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

Fantao Kong (1, 2) , Yuanxue Liang (1, 2) , Bertrand Légeret (1, 2) , Audrey Beyly-Adriano (1, 2) , Stéphanie Blangy (1, 2) , Richard Haslam (3) , Johnathan Napier (3) , Fred Beisson (1, 2) , G. Peltier (1, 2) , Yonghua Li-Beisson (1, 2)

1 EBMP - Environnement, Bioénergie, Microalgues et Plantes
2 BIAM - Institut de Biosciences et Biotechnologies d'Aix-Marseille (ex-IBEB)
3 Biological Chemistry and Crop Protection

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 H 2 O 2. 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 H 2 O 2-producing acyl-CoA oxidation activity has already evolved in the microbodies of the unicellular green alga Chlamydomonas reinhardtii.

Domains: Life Sciences [q-bio]; Biochemistry, Molecular Biology; Biochemistry [q-bio.BM]

Fantao Kong, Yuanxue Liang, Bertrand Légeret, Audrey Beyly-Adriano, Stéphanie Blangy, et al.. Chlamydomonas carries out fatty acid β-oxidation in ancestral peroxisomes using a bona fide acyl-CoA oxidase. Plant Journal, 2017, 90 (2), pp.358-371. ⟨10.1111/tpj.13498⟩. ⟨hal-01692495⟩