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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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Abstract

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.

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Acknowledgments

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.

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  1. Mete Yilmaz

    Present address: School of Forest Resources and Conservation, Program in Fisheries and Aquatic Sciences, University of Florida, 7922 N.W. 71st Street, Gainesville, FL, 32653, USA

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  1. Division of Biology and Medicine, Brown University, Providence, RI, 02912, USA

    Mete Yilmaz, Ilgu Kang & Samuel I. Beale

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  1. Mete Yilmaz
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Correspondence to Samuel I. Beale.

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Yilmaz, M., Kang, I. & Beale, S.I. 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. Photosynth Res 103, 47–59 (2010). https://doi.org/10.1007/s11120-009-9506-3

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