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Published on October 6, 2006; 10.1104/pp.106.086090


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Received June 30, 2006
Accepted September 14, 2006

Differential Operation of Dual Protochlorophyllide Reductases for Chlorophyll Biosynthesis in Response to Environmental Oxygen Levels in the Cyanobacterium Leptolyngbya boryana

Shoji Yamazaki , Jiro Nomata , and Yuichi Fujita *

Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan

* Corresponding author; email: fujita{at}agr.nagoya-u.ac.jp.

Most oxygenic phototrophs, including cyanobacteria, have two structurally unrelated protochlorophyllide (Pchlide) reductases in the penultimate step of chlorophyll biosynthesis. One is light-dependent Pchlide reductase (LPOR), and the other is dark-operative Pchlide reductase (DPOR), a nitrogenase-like enzyme assumed to be sensitive to oxygen. Very few studies have been conducted on how oxygen-sensitive DPOR operates in oxygenic phototrophic cells. Here we report that anaerobic conditions are required for DPOR to compensate for the loss of LPOR in cyanobacterial cells. An LPOR-lacking mutant of the cyanobacterium Leptolyngbya boryana (formerly Plectonema boryanum) failed to grow in high light conditions, and this phenotype was overcome by cultivating it under anaerobic conditions (2% CO2/N2). The critical oxygen level enabling the mutant to grow in high light was determined to be 3% (v/v). Oxygen-sensitive Pchlide reduction activity was successfully detected as DPOR activity in cell-free extracts of anaerobically grown mutant cells for the first time, whereas activity was undetectable in the wild type. The contents of two DPOR subunits, ChlL and ChlN, were significantly increased in the mutant cells compared with the wild type. This suggests that the increase in subunits stimulates the DPOR activity that is protected efficiently from oxygen by anaerobic environments, resulting in complementation of the loss of LPOR. These results provide important concepts for understanding how dual Pchlide reductases operate differentially in oxygenic photosynthetic cells grown under natural environments where oxygen levels undergo dynamic changes. The evolutionary implications of the coexistence of two Pchlide reductases are discussed.




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K. Minamizaki, T. Mizoguchi, T. Goto, H. Tamiaki, and Y. Fujita
Identification of Two Homologous Genes, chlAI and chlAII, That Are Differentially Involved in Isocyclic Ring Formation of Chlorophyll a in the Cyanobacterium Synechocystis sp. PCC 6803
J. Biol. Chem., February 1, 2008; 283(5): 2684 - 2692.
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