB. 2014.. Photoconversion changes bilin chromophore conjugation and protein secondary structure in the violet/orange cyanobacteriochrome NpF2163g3. . Photochem. Photobiol. Sci. 13::95162
    [Crossref] [Google Scholar]
  75. 75.
    Lim S, Yu Q, Gottlieb SM, Chang C-W, Rockwell NC, et al. 2018.. Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4. . PNAS 115::438792
    [Crossref] [Google Scholar]
  76. 76.
    Ma Q, Hua HH, Chen Y, Liu BB, Kramer AL, et al. 2012.. A rising tide of blue-absorbing biliprotein photoreceptors: characterization of seven such bilin-binding GAF domains in Nostoc sp. PCC7120. . FEBS J. 279::4095108
    [Crossref] [Google Scholar]
  77. 77.
    Miyake K, Fushimi K, Kashimoto T, Maeda K, Win NN, et al. 2020.. Functional diversification of two bilin reductases for light perception and harvesting in unique cyanobacterium Acaryochloris marina MBIC 11017. . FEBS J. 287::401631
    [Crossref] [Google Scholar]
  78. 78.
    Miyake K, Kimura H, Narikawa R. 2022.. Identification of significant residues for intermediate accumulation in phycocyanobilin synthesis. . Photochem. Photobiol. Sci. 21::43746
    [Crossref] [Google Scholar]
  79. 79.
    Moreno MV, Rockwell NC, Mora M, Fisher AJ, Lagarias JC. 2020.. A far-red cyanobacteriochrome lineage specific for verdins. . PNAS 117::2796270
    [Crossref] [Google Scholar]
  80. 80.
    Murphy JT, Lagarias JC. 1997.. The phytofluors: a new class of fluorescent protein probes. . Curr. Biol. 7::87076
    [Crossref] [Google Scholar]
  81. 81.
    Nagae T, Unno M, Koizumi T, Miyanoiri Y, Fujisawa T, et al. 2021.. Structural basis of the protochromic green/red photocycle of the chromatic acclimation sensor RcaE. . PNAS 118::e2024583118
    [Crossref] [Google Scholar]
  82. 82.
    Nakajima M, Abe K, Ferri S, Sode K. 2016.. Development of a light-regulated cell-recovery system for non-photosynthetic bacteria. . Microbes Cell Fact. 15::31
    [Crossref] [Google Scholar]
  83. 83.
    Nakajima M, Ferri S, Rogner M, Sode K. 2016.. Construction of a miniaturized chromatic acclimation sensor from cyanobacteria with reversed response to a light signal. . Sci. Rep. 6::37595
    [Crossref] [Google Scholar]
  84. 84.
    Nakane D, Enomoto G, Bahre H, Hirose Y, Wilde A, Nishizaka T. 2022.. Thermosynechococcus switches the direction of phototaxis by a c-di-GMP-dependent process with high spatial resolution. . eLife 11::e73405
    [Crossref] [Google Scholar]
  85. 85.
    Narikawa R, Enomoto G, Win NN, Fushimi K, Ikeuchi M. 2014.. A new type of dual-Cys cyanobacteriochrome GAF domain found in cyanobacterium Acaryochloris marina, which has an unusual red/blue reversible photoconversion cycle. . Biochemistry 53::505159
    [Crossref] [Google Scholar]
  86. 86.
    Narikawa R, Fukushima Y, Ishizuka T, Itoh S, Ikeuchi M. 2008.. A novel photoactive GAF domain of cyanobacteriochrome AnPixJ that shows reversible green/red photoconversion. . J. Mol. Biol. 380::84455
    [Crossref] [Google Scholar]
  87. 87.
    Narikawa R, Ishizuka T, Muraki N, Shiba T, Kurisu G, Ikeuchi M. 2013.. Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism. . PNAS 110::91823
    [Crossref] [Google Scholar]
  88. 88.
    Narikawa R, Nakajima T, Aono Y, Fushimi K, Enomoto G, et al. 2015.. A biliverdin-binding cyanobacteriochrome from the chlorophyll d-bearing cyanobacterium Acaryochloris marina. . Sci. Rep. 5::7950
    [Crossref] [Google Scholar]
  89. 89.
    Narikawa R, Suzuki F, Yoshihara S, Higashi SI, Watanabe M, Ikeuchi M. 2011.. Novel photosensory two-component system (PixA-NixB-NixC) involved in the regulation of positive and negative phototaxis of cyanobacterium Synechocystis sp. PCC 6803.. Plant Cell Physiol. 52::221424
    [Crossref] [Google Scholar]
  90. 90.
    Ng WO, Grossman AR, Bhaya D. 2003.. Multiple light inputs control phototaxis in Synechocystis sp. strain PCC6803. . J. Bacteriol. 185::1599607
    [Crossref] [Google Scholar]
  91. 91.
    Nultsch W, Schuchart H, Koenig F. 1983.. Effects of sodium azide on phototaxis of the blue-green alga Anabaena variabilis and consequences to the two-photoreceptor systems-hypothesis. . Arch. Microbiol. 134::3337
    [Crossref] [Google Scholar]
  92. 92.
    Oliinyk OS, Pletnev S, Baloban M, Verkhusha VV. 2023.. Development of bright red-shifted miRFP704nano using structural analysis of miRFPnano proteins. . Protein Sci. 32::e4709
    [Crossref] [Google Scholar]
  93. 93.
    Oliinyk OS, Shemetov AA, Pletnev S, Shcherbakova DM, Verkhusha VV. 2019.. Smallest near-infrared fluorescent protein evolved from cyanobacteriochrome as versatile tag for spectral multiplexing. . Nat. Commun. 10::279
    [Crossref] [Google Scholar]
  94. 94.
    Osoegawa S, Miyoshi R, Watanabe K, Hirose Y, Fujisawa T, et al. 2019.. Identification of the deprotonated pyrrole nitrogen of the bilin-based photoreceptor by Raman spectroscopy with an advanced computational analysis. . J. Phys. Chem. B 123::324247
    [Crossref] [Google Scholar]
  95. 95.
    Pollard AM, Bilwes AM, Crane BR. 2009.. The structure of a soluble chemoreceptor suggests a mechanism for propagating conformational signals. . Biochemistry 48::193644
    [Crossref] [Google Scholar]
  96. 96.
    Priyadarshini N, Steube N, Wiens D, Narikawa R, Wilde A, et al. 2023.. Evidence for an early green/red photocycle that precedes the diversification of GAF domain photoreceptor cyanobacteriochromes. . Photochem. Photobiol. Sci. 22::141527
    [Crossref] [Google Scholar]
  97. 97.
    Ramakrishnan P, Tabor JJ. 2016.. Repurposing Synechocystis PCC6803 UirS-UirR as a UV-violet/green photoreversible transcriptional regulatory tool in E. coli. . ACS Synth. Biol. 5::73340
    [Crossref] [Google Scholar]
  98. 98.
    Risser DD. 2023.. Hormogonium development and motility in filamentous cyanobacteria. . Appl. Environ. Microbiol. 89::e0039223
    [Crossref] [Google Scholar]
  99. 99.
    Rockwell NC, Lagarias JC. 2010.. A brief history of phytochromes. . ChemPhysChem 11::117280
    [Crossref] [Google Scholar]
  100. 100.
    Rockwell NC, Lagarias JC. 2020.. Phytochrome evolution in 3D: deletion, duplication, and diversification. . New Phytol. 225::2283300
    [Crossref] [Google Scholar]
  101. 101.
    Rockwell NC, Lagarias JC. 2023.. Cyanobacteriochromes from Gloeobacterales provide new insight into the diversification of cyanobacterial photoreceptors. . J. Mol. Biol. 436::168313
    [Crossref] [Google Scholar]
  102. 102.
    Rockwell NC, Martin SS, Feoktistova K, Lagarias JC. 2011.. Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. . PNAS 108::1185459
    [Crossref] [Google Scholar]
  103. 103.
    Rockwell NC, Martin SS, Gan F, Bryant DA, Lagarias JC. 2015.. NpR3784 is the prototype for a distinctive group of red/green cyanobacteriochromes using alternative Phe residues for photoproduct tuning. . Photochem. Photobiol. Sci. 14::25869
    [Crossref] [Google Scholar]
  104. 104.
    Rockwell NC, Martin SS, Gulevich AG, Lagarias JC. 2012.. Phycoviolobilin formation and spectral tuning in the DXCF cyanobacteriochrome subfamily. . Biochemistry 51::144963
    [Crossref] [Google Scholar]
  105. 105.
    Rockwell NC, Martin SS, Gulevich AG, Lagarias JC. 2014.. Conserved phenylalanine residues are required for blue-shifting of cyanobacteriochrome photoproducts. . Biochemistry 53::311830
    [Crossref] [Google Scholar]
  106. 106.
    Rockwell NC, Martin SS, Lagarias JC. 2012.. Mechanistic insight into the photosensory versatility of DXCF cyanobacteriochromes. . Biochemistry 51::357685
    [Crossref] [Google Scholar]
  107. 107.
    Rockwell NC, Martin SS, Lagarias JC. 2012.. Red/green cyanobacteriochromes: sensors of color and power. . Biochemistry 51::966777
    [Crossref] [Google Scholar]
  108. 108.
    Rockwell NC, Martin SS, Lagarias JC. 2015.. Identification of DXCF cyanobacteriochrome lineages with predictable photocycles. . Photochem. Photobiol. Sci. 14::92941
    [Crossref] [Google Scholar]
  109. 109.
    Rockwell NC, Martin SS, Lagarias JC. 2016.. Identification of cyanobacteriochromes detecting far-red light. . Biochemistry 55::390719
    [Crossref] [Google Scholar]
  110. 110.
    Rockwell NC, Martin SS, Lagarias JC. 2017.. There and back again: loss and reacquisition of two-Cys photocycles in cyanobacteriochromes. . Photochem. Photobiol. 93::74154
    [Crossref] [Google Scholar]
  111. 111.
    Rockwell NC, Martin SS, Lagarias JC. 2023.. Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins. . PNAS 120::e2300770120
    [Crossref] [Google Scholar]
  112. 112.
    Rockwell NC, Martin SS, Li FW, Mathews S, Lagarias JC. 2017.. The phycocyanobilin chromophore of streptophyte algal phytochromes is synthesized by HY2. . New Phytol. 214::114557
    [Crossref] [Google Scholar]
  113. 113.
    Rockwell NC, Martin SS, Lim S, Lagarias JC, Ames JB. 2015.. Characterization of red/green cyanobacteriochrome NpR6012g4 by solution nuclear magnetic resonance spectroscopy: a hydrophobic pocket for the C15-E,anti chromophore in the photoproduct. . Biochemistry 54::377283
    [Crossref] [Google Scholar]
  114. 114.
    Rockwell NC, Martin SS, Lim S, Lagarias JC, Ames JB. 2015.. Characterization of red/green cyanobacteriochrome NpR6012g4 by solution nuclear magnetic resonance spectroscopy: a protonated bilin ring system in both photostates. . Biochemistry 54::2581600
    [Crossref] [Google Scholar]
  115. 115.
    Rockwell NC, Moreno MV, Martin SS, Lagarias JC. 2022.. Protein-chromophore interactions controlling photoisomerization in red/green cyanobacteriochromes. . Photochem. Photobiol. Sci. 21::47191
    [Crossref] [Google Scholar]
  116. 116.
    Rockwell NC, Njuguna SL, Roberts L, Castillo E, Parson VL, et al. 2008.. A second conserved GAF domain cysteine is required for the blue/green photoreversibility of cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus. . Biochemistry 47::730416
    [Crossref] [Google Scholar]
  117. 117.
    Rockwell NC, Su YS, Lagarias JC. 2006.. Phytochrome structure and signaling mechanisms. . Annu. Rev. Plant Biol. 57::83758
    [Crossref] [Google Scholar]
  118. 118.
    Ruf J, Bindschedler F, Buhrke D. 2023.. The molecular mechanism of light-induced bond formation and breakage in the cyanobacteriochrome TePixJ. . Phys. Chem. Chem. Phys. 25::601624
    [Crossref] [Google Scholar]
  119. 119.
    Sanfilippo JE, Nguyen AA, Karty JA, Shukla A, Schluchter WM, et al. 2016.. Self-regulating genomic island encoding tandem regulators confers chromatic acclimation to marine Synechococcus. . PNAS 113::607782
    [Crossref] [Google Scholar]
  120. 120.
    Sato T, Kikukawa T, Miyoshi R, Kajimoto K, Yonekawa C, et al. 2019.. Protochromic absorption changes in the two-cysteine photocycle of a blue/orange cyanobacteriochrome. . J. Biol. Chem. 294::1890922
    [Crossref] [Google Scholar]
  121. 121.
    Savakis P, De Causmaecker S, Angerer V, Ruppert U, Anders K, et al. 2012.. Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803. . Mol. Microbiol. 85::23951
    [Crossref] [Google Scholar]
  122. 122.
    Schmidl SR, Sheth RU, Wu A, Tabor JJ. 2014.. Refactoring and optimization of light-switchable Escherichia coli two-component systems. . ACS Synth. Biol. 3::82031
    [Crossref] [Google Scholar]
  123. 123.
    Schuergers N, Lenn T, Kampmann R, Meissner MV, Esteves T, et al. 2016.. Cyanobacteria use micro-optics to sense light direction. . eLife 5::e12620
    [Crossref] [Google Scholar]
  124. 124.
    Shin H, Ren Z, Zeng X, Bandara S, Yang X. 2019.. Structural basis of molecular logic OR in a dual-sensor histidine kinase. . PNAS 116::1997382
    [Crossref] [Google Scholar]
  125. 125.
    Slavov C, Xu X, Zhao K-H, Gärtner W, Wachtveitl J. 2015.. Detailed insight into the ultrafast photoconversion of the cyanobacteriochrome Slr1393 from Synechocystis sp. . Biochim. Biophys. Acta Bioenerg. 1847::133544
    [Crossref] [Google Scholar]
  126. 126.
    Song JY, Cho HS, Cho JI, Jeon JS, Lagarias JC, Park YI. 2011.. Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803.. PNAS 108::1078085
    [Crossref] [Google Scholar]
  127. 127.
    Suzuki T, Yoshimura M, Arai M, Narikawa R. 2024.. Crucial residue for tuning thermal relaxation kinetics in the biliverdin-binding cyanobacteriochrome photoreceptor revealed by site-saturation mutagenesis. . J. Mol. Biol. 436::168451
    [Crossref] [Google Scholar]
  128. 128.
    Suzuki T, Yoshimura M, Hoshino H, Fushimi K, Arai M, Narikawa R. 2023.. Introduction of reversible cysteine ligation ability to the biliverdin-binding cyanobacteriochrome photoreceptor. . FEBS J. 290::49995015
    [Crossref] [Google Scholar]
  129. 129.
    Tabor JJ, Levskaya A, Voigt CA. 2011.. Multichromatic control of gene expression in Escherichia coli. . J. Mol. Biol. 405::31524
    [Crossref] [Google Scholar]
  130. 130.
    Tandeau de Marsac N. 2003.. Phycobiliproteins and phycobilisomes: the early observations. . Photosynth. Res. 76::197205
    [Crossref] [Google Scholar]
  131. 131.
    Tu JM, Zhou M, Haessner R, Ploscher M, Eichacker L, et al. 2009.. Toward a mechanism for biliprotein lyases: revisiting nucleophilic addition to phycocyanobilin. . J. Am. Chem. Soc. 131::5399401
    [Crossref] [Google Scholar]
  132. 132.
    Wagner JR, Brunzelle JS, Forest KT, Vierstra RD. 2005.. A light-sensing knot revealed by the structure of the chromophore binding domain of phytochrome. . Nature 438::32531
    [Crossref] [Google Scholar]
  133. 133.
    Wang D, Li X, Zhang S, Wang L, Yang X, Zhong D. 2020.. Revealing the origin of multiphasic dynamic behaviors in cyanobacteriochrome. . PNAS 117::1973136
    [Crossref] [Google Scholar]
  134. 134.
    Wedemayer GJ, Kidd DG, Glazer AN. 1996.. Cryptomonad biliproteins: bilin types and locations. . Photosynth. Res. 48::16370
    [Crossref] [Google Scholar]
  135. 135.
    Wei J, Jin F. 2022.. Illuminating bacterial behaviors with optogenetics. . Curr. Opin. Solid State Mater. Sci. 26::101023
    [Crossref] [Google Scholar]
  136. 136.
    Wiebeler C, Rao AG, Gärtner W, Schapiro I. 2019.. The effective conjugation length is responsible for the red/green spectral tuning in the cyanobacteriochrome Slr1393g3. . Angew. Chem. Int. Ed. Engl. 58::193438
    [Crossref] [Google Scholar]
  137. 137.
    Wiltbank LB, Kehoe DM. 2016.. Two cyanobacterial photoreceptors regulate photosynthetic light harvesting by sensing teal, green, yellow, and red light. . mBio 7::e02130-15
    [Crossref] [Google Scholar]
  138. 138.
    Wiltbank LB, Kehoe DM. 2019.. Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. . Nat. Rev. Microbiol. 17::3750
    [Crossref] [Google Scholar]
  139. 139.
    Xu X, Port A, Wiebeler C, Zhao K-H, Schapiro I, Gärtner W. 2020.. Structural elements regulating the photochromicity in a cyanobacteriochrome. . PNAS 117::243240
    [Crossref] [Google Scholar]
  140. 140.
    Xu X-L, Gutt A, Mechelke J, Raffelberg S, Tang K, et al. 2014.. Combined mutagenesis and kinetics characterization of the bilin-binding GAF domain of the protein Slr1393 from the cyanobacterium Synechocystis PCC6803. . ChemBioChem 15::119099
    [Crossref] [Google Scholar]
  141. 141.
    Yang Y, Lam V, Adomako M, Simkovsky R, Jakob A, et al. 2018.. Phototaxis in a wild isolate of the cyanobacterium Synechococcus elongatus. . PNAS 115::E1237887
    [Google Scholar]
  142. 142.
    Yeh K-C, Wu S-H, Murphy JT, Lagarias JC. 1997.. A cyanobacterial phytochrome two-component light sensory system. . Science 277::15058
    [Crossref] [Google Scholar]
  143. 143.
    Yoshihara S, Geng X, Ikeuchi M. 2002.. pilG gene cluster and split pilL genes involved in pilus biogenesis, motility and genetic transformation in the cyanobacterium Synechocystis sp. PCC 6803. . Plant Cell Physiol. 43::51321
    [Crossref] [Google Scholar]
  144. 144.
    Yoshihara S, Ikeuchi M. 2004.. Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. . Photochem. Photobiol. Sci. 3::51218
    [Crossref] [Google Scholar]
  145. 145.
    Yoshihara S, Katayama M, Geng X, Ikeuchi M. 2004.. Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue- and green-absorbing forms. . Plant Cell Physiol. 45::172937
    [Crossref] [Google Scholar]
  146. 146.
    Yoshihara S, Shimada T, Matsuoka D, Zikihara K, Kohchi T, Tokutomi S. 2006.. Reconstitution of blue-green reversible photoconversion of a cyanobacterial photoreceptor, PixJ1, in phycocyanobilin-producing Escherichia coli. . Biochemistry 45::377584
    [Crossref] [Google Scholar]
  147. 147.
    Yoshihara S, Suzuki F, Fujita H, Geng XX, Ikeuchi M. 2000.. Novel putative photoreceptor and regulatory genes required for the positive phototactic movement of the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. . Plant Cell Physiol. 41::1299304
    [Crossref] [Google Scholar]
  148. 148.
    Zhang W, Willows RD, Deng R, Li Z, Li M, et al. 2021.. Bilin-dependent regulation of chlorophyll biosynthesis by GUN4. . PNAS 118::e2104443118
    [Crossref] [Google Scholar]
  149. 149.
    Zhao C, Gan F, Shen G, Bryant DA. 2015.. RfpA, RfpB, and RfpC are the master control elements of far-red light photoacclimation (FaRLiP). . Front. Microbiol. 6::1303
    [Crossref] [Google Scholar]
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