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A novel type of lycopene ε-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4

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Abstract

Chlorophyll-b-possessing cyanobacteria of the genus Prochlorococcus share the presence of high amounts of α- and β-carotenoids with green algae and higher plants. The branch point in carotenoid biosynthesis is the cyclization of lycopene, for which in higher plants two distinct enzymes are required, ε- and β-lycopene cyclase. All cyanobacteria studied so far possess a single β-cyclase. Here, two different Prochlorococcus sp. MED4 genes were functionally identified by heterologous gene complementation in Escherichia coli to encode lycopene cyclases. Whereas one is both functionally and in sequence highly similar to the β-cyclase of Synechococcus sp. strain PCC 7942 and other cyanobacteria, the other showed several intriguing features. It acts as a bifunctional enzyme catalyzing the formation of ε- as well as of β-ionone end groups. Expression of this cyclase in E. coli resulted in the simultaneous accumulation of α- β-, δ-, and ε-carotene. Such an activity is in contrast to all lycopene ε-cyclases known so far, including those of the higher plants. Thus, for the first time among prokaryotes, two individual enzymes were identified in one organism that are responsible for the formation of cyclic carotenoids with either β- or ε-end groups. These two genes are suggested to be designated as crtL-b and crtL-e. The results indicate that both enzymes might have originated from duplication of a single gene. Consequently, we suggest that multiple gene duplications followed by functional diversification resulted several times, and in independent lineages, in the appearance of enzymes for the biosynthesis of cyclic carotenoids.

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Abbreviations

Chl :

Chlorophyll

CPDMA :

2-(4-Chlorophenylthio)-dimethylethylamine

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Acknowledgements

We thank F. Larimer, S. Stilwagon and S. W. Chisholm for access to the preliminary sequence data for Prochlorococcus strains MED4 and MIT 9313, obtained from the DOE Joint Genome Institute (JGI) at http://www.jgi.doe.gov/JGI_microbial/html/prochlorococcus/prochlo_pickastrain.html. Supported by the EU program MARGENES (QLRT-2001-01226) and grant SFB 429-TP A4 from the Deutsche Forschungsgemeinschaft, Bonn, to WRH.

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Correspondence to Wolfgang R. Hess.

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Stickforth, P., Steiger, S., Hess, W.R. et al. A novel type of lycopene ε-cyclase in the marine cyanobacterium Prochlorococcus marinus MED4. Arch Microbiol 179, 409–415 (2003). https://doi.org/10.1007/s00203-003-0545-4

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