Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases

Tian Y, Gao S, von der Heyde EL, Hallmann A, Nagel G (2018)
BMC Biology 16: 144.

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Background: The green algae Chlamydomonas reinhardtii and Volvox carteri are important models for studying light perception and response, expressing many different photoreceptors. More than 10 opsins were reported in C. reinhardtii, yet only two—the channelrhodopsins—were functionally characterized. Characterization of new opsins would help to understand the green algae photobiology and to develop new tools for optogenetics. Results: Here we report the characterization of a novel opsin family from these green algae: light-inhibited guanylyl cyclases regulated through a two-component-like phosphoryl transfer, called “two-component cyclase opsins” (2c-Cyclops). We prove the existence of such opsins in C. reinhardtii and V. carteri and show that they have cytosolic N- and C-termini, implying an eight-transmembrane helix structure. We also demonstrate that cGMP production is both light-inhibited and ATP-dependent. The cyclase activity of Cr2c-Cyclop1 is kept functional by the ongoing phosphorylation and phosphoryl transfer from the histidine kinase to the response regulator in the dark, proven by mutagenesis. Absorption of a photon inhibits the cyclase activity, most likely by inhibiting the phosphoryl transfer. Overexpression of Vc2c-Cyclop1 protein in V. carteri leads to significantly increased cGMP levels, demonstrating guanylyl cyclase activity of Vc2c-Cyclop1 in vivo. Live cell imaging of YFP-tagged Vc2c-Cyclop1 in V. carteri revealed a development-dependent, layer-like structure at the immediate periphery of the nucleus and intense spots in the cell periphery. Conclusions: Cr2c-Cyclop1 and Vc2c-Cyclop1 are light-inhibited and ATP-dependent guanylyl cyclases with an unusual eight-transmembrane helix structure of the type I opsin domain which we propose to classify as type Ib, in contrast to the 7 TM type Ia opsins. Overexpression of Vc2c-Cyclop1 protein in V. carteri led to a significant increase of cGMP, demonstrating enzyme functionality in the organism of origin. Fluorescent live cell imaging revealed that Vc2c-Cyclop1 is located in the periphery of the nucleus and in confined areas at the cell periphery.
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BMC Biology
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144
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Tian Y, Gao S, von der Heyde EL, Hallmann A, Nagel G. Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biology. 2018;16: 144.
Tian, Y., Gao, S., von der Heyde, E. L., Hallmann, A., & Nagel, G. (2018). Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biology, 16, 144. doi:10.1186/s12915-018-0613-5
Tian, Y., Gao, S., von der Heyde, E. L., Hallmann, A., and Nagel, G. (2018). Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biology 16:144.
Tian, Y., et al., 2018. Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biology, 16: 144.
Y. Tian, et al., “Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases”, BMC Biology, vol. 16, 2018, : 144.
Tian, Y., Gao, S., von der Heyde, E.L., Hallmann, A., Nagel, G.: Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases. BMC Biology. 16, : 144 (2018).
Tian, Yuehui, Gao, Shiqiang, von der Heyde, Eva Laura, Hallmann, Armin, and Nagel, Georg. “Two-component cyclase opsins of green algae are ATP-dependent and light-inhibited guanylyl cyclases”. BMC Biology 16 (2018): 144.
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124 References

Daten bereitgestellt von Europe PubMed Central.

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The rhodopsin-guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling.
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Channelrhodopsin-2, a directly light-gated cation-selective membrane channel.
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PMID: 14615590
A unique choanoflagellate enzyme rhodopsin exhibits light-dependent cyclic nucleotide phosphodiesterase activity.
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A blue-light photoreceptor mediates the feedback regulation of photosynthesis.
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Bistable retinal schiff base photodynamics of histidine kinase rhodopsin HKR1 from Chlamydomonas reinhardtii.
Penzkofer A, Luck M, Mathes T, Hegemann P., Photochem. Photobiol. 90(4), 2014
PMID: 24460585
Stable nuclear transformation of Pandorina morum.
Lerche K, Hallmann A., BMC Biotechnol. 14(), 2014
PMID: 25031031
Halorhodopsin is a light-driven chloride pump.
Schobert B, Lanyi JK., J. Biol. Chem. 257(17), 1982
PMID: 7107607
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Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL., BMC Bioinformatics 13(), 2012
PMID: 22708584
Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium.
Bogomolni RA, Spudich JL., Proc. Natl. Acad. Sci. U.S.A. 79(20), 1982
PMID: 6959114
The Chlamydomonas genome reveals the evolution of key animal and plant functions.
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR., Science 318(5848), 2007
PMID: 17932292
Cryptochrome photoreceptors in green algae: Unexpected versatility of mechanisms and functions.
Kottke T, Oldemeyer S, Wenzel S, Zou Y, Mittag M., J. Plant Physiol. 217(), 2017
PMID: 28619534
Nuclear transformation of Volvox carteri.
Schiedlmeier B, Schmitt R, Muller W, Kirk MM, Gruber H, Mages W, Kirk DL., Proc. Natl. Acad. Sci. U.S.A. 91(11), 1994
PMID: 8197189
Stable nuclear transformation of Gonium pectorale.
Lerche K, Hallmann A., BMC Biotechnol. 9(), 2009
PMID: 19591675
A Cyclic GMP-Dependent K+ Channel in the Blastocladiomycete Fungus Blastocladiella emersonii.
Avelar GM, Glaser T, Leonard G, Richards TA, Ulrich H, Gomes SL., Eukaryotic Cell 14(9), 2015
PMID: 26150416
Structure and monomer/dimer equilibrium for the guanylyl cyclase domain of the optogenetics protein RhoGC.
Kumar RP, Morehouse BR, Fofana J, Trieu MM, Zhou DH, Lorenz MO, Oprian DD., J. Biol. Chem. 292(52), 2017
PMID: 29118188
Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium Beggiatoa.
Stierl M, Stumpf P, Udwari D, Gueta R, Hagedorn R, Losi A, Gartner W, Petereit L, Efetova M, Schwarzel M, Oertner TG, Nagel G, Hegemann P., J. Biol. Chem. 286(2), 2010
PMID: 21030594
The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses.
Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P., J. Cell. Sci. 114(Pt 21), 2001
PMID: 11719552
"Vision" in single-celled algae.
Kateriya S, Nagel G, Bamberg E, Hegemann P., News Physiol. Sci. 19(), 2004
PMID: 15143209
Evolution of sexes from an ancestral mating-type specification pathway.
Geng S, De Hoff P, Umen JG., PLoS Biol. 12(7), 2014
PMID: 25003332
Purification and Characterization of RhoPDE, a Retinylidene/Phosphodiesterase Fusion Protein and Potential Optogenetic Tool from the Choanoflagellate Salpingoeca rosetta.
Lamarche LB, Kumar RP, Trieu MM, Devine EL, Cohen-Abeles LE, Theobald DL, Oprian DD., Biochemistry 56(43), 2017
PMID: 28976747
OligoCalc: an online oligonucleotide properties calculator.
Kibbe WA., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17452344
Functions of a new photoreceptor membrane.
Oesterhelt D, Stoeckenius W., Proc. Natl. Acad. Sci. U.S.A. 70(10), 1973
PMID: 4517939
Stable nuclear transformation of Eudorina elegans.
Lerche K, Hallmann A., BMC Biotechnol. 13(), 2013
PMID: 23402598
A light-driven sodium ion pump in marine bacteria.
Inoue K, Ono H, Abe-Yoshizumi R, Yoshizawa S, Ito H, Kogure K, Kandori H., Nat Commun 4(), 2013
PMID: 23575682
Targeted expression of nuclear transgenes in Chlamydomonas reinhardtii with a versatile, modular vector toolkit.
Lauersen KJ, Kruse O, Mussgnug JH., Appl. Microbiol. Biotechnol. 99(8), 2015
PMID: 25586579
Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri.
Zhang F, Prigge M, Beyriere F, Tsunoda SP, Mattis J, Yizhar O, Hegemann P, Deisseroth K., Nat. Neurosci. 11(6), 2008
PMID: 18432196
Chlamyrhodopsin represents a new type of sensory photoreceptor.
Deininger W, Kroger P, Hegemann U, Lottspeich F, Hegemann P., EMBO J. 14(23), 1995
PMID: 8846778
Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp.
Gao S, Nagpal J, Schneider MW, Kozjak-Pavlovic V, Nagel G, Gottschalk A., Nat Commun 6(), 2015
PMID: 26345128
A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by ultraviolet and blue light.
Luck M, Mathes T, Bruun S, Fudim R, Hagedorn R, Tran Nguyen TM, Kateriya S, Kennis JT, Hildebrandt P, Hegemann P., J. Biol. Chem. 287(47), 2012
PMID: 23027869
Photochemical chromophore isomerization in histidine kinase rhodopsin HKR1.
Luck M, Bruun S, Keidel A, Hegemann P, Hildebrandt P., FEBS Lett. 589(10), 2015
PMID: 25836735
Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii.
Sineshchekov OA, Jung KH, Spudich JL., Proc. Natl. Acad. Sci. U.S.A. 99(13), 2002
PMID: 12060707
Structure, signaling mechanism and regulation of the natriuretic peptide receptor guanylate cyclase.
Misono KS, Philo JS, Arakawa T, Ogata CM, Qiu Y, Ogawa H, Young HS., FEBS J. 278(11), 2011
PMID: 21375693
Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization.
Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, Yoshida K, Watanabe M, Daiyasu H, Toh H, Asamizu E, Tabata S, Miura K, Fukuzawa H, Nakamura S, Takahashi T., Biochem. Biophys. Res. Commun. 301(3), 2003
PMID: 12565839
Rhodopsin-like protein from the purple membrane of Halobacterium halobium.
Oesterhelt D, Stoeckenius W., Nature New Biol. 233(39), 1971
PMID: 4940442
NEUROSCIENCE. Natural light-gated anion channels: A family of microbial rhodopsins for advanced optogenetics.
Govorunova EG, Sineshchekov OA, Janz R, Liu X, Spudich JL., Science 349(6248), 2015
PMID: 26113638
Crystal structure of the guanylyl cyclase Cya2.
Rauch A, Leipelt M, Russwurm M, Steegborn C., Proc. Natl. Acad. Sci. U.S.A. 105(41), 2008
PMID: 18840690
Expression, purification, and spectral tuning of RhoGC, a retinylidene/guanylyl cyclase fusion protein and optogenetics tool from the aquatic fungus Blastocladiella emersonii.
Trieu MM, Devine EL, Lamarche LB, Ammerman AE, Greco JA, Birge RR, Theobald DL, Oprian DD., J. Biol. Chem. 292(25), 2017
PMID: 28473465
Targeting of Photoreceptor Genes in Chlamydomonas reinhardtii via Zinc-Finger Nucleases and CRISPR/Cas9.
Greiner A, Kelterborn S, Evers H, Kreimer G, Sizova I, Hegemann P., Plant Cell 29(10), 2017
PMID: 28978758
A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus.
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