Interrelated modules in cyanobacterial photosynthesis: The carbon-concentrating mechanism, photorespiration, and light perception

Journal of Experimental Botany

Volumn 67, Issue 10, 2016, Pages 2931-2940

  Montgomery, Beronda L ^a,b   Lechno Yossef, Sigal ^a   Kerfeld, Cheryl A ^a,b,c,d  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Carbon concentrating mechanisms; Complementary chromatic acclimation; Cyanobacteria; Module; Photoreceptor; Photorespiration; Photosynthesis; Phytochrome

Indexed keywords

CARBON; VISUAL PROTEINS AND PIGMENTS;

CYANOBACTERIUM; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHOTOSYNTHETIC PHOSPHORYLATION; PHYSIOLOGY;

CARBON; CYANOBACTERIA; LIGHT; PHOTOPHOSPHORYLATION; PHOTORECEPTORS, PLANT; PHOTOSYNTHESIS;

EID: 84969945360     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw162     Document Type: Review

References (77)

1. Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, Cournac L, Aro E-M. 2011. Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. Journal of Biological Chemistry 286, 24007-24014
2. Axen SD, Erbilgin O, Kerfeld CA. 2014. A taxonomy of bacterial microcompartment loci constructed by a novel scoring method. PLoS Computational Biology 10, 1003898
3. 2 concentrating mechanism in cyanobacteria and microalgae. Physiologia Plantarum 90, 529-536
4. Bennett A, Bogorad L. 1973. Complementary chromatic adaptation in a filamentous blue-green alga. Journal of Cell Biology 58, 419-435
5. Boldt R, Edner C, Kolukisaoglu Ü, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H. 2005. D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. The Plant Cell 17, 2413-2420
6. Bordowitz JR, Montgomery BL. 2008. Photoregulation of cellular morphology during complementary chromatic adaptation requires sensorkinase-class protein RcaE in Fremyella diplosiphon. Journal of Bacteriology 190, 4069-4074
7. Bordowitz JR, Whitaker MJ, Montgomery BL. 2010. Independence and interdependence of the photoregulation of pigmentation and development in Fremyella diplosiphon. Communicative and Integrative Biology 3, 151-153
8. Burnap RL, Nambudiri R, Holland S. 2013. Regulation of the carbonconcentrating mechanism in the cyanobacterium Synechocystis sp. PCC6803 in response to changing light intensity and inorganic carbon availability. Photosynthesis Research 118, 115-124
9. Busch AWU, Montgomery BL. 2015. The tryptophan-rich sensory protein (TSPO) is involved in stress-related and light-dependent processes in the cyanobacterium Fremyella diplosiphon. Frontiers in Microbiology 6, 1393
10. 2 leakage barrier. PLoS One 4, 0007521
11. Cameron JC, Sutter M, Kerfeld CA. 2014. The carboxysome: function, structure &cellular dynamics. In: Flores E, Herrero A, eds. The cell biology of cyanobacteria. Caister Academic Press: Norfolk, UK, 171-188
12. Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA. 2013. Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155, 1131-1140
13. Campbell D. 1996. Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. Microbiology 142, 1255-1263
14. 2 release. Plant Physiology 148, 786-795
15. Csete ME, Doyle JC. 2002. Reverse engineering of biological complexity. Science 295, 1664-1669
16. Danon A, Sánchez C.N., Apel K. 2006. Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 103, 17036-17041
17. Desai M, Hu J. 2008. Light induces peroxisome proliferation in Arabidopsis seedlings through the photoreceptor phytochrome A, the transcription factor HY5 HOMOLOG, and the peroxisomal protein PEROXIN11b. Plant Physiology 146, 1117-1127
18. Drews G, Niklowitz W. 1956. Cytology of Cyanophycea. II. Centroplasm and granular inclusions of Phormidium uncinatum. Archiv für Mikrobiologie 24, 147-162
19. Eisenhut M, Aguirre Wobeser E, Jonas L, Schubert H, Ibelings BW, Bauwe H, Matthijs HC, Hagemann M. 2007. Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiology 144, 1946-1959
20. 2 glycolate cycle and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiology 142, 333-342
21. Eisenhut M, Ruth W, Haimovich M, Bauwe H, Kaplan A, Hagemann M. 2008. The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proceedings of the National Academy of Sciences, USA 105, 17199-17204
22. Espie GS, Kimber MS. 2011. Carboxysomes: cyanobacterial RubisCO comes in small packages. Photosynthesis Research 109, 7-20
23. 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
24. Fraser HB. 2005. Modularity and evolutionary constraint on proteins. Nature Genetics 37, 351-352
25. Gaudana SB, Zarzycki J, Moparthi VK, Kerfeld CA. 2015. Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria. Photosynthasis Research 126, 99-109
26. Gutu A, Kehoe DM. 2012. Emerging perspectives on the mechanisms, regulation, and distribution of light color acclimation in cyanobacteria. Molecular Plant 5, 1-13
27. Hackenberg C, Kern R, Hüge J, Stal LJ, Tsuji Y, Kopka J, Shiraiwa Y, Bauwe H, Hagemann M. 2011. Cyanobacterial lactate oxidases serve as essential partners in N2 fixation and evolved into photorespiratory glycolate oxidases in plants. The Plant Cell 23, 2978-2990
28. Hartwell LH, Hopfield JJ, Leible S, Murray AW. 1999. From molecular to modular cell biology. Nature 402, C47-C52
29. Heinhorst S, Cannon GC, Shively JM. 2014. Carboxysomes and their structural organization in prokaryotes. In: Barton LL, Bazylinski DA, Xu H, eds. Nanomicrobiology Springer: New York, 75-101
30. Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M. 2001. DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. The Plant Cell 13, 793-806
31. Hirose Y, Rockwell NC, Nishiyama K, Narikawa R, Ukaji Y, Inomata K, Lagarias JC, Ikeuchi M. 2013. Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proceedings of the National Academy of Sciences, USA 110, 4974-4979
32. 2 cycle. Critical Reviews in Plant Sciences 5, 45-100
33. Iancu CV, Morris DM, Dou ZC, Heinhorst S, Cannon GC, Jensen GJ. 2010. Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. Journal of Molecular Biology 396, 105-117
34. Igamberdiev AU, Eprintsev AT, Fedorin DN, Popov VN. 2014. Phytochrome-mediated regulation of plant respiration and photorespiration. Plant, Cell and Environment 37, 290-299
35. Kangasjärvi S, Neukermans J, Li S, Aro E-M, Noctor G. 2012. Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany 63, 1619-1636
36. 2 concentrating mechanisms in photosynthetic microorganisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 539-570
37. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stabler N, Schonfeld B, Kreuzaler F, Peterhansel C. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology 25, 593-599
38. Kehoe DM, Grossman AR. 1996. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273, 1409-1412
39. Kerfeld CA. 2015. Plug-and-play for improving primary productivity. American Journal of Botany 102, 1949-1950
40. Kerfeld CA, Erbilgin O. 2015. Bacterial microcompartments and the modular construction of microbial metabolism. Trends in Microbiology 23, 22-34
41. Kerfeld CA, Melnicki M. 2016. Assembly, function and evolution of cyanobacterial carboxysomes. Current Opinion in Plant Biology 31, 66-75
42. Kerfeld CA, Sawaya MR, Tanaka S, Nguyen CV, Phillips M, Beeby M, Yeates TO. 2005. Protein structures forming the shell of primitive bacterial organelles. Science 309, 936-938
43. Kinney JN, Axen SD, Kerfeld CA. 2011. Comparative analysis of carboxysome shell proteins. Photosynthesis Research 109, 21-32
44. Long BM, Badger MR, Whitney SM, price GD. 2007. Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple RubisCO complexes with carboxysomal proteins CcmM and CcaA. Journal of Biological Chemistry 282, 29323-29335
45. Ludwig M, Sultemeyer D, Price GD. 2000. Isolation of ccmKLMN genes from the marine cyanobacterium, Synechococcus sp PCC7002 (Cyanobacteria), and evidence that CcmM is essential for carboxysome assembly. Journal of Phycology 36, 1109-1118
46. Maier A, Fahnenstich H, von Caemmerer S, Engqvist MKM, Weber APM, Flugge UI, Maurino VG. 2012. Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Frontiers in Plant Science 3, 00038
47. Mitchell MC, Meyer MT, Griffiths H. 2014. Dynamics of carbonconcentrating mechanism induction and protein relocalization during the dark-to-light transition in synchronized Chlamydomonas reinhardtii. Plant Physiology 166, 1073-1082
48. Montgomery BL. 2015. Light-dependent governance of cell shape dimensions in cyanobacteria. Frontiers in Microbiology 6, 514
49. 2-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
50. Norman EG, Colman B. 1991. Characterization of a malate dehydrogenase in the cyanobacterium Coccochloris peniocystis. Archives of Microbiology 156, 28-33
51. 2-induced activation of the bicarbonate transporter operon in cyanobacteria. Journal of Bacteriology 183, 1891-1898
52. Pattanaik B, Busch AWU, Hu P, Chen J, Montgomery BL. 2014. Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon. Microbiology 160, 992-1005
53. Pattanaik B, Whitaker MJ, Montgomery BL. 2012. Light quantity affects the regulation of cell shape in Fremyella diplosiphon. Frontiers in Microbiology 3, 170
54. Postius C, Neuschaefer-Rube O, Haid V, Böger P. 2001. N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance. FEMS Microbiology Ecology 37, 117-125
55. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59, 1441-1461
56. 2 fixation in cyanobacteria and some proteobacteria. Microbiology and Molecular Biology Reviews 77, 357-379
57. Rockwell NC, Lagarias JC. 2010. A brief history of phytochromes. ChemPhysChem 11, 1172-1180
58. Schlosser G. 2002. Modularity and the units of evolution. Theory in Biosciences 121, 1-80
59. Shi N, Li X, Fan T, Zhou H, Zhang D, Zhu H. 2014. Artificial chloroplast: Au/chloroplast-morph-TiO2 with fast electron transfer and enhanced photocatalytic activity. International Journal of Hydrogen Energy 39, 5617-5624
60. 2-fixing photorespiratory bypass into a cyanobacterium. Journal of Biological Chemistry 289, 9493-9500
61. 2-limited conditions. Plant Physiology 167, 472-480
62. Singh SP, Miller HL, Montgomery BL. 2013. Temporal dynamics of changes in reactive oxygen species (ROS) levels and cellular morphology are coordinated during complementary chromatic acclimation in Fremyella diplosiphon. Photosynthesis Research 118, 95-104
63. Singh SP, Montgomery BL. 2012. Reactive oxygen species are involved in the morphology-determining mechanism of Fremyella diplosiphon cells during complementary chromatic adaptation. Microbiology 158, 2235-2245
64. Slusarczyk AL, Lin A, Weiss R. 2012. Foundations for the design and implementation of synthetic genetic circuits. Nature Reviews Genetics 13, 406-420
65. 2-concentrating system in Chlamydomonas reinhardii. FEBS Letters 145, 41-44
66. Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S, Cannon GC, Yeates TO. 2008. Atomic-level models of the bacterial carboxysome shell. Science 319, 1083-1086
67. Tandeau de Marsac N. 1991. Chromatic adaptation by cyanobacteria. In: Bogorad L, Vasil IK, eds. Cell culture and somatic cell genetics of plants , Vol. 7. Academic Press Inc: New York, 417-446
68. Tepperman JM, Hudson ME, Khanna R, Zhu T, Chang SH, Wang X, Quail PH. 2004. Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. The Plant Journal 38, 725-739
69. Terauchi K, Montgomery BL, Grossman AR, Lagarias JC, Kehoe DM. 2004. RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Molecular Microbiology 51, 567-577
70. Thum KE, Shin MJ, Palenchar PM, Kouranov A, Coruzzi GM. 2004. Genome-wide investigation of light and carbon signaling interactions in Arabidopsis. Genome Biology 5, R10
71. Timm S, Nunes-Nesi A, Pärnik T, Morgenthal K, Wienkoop S, Keerberg O, Weckwerth W, Kleczkowski LA, Fernie AR, Bauwe H. 2008. A cytosolic pathway for the conversion of hydroxypyruvate to glycerate during photorespiration in Arabidopsis. The Plant Cell 20, 2848-2859
72. 2 oxidative photosynthetic carbon cycle. Annual Review of Plant Physiology and Plant Molecular Biology 48, 1-25
73. Ulijasz AT, Vierstra RD. 2011. Phytochrome structure and photochemistry: recent advances toward a complete molecular picture. Current Opinion in Plant Biology 14, 498-506
74. Walters KJ, Whitaker MJ, Singh SP, Montgomery BL. 2013. Light intensity and reactive oxygen species are centrally involved in photoregulatory responses during complementary chromatic adaptation in Fremyella diplosiphon. Communicative and Integrative Biology 6, e25005
75. Yerrapragada S, Shukla A, Hallsworth-Pepin K, et al. 2015. Extreme sensory complexity encoded in the 10-Megabase draft genome sequence of the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601. Genome Announcements 3, e00355-00315
76. Zhong HH, Young JC, Pease EA, Hangarter RP, McClung CR. 1994. Interactions between light and the circadian clock in the regulation of CAT2 expression in Arabidopsis. Plant Physiology 104, 889-898
77. Zilliges Y, Kehr JC, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Borner T, Dittmann E. 2011. The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of microcystis under oxidative stress conditions. PLoS One 6, 0017615