The transcriptional regulator RbcR controls ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) genes in the cyanobacterium Synechocystis sp. PCC 6803.
Synechocystis
Calvin-Benson-Bassham cycle
RuBisCO
cyanobacteria
gene regulation
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
received:
19
11
2021
accepted:
19
03
2022
pubmed:
5
4
2022
medline:
18
6
2022
entrez:
4
4
2022
Statut:
ppublish
Résumé
Oxygenic photosynthesis evolved in cyanobacteria, primary producers of striking ecological importance. Like plants, cyanobacteria use the Calvin-Benson-Bassham cycle for CO
Substances chimiques
Ribulosephosphates
0
Carbon Dioxide
142M471B3J
ribulose-1,5 diphosphate
2002-28-0
Oxygenases
EC 1.13.-
Ribulose-Bisphosphate Carboxylase
EC 4.1.1.39
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
432-445Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.
Références
Appel J, Hueren V, Boehm M, Gutekunst K. 2020. Cyanobacterial in vivo solar hydrogen production using a photosystem I-hydrogenase (PsaD-HoxYH) fusion complex. Nature Energy 5: 458-467.
Ataeian M, Liu Y, Canon-Rubio KA, Nightingale M, Strous M, Vadlamani A. 2019. Direct capture and conversion of CO2 from air by growing a cyanobacterial consortium at pH up to 11.2. Biotechnology and Bioengineering 116: 1604-1611.
Badger MR, Hanson D, Price GD. 2002. Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Functional Plant Biology: FPB 29: 161-173.
Badger MR, Price GD. 2003. CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. Journal of Experimental Botany 54: 609-622.
Bar-On YM, Milo R. 2019. The global mass and average rate of rubisco. Proceedings of the National Academy of Sciences, USA 116: 4738-4743.
van den Bergh ER, Dijkhuizen L, Meijer WG. 1993. CbbR, a LysR-type transcriptional activator, is required for expression of the autotrophic CO2 fixation enzymes of Xanthobacter flavus. Journal of Bacteriology 175: 6097-6104.
Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.
Burnap RL, Hagemann M, Kaplan A. 2015. Regulation of CO2 concentrating mechanism in cyanobacteria. Life 5: 348-371.
Colman B. 1989. Photosynthetic carbon assimilation and the suppression of photorespiration in the cyanobacteria. Aquatic Botany 34: 211-231.
Cramm R, Pohlmann A, Friedrich B. 1999. Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Letters 460: 6-10.
Dai W, Chen M, Myers C, Ludtke SJ, Pettitt BM, King JA, Schmid MF, Chiu W. 2018. Visualizing individual RuBisCO and Its assembly into carboxysomes in marine cyanobacteria by cryo-electron tomography. Journal of Molecular Biology 430: 4156-4167.
Dangel AW, Gibson JL, Janssen AP, Tabita FR. 2005. Residues that influence in vivo and in vitro CbbR function in Rhodobacter sphaeroides and identification of a specific region critical for co-inducer recognition. Molecular Microbiology 57: 1397-1414.
Dangel AW, Tabita FR. 2009. Protein-protein interactions between CbbR and RegA (PrrA), transcriptional regulators of the cbb operons of Rhodobacter sphaeroides. Molecular Microbiology 71: 717-729.
Dangel AW, Tabita FR. 2015. CbbR, the master regulator for microbial carbon dioxide fixation. Journal of Bacteriology 197: 3488-3498.
Deghmane A-E, Giorgini D, Maigre L, Taha M-K. 2004. Analysis in vitro and in vivo of the transcriptional regulator CrgA of Neisseria meningitidis upon contact with target cells. Molecular Microbiology 53: 917-927.
Dubbs P, Dubbs JM, Tabita FR. 2004. Effector-mediated interaction of CbbRI and CbbRII regulators with target sequences in Rhodobacter capsulatus. Journal of Bacteriology 186: 8026-8035.
Ducat DC, Way JC, Silver PA. 2011. Engineering cyanobacteria to generate high-value products. Trends in Biotechnology 29: 95-103.
Dutheil J, Saenkham P, Sakr S, Leplat C, Ortega-Ramos M, Bottin H, Cournac L, Cassier-Chauvat C, Chauvat F. 2012. The AbrB2 autorepressor, expressed from an atypical promoter, represses the hydrogenase operon to regulate hydrogen production in Synechocystis strain PCC6803. Journal of Bacteriology 194: 5423-5433.
Figge RM, Cassier-Chauvat C, Chauvat F, Cerff R. 2001. Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress. Molecular Microbiology 39: 455-468.
Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D et al. 2013. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences, USA 110: 9824-9829.
Foyer CH, Bloom AJ, Queval G, Noctor G. 2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology 60: 455-484.
García-Cañas R, Giner-Lamia J, Florencio FJ, López-Maury L. 2021. A protease-mediated mechanism regulates the cytochrome c6/plastocyanin switch in Synechocystis sp. PCC 6803. Proceedings of the National Academy of Sciences, USA 118: 229-240.
Gärtner K, Klähn S, Watanabe S, Mikkat S, Scholz I, Hess WR, Hagemann M. 2019. Cytosine N4-methylation via M.Ssp6803II is involved in the regulation of transcription, fine- tuning of DNA replication and DNA repair in the cyanobacterium Synechocystis sp. PCC 6803. Frontiers in Microbiology 10: 1233.
Georg J, Voß B, Scholz I, Mitschke J, Wilde A, Hess WR. 2009. Evidence for a major role of antisense RNAs in cyanobacterial gene regulation. Molecular Systems Biology 5: 305.
Gibson JL, Dubbs JM, Tabita FR. 2002. Differential expression of the CO2 fixation operons of Rhodobacter sphaeroides by the Prr/Reg two-component system during chemoautotrophic growth. Journal of Bacteriology 184: 6654-6664.
Gibson JL, Tabita FR. 1996. The molecular regulation of the reductive pentose phosphate pathway in proteobacteria and cyanobacteria. Archives of Microbiology 166: 141-150.
Gruber S, Schwab H, Heidinger P. 2017. CbbR and RegA regulate cbb operon transcription in Ralstonia eutropha H16. Journal of Biotechnology 257: 78-86.
Hagemann M, Hess WR. 2018. Systems and synthetic biology for the biotechnological application of cyanobacteria. Current Opinion in Biotechnology 49: 94-99.
Hagemann M, Kern R, Maurino VG, Hanson DT, Weber APM, Sage RF, Bauwe H. 2016. Evolution of photorespiration from cyanobacteria to land plants, considering protein phylogenies and acquisition of carbon concentrating mechanisms. Journal of Experimental Botany 67: 2963-2976.
Hein S, Scholz I, Voß B, Hess WR. 2013. Adaptation and modification of three CRISPR loci in two closely related cyanobacteria. RNA Biology 10: 852-864.
Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, Lamerdin J, Chisholm SW. 2001. The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynthesis Research 70: 53-71.
Hügler M, Sievert SM. 2011. Beyond the calvin cycle: autotrophic carbon fixation in the ocean. Annual Review of Marine Science 3: 261-289.
Jiang Y-L, Wang X-P, Sun H, Han S-J, Li W-F, Cui N, Lin G-M, Zhang J-Y, Cheng W, Cao D-D et al. 2018. Coordinating carbon and nitrogen metabolic signaling through the cyanobacterial global repressor NdhR. Proceedings of the National Academy of Sciences, USA 115: 403-408.
Joshi GS, Zianni M, Bobst CE, Tabita FR. 2013. Regulatory twist and synergistic role of metabolic coinducer- and response regulator-mediated CbbR-cbbI interactions in Rhodopseudomonas palustris CGA010. Journal of Bacteriology 195: 1381-1388.
Kinney JN, Axen SD, Kerfeld CA. 2011. Comparative analysis of carboxysome shell proteins. Photosynthesis Research 109: 21-32.
Klähn S, Orf I, Schwarz D, Matthiessen JKF, Kopka J, Hess WR, Hagemann M. 2015. Integrated transcriptomic and metabolomic characterization of the low-carbon response using an ndhR mutant of Synechocystis sp. PCC 6803. Plant Physiology 169: 1540-1556.
Krasikov V, Aguirre von Wobeser E, Dekker HL, Huisman J, Matthijs HCP. 2012. Time-series resolution of gradual nitrogen starvation and its impact on photosynthesis in the cyanobacterium Synechocystis PCC 6803. Physiologia Plantarum 145: 426-439.
Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
Lochowska A, Iwanicka-Nowicka R, Plochocka D, Hryniewicz MM. 2001. Functional dissection of the LysR-type CysB transcriptional regulator. Regions important for DNA binding, inducer response, oligomerization, and positive control. Journal of Biological Chemistry 276: 2098-2107.
Lochowska A, Iwanicka-Nowicka R, Zaim J, Witkowska-Zimny M, Bolewska K, Hryniewicz MM. 2004. Identification of activating region (AR) of Escherichia coli LysR-type transcription factor CysB and CysB contact site on RNA polymerase alpha subunit at the cysP promoter. Molecular Microbiology 53: 791-806.
Lyons TW, Reinhard CT, Planavsky NJ. 2014. The rise of oxygen in earth's early ocean and atmosphere. Nature 506: 307-315.
Maddocks SE, Oyston PCF. 2008. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609-3623.
McFarlane CR, Shah NR, Kabasakal BV, Echeverria B, Cotton CAR, Bubeck D, Murray JW. 2019. Structural basis of light-induced redox regulation in the Calvin-Benson cycle in cyanobacteria. Proceedings of the National Academy of Sciences, USA 116: 20984-20990.
Miller SR, Castenholz RW. 2000. Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Applied and Environmental Microbiology 66: 4222-4229.
Minoda A, Weber APM, Tanaka K, Miyagishima S. 2010. Nucleus-independent control of the rubisco operon by the plastid-encoded transcription factor Ycf30 in the red alga Cyanidioschyzon merolae. Plant Physiology 154: 1532-1540.
Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J, Voß B, Steglich C, Wilde A, Vogel J et al. 2011. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC 6803. Proceedings of the National Academy of Sciences, USA 108: 2124-2129.
Montoya JP, Holl CM, Zehr JP, Hansen A, Villareal TA, Capone DG. 2004. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430: 1027-1032.
Morone J, Alfeus A, Vasconcelos V, Martins R. 2019. Revealing the potential of cyanobacteria in cosmetics and cosmeceuticals - A new bioactive approach. Algal Research 41: 101541.
Nishimura T, Takahashi Y, Yamaguchi O, Suzuki H, Maeda S-I, Omata T. 2008. Mechanism of low CO2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Molecular Microbiology 68: 98-109.
Orf I, Schwarz D, Kaplan A, Kopka J, Hess WR, Hagemann M, Klähn S. 2016. CyAbrB2 contributes to the transcriptional regulation of low CO2 acclimation in Synechocystis sp. PCC 6803. Plant & Cell Physiology 57: 2232-2243.
Pandey KD, Shukla SP, Shukla PN, Giri DD, Singh JS, Singh P, Kashyap AK. 2004. Cyanobacteria in Antarctica: ecology, physiology and cold adaptation. Cellular and Molecular Biology 50: 575-584.
Park W, Jeon CO, Madsen EL. 2002. Interaction of NahR, a LysR-type transcriptional regulator, with the alpha subunit of RNA polymerase in the naphthalene degrading bacterium, Pseudomonas putida NCIB 9816-4. FEMS Microbiology Letters 213: 159-165.
Parsek MR, Ye RW, Pun P, Chakrabarty AM. 1994. Critical nucleotides in the interaction of a LysR-type regulator with its target promoter region. catBC promoter activation by CatR. Journal of Biological Chemistry 269: 11279-11284.
Picossi S, Belitsky BR, Sonenshein AL. 2007. Molecular mechanism of the regulation of Bacillus subtilis gltAB expression by GltC. Journal of Molecular Biology 365: 1298-1313.
Picossi S, Flores E, Herrero A. 2015. The LysR-type transcription factor PacR is a global regulator of photosynthetic carbon assimilation in Anabaena. Environmental Microbiology 17: 3341-3351.
Pierce J, Carlson TJ, Williams JG. 1989. A cyanobacterial mutant requiring the expression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. Proceedings of the National Academy of Sciences, USA 86: 5753-5757.
Pinto FL, Thapper A, Sontheim W, Lindblad P. 2009. Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Molecular Biology 10: 79.
Price GD, Badger MR, Woodger FJ, Long BM. 2008. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59: 1441-1461.
Puente-Sánchez F, Arce-Rodríguez A, Oggerin M, García-Villadangos M, Moreno-Paz M, Blanco Y, Rodríguez N, Bird L, Lincoln SA, Tornos F et al. 2018. Viable cyanobacteria in the deep continental subsurface. Proceedings of the National Academy of Sciences, USA 115: 10702-10707.
Raven JA. 2009. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology 56: 177-192.
Reed RH, Chudek JA, Foster R, Stewart WDP. 1984. Osmotic adjustment in cyanobacteria from hypersaline environments. Archives of Microbiology 138: 333-337.
Riediger M, Kadowaki T, Nagayama R, Georg J, Hihara Y, Hess WR. 2019. Biocomputational analyses and experimental validation identify the regulon controlled by the redox-responsive transcription factor RpaB. iScience 15: 316-331.
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111: 1-61.
Saper G, Kallmann D, Conzuelo F, Zhao F, Tóth TN, Liveanu V, Meir S, Szymanski J, Aharoni A, Schuhmann W et al. 2018. Live cyanobacteria produce photocurrent and hydrogen using both the respiratory and photosynthetic systems. Nature Communications 9: 2168.
Schell MA. 1993. Molecular biology of the LysR family of transcriptional regulators. Annual Review of Microbiology 47: 597-626.
Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T. 2002. Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. Journal of Biological Chemistry 277: 18658-18664.
Shively JM, vanKeulen G, Meijer WG. 1998. SOMETHING FROM ALMOST NOTHING: carbon dioxide fixation in chemoautotrophs. Annual Review of Microbiology 52: 191-230.
Skulberg O. 1996. Part 9. Terrestrial and limnic algae and cyanobacteria. Norsk Polarinstitutt Skrifter 198: 383-395.
Song K, Wei L, Liu J, Wang J, Qi H, Wen J. 2017. Engineering of the LysR family transcriptional regulator FkbR1 and its target gene to improve ascomycin production. Applied Microbiology and Biotechnology 101: 4581-4592.
Soo RM, Hemp J, Hugenholtz P. 2019. Evolution of photosynthesis and aerobic respiration in the cyanobacteria. Free Radical Biology & Medicine 140: 200-205.
Spreitzer RJ, Salvucci ME. 2002. RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology 53: 449-475.
Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G. 1971. Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriological Reviews 35: 171-205.
Stauffer LT, Stauffer GV. 2005. GcvA interacts with both the alpha and sigma subunits of RNA polymerase to activate the Escherichia coli gcvB gene and the gcvTHP operon. FEMS Microbiology Letters 242: 333-338.
Tabita FR. 1999. Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a different perspective. Photosynthesis Research 60: 1-28.
Tamoi M, Miyazaki T, Fukamizo T, Shigeoka S. 2005. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. The Plant Journal 42: 504-513.
Terazono K, Hayashi NR, Igarashi Y. 2001. CbbR, a LysR-type transcriptional regulator from Hydrogenophilus thermoluteolus, binds two cbb promoter regions. FEMS Microbiology Letters 198: 151-157.
Tomar V, Sidhu GK, Nogia P, Mehrotra R, Mehrotra S. 2017. Regulatory components of carbon concentrating mechanisms in aquatic unicellular photosynthetic organisms. Plant Cell Reports 36: 1671-1688.
Viswanathan P, Ueki T, Inouye S, Kroos L. 2007. Combinatorial regulation of genes essential for Myxococcus xanthus development involves a response regulator and a LysR-type regulator. Proceedings of the National Academy of Sciences, USA 104: 7969-7974.
Wang H-L, Postier BL, Burnap RL. 2004. Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of NdhR, a LysR family regulator. Journal of Biological Chemistry 279: 5739-5751.
Wijffels RH, Kruse O, Hellingwerf KJ. 2013. Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Current Opinion in Biotechnology 24: 405-413.
Wilson RL, Urbanowski ML, Stauffer GV. 1995. DNA binding sites of the LysR-type regulator GcvA in the gcv and gcvA control regions of Escherichia coli. Journal of Bacteriology 177: 4940-4946.
Zhang P, Eisenhut M, Brandt A-M, Carmel D, Silén HM, Vass I, Allahverdiyeva Y, Salminen TA, Aro E-M. 2012. Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24: 1952-1971.
Zinchenko V, Piven IV, Melnik V, Shestakov S. 1999. Vectors for the complementation analysis of cyanobacterial mutants. Russian Journal of Genetics 35: 228-232.