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
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Cyanobacteria, red algae, and cryptomonad algae utilize phycobilin chromophores that are attached to phycobiliproteins to harvest solar energy. Heme oxygenase (HO) in these organisms catalyzes the first step in phycobilin formation through the conversion of heme to biliverdin IXα, CO, and iron. The Synechocystis sp. PCC 6803 genome contains two open reading frames, ho1 (sll1184) and ho2 (sll1875), whose products have in vitro HO activity. We report that HO2, the protein encoded by ho2, was induced in the cells growing under a microaerobic atmosphere [0.2% (v/v) O2], whereas HO1 was constitutively expressed under both aerobic and microaerobic atmospheres. Light intensity did not have an effect on the expression of both the HOs. Cells, in which ho2 was disrupted, were unable to grow microaerobically at a light intensity of 40 μmol m−2 s−1, but did grow microaerobically at 10 μmol m−2 s−1 light intensity. These cells grew normally aerobically at both light intensities. Comparative analysis of complete cyanobacterial genomes revealed that possession of two HOs is common in cyanobacteria. In phylogenetic analysis of their amino acid sequences, cyanobacterial HO1 and HO2 homologs formed distinct clades. HO sequences of cyanobacteria that have only one isoform were most similar to HO1 sequences. We propose that HO2 might be the more ancient HO homolog that functioned under low O2 tension, whereas the derived HO1 can better accommodate increased O2 tension in the environment.
KeywordsHeme oxygenase Cyanobacteria Synechocystis sp. PCC 6803 Microaerobic Phycobilin Chlorophyll
We thank G. Burleigh for suggestions on phylogenetic analysis and comments on the manuscript, and W. Vermaas for the ΔPSII strain of Synechocystis sp. PCC 6803. M. Yilmaz was supported by a fellowship from the Turkish Council of Higher Education.
- 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 731–798Google Scholar
- Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008) Identification of two homologous genes, chlA I and chlA (II), that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283:2684–2692CrossRefPubMedGoogle Scholar
- Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, NYGoogle Scholar
- 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 18:357–369CrossRefPubMedGoogle Scholar
- Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21:179–211Google Scholar