PfsR is a key regulator of iron homeostasis in Synechocystis PCC 6803

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Cheng, Dan ^a   He, Qingfang ^a  

^a Department of Applied Science University of Arkansas at Little Rock ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOFERRITIN; CAROTENOID; CHLOROPHYLL A; CHLOROPHYLL BINDING PROTEIN; FERRIC UPTAKE REGULATOR; HEME OXYGENASE; IRON; PHYCOCYANIN; PROTEIN PFSR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HEME;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL VIABILITY; BACTERIUM MUTANT; BFR GENE; BIOACCUMULATION; CONTROLLED STUDY; DELETION MUTANT; FEOB GENE; FURA GENE; FUT GENE; GENE; GENE EXPRESSION; GENE INACTIVATION; GENETIC TRANSCRIPTION; HO GENE; IRON METABOLISM; ISIA GENE; NONHUMAN; NUTRIENT LIMITATION; PFSR GENE; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PROTEIN FUNCTION; SYNECHOCYSTIS; WILD TYPE; CYTOLOGY; GENE DELETION; GENETICS; HOMEOSTASIS; INTRACELLULAR SPACE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PIGMENTATION;

BACTERIAL PROTEINS; HEME; HOMEOSTASIS; INTRACELLULAR SPACE; IRON; PHOTOSYNTHESIS; PIGMENTATION; SEQUENCE DELETION; STRESS, PHYSIOLOGICAL; SYNECHOCYSTIS;

EID: 84904256996     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101743     Document Type: Article

References (78)

1. Entsch B, Sim RG, Hatcher BG (1983) Indications from photosynthetic components that iron is a limiting nutrient in primary producers on coral reefs. Mar Biol 73: 17-30.
2. Behrenfeld MJ, Milligan AJ (2013) Photophysiological expressions of iron stress in phytoplankton. Ann Rev Mar Sci 5: 217-246.
3. Shcolnick S, Summerfield TC, Reytman L, Sherman LA, Keren K (2009) The mechanism of iron homeostasis in the unicellular cyanobacterium Synechocystis sp. PCC 6803 and its relationship to oxidative stress. Plant Physiol 150: 2045-2056.
4. Ferreira F, Straus NA (1994) Iron deprivation in cyanobacteria. J Appl Phycol 6: 199-210.
5. Straus NA (1994) Iron deprivation: physiology and gene regulation. In: Bryant DA, editors, The Molecular Biology of Cyanobacteria. Dordrecht: Kluwer Academic Publishers. pp. 731-750.
6. Sandmann G (1985) Consequences of iron deficiency on photosynthetic and respiratory electron transport in blue-green algae. Photosynth Res 6: 261-271.
7. Ivanov AG, Park YI, Miskiewicz E, Raven JA, Huner NPA, et al. (2000) Iron stress restricts photosynthetic inersysterm electron transport in Synechococcus sp. PCC 7942. FEBS Lett 485: 173-177.
8. Sandström S, Ivanov AG, Park YI, Oquist G, Gustafsson P (2002) Iron stress responses in the cyanobacterium Synechococcus sp. PCC7942. Physiol Plant 116: 255-263.
9. Ryan-Keogh TJ, Macey AI, Cockshutt AM, Moore CM, Bibby TS (2012) The cyanobacterial chlorophyll-binding-protein IsiA acts to increase the in vivo effective absorption cross-section of PSI under iron limitation. J phycol 48: 145-154.
10. Fraser JM, Tulk SE, Jeans JA, Campbell DA, Bibby TS, et al. (2013) Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongates PCC 7942. PLoS ONE 8: e59861.
11. Öquist G (1974) Iron deficiency in the blue green alga Anacystis nidulans: Fluorescence and absorption spectra recorded at 77 K. Physiol Plant 31: 55-58.
12. Katoh H, Hagino N, Grossman AR, Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechodystis sp. strain PCC 6803. J Bacteriol 183: 2779-2784. (Pubitemid 32319280)
13. Sandmann G, Peleato ML, Fillat MF, Lazaro MC, Gomez-Moreno C (1990) Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosynth Res 26: 119-125.
14. Laudenbach D, Straus N (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170: 5018-5026.
15. Burnap RL, Troyan T, Sherman LA (1993) The highly abundant chorophyll-protein of iron-deficient Synehococcus sp. PCC 7942 (CP439) is encoded by the isiA gene. Plant Physiol 103: 893-902. (Pubitemid 2023342)
16. Falk S, Samson G, Bruce D, Huner NPA, Laudenbach DE (1995) Functional analysis of the iron-stress induced CP439 polypeptide of PSII in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 45: 51-60.
17. Bibby TS, Nield J, Barber J (2001) Iron deficiency induced the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412: 743-745. (Pubitemid 32771998)
18. Bibby TS, Nield J, Barber J (2001) Three-dimensional model and characterization of the iron stress-induced CP439-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803. J Biol Chem 276: 43246-43252.
19. Boekema EJ, Hifney A, Yakkushevska AE, Piotrowski M, Keegstra W, et al. (2001) A giant chlorophyll-protein complex induced by iron-defeiciency in cyanobacteria. Nature 412: 745-748. (Pubitemid 32771999)
20. Aspinwall CL, Duncan J, Bibby T, Mullineaux CW, Barber J (2004) The trimeric organisation of photosystem I is not necessary for the iron-stress induced CP439 protein to functionally associate with this reaction centre. FEBS Lett 574: 126-130. (Pubitemid 39200907)
21. Yeremenko N, Kouril R, Ihalainem J, D'Haene S, van Oosterwijk N, et al. (2004) Supramolecular organization and dual function of the IsiA chlorophyllbinding protein in cyanobacteria. Biochemistry 43: 10308-10313. (Pubitemid 39079304)
22. Wang Q, Hall CL, AI-Adami MZ, He Q (2010) IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in Synechocystis PCC 6803. PLoS ONE 5: e10432.
23. Chauhan D, Folea IM, Jolley CC, Kouril R, Lubner CE, et al. (2011) A novel photosynthetic strategy for adaptation to low-iron aquatic environments. Biochemistry 50: 686-692.
24. Park Y, Sandström P, Gustafsson P, Öquist G (1999) Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation. Mol Microbiol 32: 123-129. (Pubitemid 29164139)
25. Sandström S, Park YI, Öquist G, Gustafsson P (2001) CP43', the isiA gene product, functions as an excitation energy dissipation in the cyanobacterium Synechococcus sp. PCC 7942. Photochem Photobiol 74: 431-437.
26. Andrizhiyevskaya EG, Schwabe TM, Germano M, D'Haene S, Kruip J, et al. (2002) Spectroscopic properties of PSI-IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1556: 265-272. (Pubitemid 35379686)
27. Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE (2003) Time-resolved absorption and emission show that the CP43' antenna ring of ironstressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42: 3893-3903. (Pubitemid 36402682)
28. Ihalainen JA, D'Haene S, Yeremenko N, van Roon H, Arteni AA, et al. (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43') dissipate energy in cyanobacteria. Biochemistry 44: 10846-10853. (Pubitemid 41153645)
29. Karapetyan NV (2008) Protective dissipation of excess absorbed energy by photosynthetic apparatus of cyanobacteria: role of antenna terminal emitters. Photosynth Res 97: 195-204.
30. Jantaro S, Ali Q, Lone S, He Q (2006) Suppression of the lethality of high light to a quadruple HLI mutant by the inactivation of the regulatory protein PfsR in Synechocystis PCC 6803. J Biol Chem 281: 30865-30874. (Pubitemid 44582141)
31. Ramos JL, Martínez-Bueno M, Molina-Henares AJ, Terán W, Watanabe K, et al. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356. (Pubitemid 40847943)
32. Pareja E, Pareja-Tobes P, Manrique M, Pareja-Toves E, Bonal J, et al. (2006) ExtraTrain: a database of extragenic regions and transcriptional information in prokaryotic organisms. BMC Microbiol 6: 29.
33. Moran R (1982) Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. Plant Physiol 69: 1376-1381.
34. Collier JL, Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174: 4718-4726.
35. He Q, Vermaas W (1998) Chlorophyll a availability affects psbA translation and D1 precursor processing in vivo in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 95: 5830-5835. (Pubitemid 28224182)
36. Peter GF, Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Bio Chem 266: 16745-16754. (Pubitemid 21907862)
37. Thomas PE, Ryan D, Levin W (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75: 168-176.
38. Cheng Y, Li JH, Shi L, Wang L, Latifi A, et al. (2006) A pair of iron-responsive genes encoding protein kinases with a Ser/Thr kinase domain and a His kinase domain are regulated by NtcA in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 188: 4822-4829. (Pubitemid 43956080)
39. Michel KP, Berry S, Hifney A, Kruip J, Pistorius EK (2003) Adaptation to iron deficiency: a comparison between the cyanobacterium Synechococcus elongates PCC 7942 wild-type and a DpsA-free mutan. Photosynth Res 75: 71-84. (Pubitemid 36333178)
40. Latifi A, Jeanjean R, Lemeille S, Havaux M, Zhang CC (2005) Iron starvation leads to oxidative stress in Anabaena sp. strain PCC 7120. J Bacteriol 187: 6596-6598. (Pubitemid 41318423)
41. Singh AK, Mclntyre LM, Serman LA (2003) Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 132: 1825-1839. (Pubitemid 37024145)
42. Houot L, Floutier M, Marteyn B, Michaut M, Picciocchi A, et al. (2007) Cadmium triggers an integrated reprogramming of the metabolism of Synechocystis PCC 6803, under the control of the Slr1738 regulator. BMC Genomics 8: 350.
43. Hernández-Prieto MA, Schön V, Georg J, Barreira L, Varela J (2012) Iron deprivation in Synechocystis: inference of pathways, non-coding RNAs, and regulatory elements from comprehensive expression profiling. G3 (Bethesda) 2: 1475-1495.
44. Katoh H, Grossman AR, Hagino N, Ogawa T (2000) A gene of Synechocystis sp. strain PCC 6803 encoding a novel iron transporter. J Bacteriol 182: 6523-6524.
45. Keren N, Aurora R, Pakrasi HB (2004) Critical roles of bacterioferritins in iron storage and proliferation of cyanobacteria. Plant Physiol 135: 1666-1673. (Pubitemid 39009410)
46. Lewin A, Moore GR, Le Brun NE (2005) Formation of protein-coated iron minerals. Dalton Trans 3597-3610. (Pubitemid 41677554)
47. Cornejo J, Willows RD, Beale SI (1998) Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J 15: 99-107.
48. Sugishima M, Migita CT, Zhang X, Yoshida T, Fukuyama K (2004) Crystal structure of heme oxygenase-1 from cyanobacterium Synechocystis sp. PCC 6803 in complex with heme. FEBS J 271: 4517-4525. (Pubitemid 39576567)
49. Zhang X, Migita CT, Sato M, Sasahara M, Yoshida T (2005) Protein expressed by the ho2 gene of the cyanobacterium Synechocystissp. PCC 6803 is a true heme oxygenase. FEBS J 272: 1012-1022. (Pubitemid 40278837)
50. Yilmaz M, Kang I, Beale SI (2010) Heme oxygenase 2 of the cyanobacterium Synechocystis sp. PCC6803 is induced under a microaerobic atmosphere and is requiredfor microaerobic growth at high light intensity. Photosynth Res 103: 47-59.
51. Fenton HJH (1894) Oxidation of tartaric acid in presence of iron. J Chem Soc Trans 65: 899-910.
52. Choudhary M, Jetley UK, Khan MA, Zutshi S, Fatma T (2007) Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotox Environ Safe 66: 204-209. (Pubitemid 44821410)
53. Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33: 737-742. (Pubitemid 41160854)
54. Kashiyama Y, Yokoyama A, Kinoshita Y, Shoji S, Miyashiya H, et al. (2012) Ubiquity and quantitative significance of detoxification catabolism of chlorophyll associated with protistan herbivory. Proc Natl Acad Sci USA 109: 17328-17335.
55. Kunert A, Vinnemeier J, Erdmann N, Hagemann M (2003) Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 227: 255-262. (Pubitemid 37329885)
56. Dühring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103: 7054-7058.
57. Ghassemian M, Straus NA (1996) Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942. Microbiology 142: 1469-1476. (Pubitemid 26193855)
58. González A, Bes MT, Valladares A, Peleato ML, Fillat MF (2012) FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environ Micobiol 14: 3175-3187.
59. Hantke K (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172-177.
60. McHugh JP, Rodríqez-Quiñones F, Abdul-Tehrani H, Svistunenko DA, Poole RK, et al. (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 8: 29478-29486. (Pubitemid 36962327)
61. Fuangthong M, Herbig AF, Bsat N, Helmann JD (2002) Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J Bacteriol 184: 3276-3286. (Pubitemid 34568937)
62. Hernández JA, Lápez-Gomollón S, Bes MT, Fillat MF, Peleato ML (2004) Three fur homologues from Anabaena sp. PCC 7120: exploring reciprocal protein-promoter recognition. FEMS Microbiol Lett 236: 275-282. (Pubitemid 38906661)
63. Zheng M, Doan B, Schneider TD, Storz G (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181: 4639-4643. (Pubitemid 29357947)
64. Hernández JA, Muro-Pastor AM, Flores E, Bes MT, Peleato ML, et al. (2006) Identification of a furA cis antisense RNA in the cyanobacterium Anabaena sp. PCC 7120. J Mol Biol 355: 325-334. (Pubitemid 41785741)
65. Martin-Luna B, Sevilla E, Gonzalez A, Bes MT, Fillat MF, et al. (2011) Expression of fur and its antisense a-fur from Microcystis aeruginosa PCC7806 as response to light and oxidative stress. J Plant Physiol 168: 2244-2250.
66. Sevilla E, Msrtín-Luna B, González A, Gonzalo-Asensio JA, Peleato ML, et al. (2011) Identification of three novel antisense RNAs in the fur locus from unicellular cyanobacteria. Microbiology 157: 3398-3404.
67. Kammler M, Schon C, Hantke K (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175: 6212-6219. (Pubitemid 23292435)
68. Chen CY, Morse SA (1999) Neisseria gonorrhoeae bacterioferritin: structural heterogeneity, involvement in iron storage and protection against oxidative stress. Microbiology 145: 2967-2975.
69. Babykin MM, Sidoruk KV, Zinchenko VV, Nefedova LN, Cerff R, et al. (2003) On the involvement of the regulatory gene prqR in the development of resistance to methyl viologen in cyanobacterium Synechocystis sp. PCC 6803. Genetika 39: 25-32. (Pubitemid 44273244)
70. Kirik IA, Zinchenko VV, Shestakov SV, Babykin MM (2003) Trans- and cis-acting autorepressors of the prqR gene in Synechocystis cyanobacteria sp. PCC 6803. Mol Biol (Mosk) 37: 1035-1044.
71. Nefedova LN, Fantin IUS, Zinchenko VV, Babykin MM (2003) The prqA and mvrA genes encoding carrier proteins control resistance to methyl viologen in the cyanobacterium Synechocystis sp. PCC 6803. Genetika 39: 336-340. (Pubitemid 44273227)
72. Becskei A, Serrano L (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
73. Wall M, Hlavacek W, Savageau M (2003) Design principles for regulator gene expression in a repressible gene circuit. J Mol Biol 332: 861-876. (Pubitemid 37101373)
74. Shinar G, Dekel E, Tlusty T, Alon U (2006) Rules for biological regulation based on error minimization. Proc Natl Acad Sci USA 103: 3999-4004.
75. Stekel DJ, Jenkins DJ (2008) Strong negative self regulation of prokaryotic transcription factors increases the intrinsic noise of protein expression. BMC Syst Biol 2: 6.
76. Rosenfeld N, Elowitz M, Alon U (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323: 785-793. (Pubitemid 35341055)
77. Sukrong S, Yun K, Stadler P, Kumar C, Facciuolo T, et al. (2012) Improved growth and stress tolerance in the Arabidopsis oxt1 mutant triggered by altered adenine metabolism. Mol Plant 5: 1310-1332.
78. Novillo F, Alonso JM, Ecker JR, Salinas J (2003) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101: 3985-3990. (Pubitemid 38381089)