Heme oxygenase 2 of the cyanobacterium Synechocystis sp. PCC 6803 is induced under a microaerobic atmosphere and is required for microaerobic growth at high light intensity

Photosynthesis Research

Volumn 103, Issue 1, 2010, Pages 47-59

  Yilmaz, Mete ^a,b   Kang, Ilgu ^a   Beale, Samuel I ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Chlorophyll; Cyanobacteria; Heme oxygenase; Microaerobic; Phycobilin; Synechocystis sp. PCC 6803

Indexed keywords

ALGAE; CRYPTOPHYTA; CYANOBACTERIA; RHODOPHYTA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 76149126413     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-009-9506-3     Document Type: Article

References (48)

1. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55: 539-552.
2. Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4: 14.
3. Beale SI (1993) Biosynthesis of phycobilins. Chem Rev 93: 785-802.
4. Beale SI (2008a) Biosynthesis of chlorophylls and hemes. In: Harris L, Stern DB, Witman G (eds) The chlamydomonas sourcebook, vol 2, 2nd edn. Elsevier, Dordrecht, pp 731-798.
5. Beale SI (2008b) Photosynthetic pigments: perplexing persistent prevalence of 'Superfluous' pigment production. Curr Biol 18: R342-R343.
6. Bruggemann H, Bauer R, Raffestin S, Gottschalk G (2004) Characterization of a heme oxygenase of Clostridium tetani and its possible role in oxygen tolerance. Arch Microbiol 182: 259-263.
7. Cornejo J, Beale SI (1997) Phycobilin biosynthetic reactions in extracts of cyanobacteria. Photosynth Res 51: 223-230.
8. 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.
9. Dore S, Takahashi M, Ferris CD, Zakhary R, Hester LD, Guastella D, Snyder SH (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc Natl Acad Sci USA 96: 2445-2450.
10. Glazer AN (1988) Phycobiliproteins. Methods Enzymol 167: 291-303.
11. Gray MW (1989) The evolutionary origins of organelles. Trends Genet 5: 294-299.
12. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
13. Howitt CA, Cooley JW, Wiskich JT, Vermaas WFJ (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.
14. Lascelles J, Hatch TP (1969) Bacteriochlorophyll and heme synthesis in Rhodopseudomonas spheroides-possible role of heme in regulation of branched biosynthetic pathway. J Bacteriol 98: 712-720.
15. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307-1320.
16. MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124: 311-334.
17. Migita CT, Zhang X, Yoshida T (2003) Expression and characterization of cyanobacterium heme oxygenase, a key enzyme in the phycobilin synthesis. Properties of the heme complex of recombinant active enzyme. Eur J Biochem 270: 687-698.
18. Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008) Identification of two homologous genes, chlAI and chlA(II), that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283: 2684-2692.
19. Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7: 357-366.
20. Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A, Partensky F, Burd H, Kaznadzey D, Haselkorn R, Galperin MY (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci USA 103: 13126-13131.
21. Nowack ECM, Melkonian M, Glockner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18: 410-418.
22. Puri S, O'Brian MR (2006) The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J Bacteriol 188: 6476-6482.
23. Ratliff M, Zhu W, Deshmukh R, Wilks A, Stojiljkovic I (2001) Homologues of neisserial heme oxygenase in gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 183: 6394-6403.
24. Rieble S, Beale SI (1988) Transformation of glutamate to delta-aminolevulinic-acid by soluble extracts of Synechocystis sp. PCC 6803 and other oxygenic prokaryotes. J Biol Chem 263: 8864-8871.
25. Rieble S, Beale SI (1991) Purification of glutamyl-tRNA reductase from Synechocystis sp. PCC 6803. J Biol Chem 266: 9740-9745.
26. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, NY.
27. Schmitt MP (1997) Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J Bacteriol 179: 838-845.
28. Schrautemeier B, Neveling U, Schmitz S (1995) Distinct and differently regulated Mo-dependent nitrogen-fixing systems evolved for heterocysts and vegetative cells of Anabaena variabilis ATCC 29413-characterization of the fdxh1/2 gene regions as part of the nif1/2 gene clusters. Mol Microbiol 18: 357-369.
29. 2-dependent anoxygenic photosynthesis in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743. Int J Photoenergy 4: 169-173.
30. Sicora CI, Ho FM, Salminen T, Styring S, Aro EM (2009) Transcription of a "silent" cyanobacterial psbA gene is induced by microaerobic conditions. Biochim Biophys Acta Bioenerg 1787: 105-112.
31. Skaar EP, Gaspar AH, Schneewind O (2004) IsdG and IsdI, heme-degrading enzymes in the cytoplasm of Staphylococcus aureus. J Biol Chem 279: 436-443.
32. Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21: 179-211.
33. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order chroococcales). Bacteriol Rev 35: 171-205.
34. 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. Eur J Biochem 271: 4517-4525.
35. Sugishima M, Hagiwara Y, Zhang X, Yoshida T, Migita CT, Fukuyama K (2005) Crystal structure of dimeric heme oxygenase-2 from Synechocystis sp. PCC 6803 in complex with heme. Biochemistry 44: 4257-4266.
36. Summerfield TC, Toepel J Jr, Sherman LA (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47: 12939-12941.
37. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
38. Terry MJ, Linley PJ, Kohchi T (2002) Making light of it: the role of plant haem oxygenases in phytochrome chromophore synthesis. Biochem Soc Trans 30: 604-609.
39. Thiel T, Lyons EM, Erker JC, Ernst A (1995) A 2nd nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci USA 92: 9358-9362.
40. Thiel T, Lyons EM, Erker JC (1997) Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 179: 5222-5225.
41. Unno M, Matsui T, Ikeda-Saito M (2007) Structure and catalytic mechanism of heme oxygenase. Nat Prod Rep 24: 553-570.
42. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH (1993) Carbon monoxide: a putative neural messenger. Science 259: 381-384.
43. Wegele R, Tasler R, Zeng Y, Rivera M, Frankenberg-Dinkel N (2004) The heme oxygenase(s)-phytochrome system of Pseudomonas aeruginosa. J Biol Chem 279: 45791-45802.
44. Wilks A, Schmitt MP (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J Biol Chem 273: 837-841.
45. Williams JGK (1988) Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol 167: 766-778.
46. Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K, Takenaka D, Yamashita A, Nijo N, Inagawa K, Morita N, Sasaki T, Yamamoto Y (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth Res 98: 589-608.
47. Zhang X, Migita CT, Sato M, Sasahara M, Yoshida T (2005) Protein expressed by the ho2 gene of the cyanobacterium Synechocystis sp. PCC 6803 is a true heme oxygenase. Properties of the heme and enzyme complex. FEBS J 272: 1012-1022.
48. Zhu W, Wilks A, Stojiljkovic I (2000) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase. J Bacteriol 182: 6783-6790.