Light modulates the biosynthesis and organization of cyanobacterial carbon fixation machinery through photosynthetic electron flow

Plant Physiology

Volumn 171, Issue 1, 2016, Pages 530-541

  Sun, Yaqi ^a   Casella, Selene ^a   Fang, Yi ^a   Huang, Fang ^a   Faulkner, Matthew ^a   Barrett, Steve ^a   Liu, Lu Ning ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIURON; GREEN FLUORESCENT PROTEIN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

CARBON CYCLE; DRUG EFFECTS; ELECTRON TRANSPORT; FLUORESCENCE MICROSCOPY; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PROCEDURES; SYNECHOCOCCUS; TRANSGENIC ORGANISM;

CARBON CYCLE; DIURON; ELECTRON TRANSPORT; GREEN FLUORESCENT PROTEINS; LIGHT; MICROSCOPY, FLUORESCENCE; ORGANISMS, GENETICALLY MODIFIED; PHOTOSYNTHESIS; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SYNECHOCOCCUS;

EID: 84964857930     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00107     Document Type: Article

References (69)

1. Agarwal R, Ortleb S, Sainis JK, Melzer M (2009) Immunoelectron microscopy for locating calvin cycle enzymes in the thylakoids of synechocystis 6803. Mol Plant 2: 32-42
2. Aryal UK, Stöckel J, Krovvidi RK, Gritsenko MA, Monroe ME, Moore RJ, Koppenaal DW, Smith RD, Pakrasi HB, Jacobs JM(2011) Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across lightdark diurnal cycles. BMC Syst Biol 5: 194
3. Asayama M (2006) Regulatory system for light-responsive gene expression in photosynthesizing bacteria: cis-elements and trans-acting factors in transcription and post-transcription. Biosci Biotechnol Biochem 70: 565-573
4. Bobik TA, Lehman BP, Yeates TO (2015) Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways. Mol Microbiol 98: 193-207
5. 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. Photosynth Res 118: 115-124
6. Cai F, Sutter M, Bernstein SL, Kinney JN, Kerfeld CA (2015) Engineering bacterial microcompartment shells: chimeric shell proteins and chimeric carboxysome shells. ACS Synth Biol 4: 444-453
7. Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA (2013) Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155: 1131-1140
8. Chen AH, Robinson-Mosher A, Savage DF, Silver PA, Polka JK (2013) The bacterial carbon-fixing organelle is formed by shell envelopment of preassembled cargo. PLoS One 8: e76127
9. Cohen SE, Erb ML, Selimkhanov J, Dong G, Hasty J, Pogliano J, Golden SS (2014) Dynamic localization of the cyanobacterial circadian clock proteins. Curr Biol 24: 1836-1844
10. Dalla Chiesa M, Friso G, Deák Z, Vass I, Barber J, Nixon PJ (1997) Reduced turnover of the D1 polypeptide and photoactivation of electron transfer in novel herbicide resistant mutants of Synechocystis sp. PCC 6803. Eur J Biochem 248: 731-740
11. Dou Z, Heinhorst S, Williams EB, Murin CD, Shively JM, Cannon GC (2008) CO2 fixation kinetics of Halothiobacillus neapolitanus mutant carboxysomes lacking carbonic anhydrase suggest the shell acts as a diffusional barrier for CO2. J Biol Chem 283: 10377-10384
12. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237-240
13. Fujita Y, Murakami A, Ohki K (1987) Regulation of photosystem composition in the cyanobacterial photosynthetic system: the regulation occurs in response to the redox state of the electron pool located between the two photosystems. Plant Cell Physiol 28: 283-292
14. Gill RT, Katsoulakis E, Schmitt W, Taroncher-Oldenburg G, Misra J, Stephanopoulos G (2002) Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J Bacteriol 184: 3671-3681
15. Golden SS (1988) Mutagenesis of cyanobacteria by classical and genetransfer- based methods. Methods Enzymol 167: 714-727
16. Gonzalez-Esquer CR, Shubitowski TB, Kerfeld CA (2015) Streamlined construction of the cyanobacterial CO2-fixing organelle via protein domain fusions for use in plant synthetic biology. Plant Cell 27: 2637-2644
17. Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ, Chater KF (2004) Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol 54: 107-128
18. Gust B, Kieser T, Chater KF (2002) REDIRECT Technology: PCR-targeting System in Streptomyces coelicolor. John Innes Centre, Norwich, UK
19. Hantke MF, Hasse D, Maia FRNC, Ekeberg T, John K, Svenda M, Loh ND, Martin AV, Timneanu N, Larsson DSD, et al (2014) High-throughput imaging of heterogeneous cell organelles with an X-ray laser. Nat Photonics 8: 943-949
20. Harano K, Ishida H, Kittaka R, Kojima K, Inoue N, Tsukamoto M, Satoh R, Himeno M, Iwaki T, Wadano A (2003) Regulation of the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) in a cyanobacterium, Synechococcus PCC7942. Photosynth Res 78: 59-65
21. Havemann GD, Sampson EM, Bobik TA (2002) PduA is a shell protein of polyhedral organelles involved in coenzyme B(12)-dependent degradation of 1,2-propanediol in Salmonella enterica serovar typhimurium LT2. J Bacteriol 184: 1253-1261
22. Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13: 793-806
23. Howitt CA, Cooley JW, Wiskich JT, Vermaas WF (2001) A strain of Synechocystis sp. PCC 6803 without photosynthetic oxygen evolution and respiratory oxygen consumption: implications for the study of cyclic photosynthetic electron transport. Planta 214: 46-56
24. Huang L, McCluskey MP, Ni H, LaRossa RA (2002) Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol 184: 6845-6858
25. Ito H, Mutsuda M, Murayama Y, Tomita J, Hosokawa N, Terauchi K, Sugita C, Sugita M, Kondo T, Iwasaki H (2009) Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc Natl Acad Sci USA 106: 14168-14173
26. Ivleva NB, Bramlett MR, Lindahl PA, Golden SS (2005) LdpA: a component of the circadian clock senses redox state of the cell. EMBO J 24: 1202-1210
27. Ivleva NB, Gao T, LiWang AC, Golden SS (2006) Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. Proc Natl Acad Sci USA 103: 17468-17473
28. Jain IH, Vijayan V, O’Shea EK (2012) Spatial ordering of chromosomes enhances the fidelity of chromosome partitioning in cyanobacteria. Proc Natl Acad Sci USA 109: 13638-13643
29. Kerfeld CA, Erbilgin O (2015) Bacterial microcompartments and the modular construction of microbial metabolism. Trends Microbiol 23: 22-34
30. Kerfeld CA, Heinhorst S, Cannon GC (2010) Bacterial microcompartments. Annu Rev Microbiol 64: 391-408
31. 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
32. Kinney JN, Axen SD, Kerfeld CA (2011) Comparative analysis of carboxysome shell proteins. Photosynth Res 109: 21-32
33. Lin MT, Occhialini A, Andralojc PJ, Devonshire J, Hines KM, Parry MA, Hanson MR (2014a) β-Carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts. Plant J 79: 1-12
34. Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR (2014b) A faster Rubisco with potential to increase photosynthesis in crops. Nature 513: 547-550
35. Liu H, Landry MR, Vaulot D, Campbell L (1999) Prochlorococcus growth rates in the central equatorial Pacific: An application of the ƒmax approach. J Geophys Res 104: 3391-3399
36. Liu LN (2016) Distribution and dynamics of electron transport complexes in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1857: 256-265
37. Liu LN, Bryan SJ, Huang F, Yu J, Nixon PJ, Rich PR, Mullineaux CW (2012) Control of electron transport routes through redox-regulated redistribution of respiratory complexes. Proc Natl Acad Sci USA 109: 11431-11436
38. Long BM, Tucker L, Badger MR, Price GD (2010) Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153: 285-293
39. Mangan N, Brenner M (2014) Systems analysis of the CO2 concentrating mechanism in cyanobacteria. eLife 3: e02043
40. 2- concentrating mechanism in Synechocystis sp. PCC6803. Plant Cell Environ 27: 615-626
41. McKay RM, Gibbs S, Espie G (1993) Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159: 21-29
42. Menon BB, Heinhorst S, Shively JM, Cannon GC (2010) The carboxysome shell is permeable to protons. J Bacteriol 192: 5881-5886
43. Mullineaux CW (2001) How do cyanobacteria sense and respond to light? Mol Microbiol 41: 965-971
44. Mullineaux CW, Allen JF (1990) State 1-State 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystems I and II. Photosynth Res 23: 297-311
45. Ohbayashi R, Watanabe S, Kanesaki Y, Narikawa R, Chibazakura T, Ikeuchi M, Yoshikawa H (2013) DNA replication depends on photosynthetic electron transport in cyanobacteria. FEMS Microbiol Lett 344: 138-144
46. Omata T, Gohta S, Takahashi Y, Harano Y, Maeda S (2001) Involvement of a CbbR homolog in low CO2-induced activation of the bicarbonate transporter operon in cyanobacteria. J Bacteriol 183: 1891-1898
47. Peña KL, Castel SE, de Araujo C, Espie GS, Kimber MS (2010) Structural basis of the oxidative activation of the carboxysomal gamma-carbonic anhydrase, CcmM. Proc Natl Acad Sci USA 107: 2455-2460
48. 2 within the carboxysome. Plant Physiol 91: 514-525
49. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461
50. Price GD, Coleman JR, Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 784-793
51. Rae BD, Long BM, Badger MR, Price GD (2012) Structural determinants of the outer shell of b-carboxysomes in Synechococcus elongatus PCC 7942: roles for CcmK2, K3-K4, CcmO, and CcmL. PLoS One 7: e43871
52. 2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77: 357-379
53. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1-61
54. Savage DF, Afonso B, Chen AH, Silver PA (2010) Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327: 1258-1261
55. Schwarz R, Reinhold L, Kaplan A (1995) Low activation state of ribulose- 1,5-bisphosphate carboxylase/oxygenase in carboxysome-defective Synechococcus mutants. Plant Physiol 108: 183-190
56. Shively JM, Ball F, Brown DH, Saunders RE (1973) Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182: 584-586
57. Smith RM, Williams SB (2006) Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus. Proc Natl Acad Sci USA 103: 8564-8569
58. Sutter M, Faulkner M, Aussignargues C, Paasch BC, Barrett S, Kerfeld CA, Liu L-N (2016) Visualization of bacterial microcompartment facet assembly using high-speed atomic force microscopy. Nano Lett 16: 1590-1595
59. 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
60. Ting CS, Hsieh C, Sundararaman S, Mannella C, Marko M (2007) Cryoelectron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium. J Bacteriol 189: 4485-4493
61. Trebst A (1980) Inhibitors in electron flow: Tools for the functional and structural localization of carriers and energy conservation sites. Meth Enzymol 69: 675-715
62. Tsai Y, Sawaya MR, Cannon GC, Cai F, Williams EB, Heinhorst S, Kerfeld CA, Yeates TO (2007) Structural analysis of CsoS1A and the protein shell of the Halothiobacillus neapolitanus carboxysome. PLoS Biol 5: e144
63. Watson GM, Tabita FR (1996) Regulation, unique gene organization, and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium. Plant Mol Biol 32: 1103-1115
64. Whitehead L, Long BM, Price GD, Badger MR (2014) Comparing the in vivo function of a-carboxysomes and b-carboxysomes in two model cyanobacteria. Plant Physiol 165: 398-411
65. Wood TL, Bridwell-Rabb J, Kim YI, Gao T, Chang YG, LiWang A, Barondeau DP, Golden SS (2010) The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor. Proc Natl Acad Sci USA 107: 5804-5809
66. Woodger FJ, Badger MR, Price GD (2003) Inorganic carbon limitation induces transcripts encoding components of the CO(2)-concentrating mechanism in Synechococcus sp. PCC7942 through a redox-independent pathway. Plant Physiol 133: 2069-2080
67. Yeates TO, Crowley CS, Tanaka S (2010) Bacterial microcompartment organelles: protein shell structure and evolution. Annu Rev Biophys 39: 185-205
68. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM (2008) Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 6: 681-691
69. Zhang P, Eisenhut M, Brandt AM, Carmel D, Silén HM, Vass I, Allahverdiyeva Y, Salminen TA, Aro EM (2012) Operon flv4-flv2 provides cyanobacterial photosystem II with flexibility of electron transfer. Plant Cell 24: 1952-1971