Chlamydomonas carries out fatty acid beta-oxidation in ancestral peroxisomes using a bona fide acyl-CoA oxidase

A - Papers appearing in refereed journals

Kong, F. T., Liang, Y. X., Legeret, B., Beyly-Adriano, A., Blangy, S., Haslam, R. P., Napier, J. A., Beisson, F., Peltier, G. and Li-Beisson, Y. 2017. Chlamydomonas carries out fatty acid beta-oxidation in ancestral peroxisomes using a bona fide acyl-CoA oxidase. The Plant Journal. 90 (2), pp. 358-371.

AuthorsKong, F. T., Liang, Y. X., Legeret, B., Beyly-Adriano, A., Blangy, S., Haslam, R. P., Napier, J. A., Beisson, F., Peltier, G. and Li-Beisson, Y.
Abstract

Peroxisomes are thought to have played a key role in the evolution of metabolic networks of photosynthetic organisms by connecting oxidative and biosynthetic routes operating in different compartments. While the various oxidative pathways operating in the peroxisomes of higher plants are fairly well characterized, the reactions present in the primitive peroxisomes (microbodies) of algae are poorly understood. Screening of a Chlamydomonas insertional mutant library identified a strain strongly impaired in oil remobilization and defective in Cre05.g232002 (CrACX2), a gene encoding a member of the acyl‐CoA oxidase/dehydrogenase superfamily. The purified recombinant CrACX2 expressed in Escherichia coli catalyzed the oxidation of fatty acyl‐CoAs into trans‐2‐enoyl‐CoA and produced H2O2. This result demonstrated that CrACX2 is a genuine acyl‐CoA oxidase, which is responsible for the first step of the peroxisomal fatty acid (FA) β‐oxidation spiral. A fluorescent protein‐tagging study pointed to a peroxisomal location of CrACX2. The importance of peroxisomal FA β‐oxidation in algal physiology was shown by the impact of the mutation on FA turnover during day/night cycles. Moreover, under nitrogen depletion the mutant accumulated 20% more oil than the wild type, illustrating the potential of β‐oxidation mutants for algal biotechnology. This study provides experimental evidence that a plant‐type FA β‐oxidation involving H2O2‐producing acyl‐CoA oxidation activity has already evolved in the microbodies of the unicellular green alga Chlamydomonas reinhardtii.

Keywordsacyl-CoA oxidase; microbodies; lipid catabolism; oil content; hydrogen peroxide; lipid homeostasis; nitrogen starvation; catalase; lipid droplet; Chlamydomonas reinhardtii
Year of Publication2017
JournalThe Plant Journal
Journal citation90 (2), pp. 358-371
Digital Object Identifier (DOI)doi:10.1111/tpj.13498
Open accessPublished as bronze (free) open access
FunderBiotechnology and Biological Sciences Research Council
Funder project or codeDesigning Seeds for Nutrition and Health (DS)
*Design Oilseeds (Olga Sayanova)
WP1 - Richard Haslam [Tailoring Plant Metabolism]
Publisher's version
Output statusPublished
Publication dates
Online31 Jan 2017
Publication process dates
Accepted27 Jan 2017
Copyright licensePublisher copyright
ISSN0960-7412
PublisherWiley-Blackwell

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