Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles.
The seawater microalga Nannochloropsis gaditana is capable of accumulating a large fraction of reduced carbon as lipids. To clarify the molecular bases of this metabolic feature, we investigated light-driven lipid biosynthesis in Nannochloropsis gaditana cultures combining the analysis of photosynthetic functionality with transcriptomic, lipidomic and metabolomic approaches. Light-dependent alterations are observed in amino acid, isoprenoid, nucleic acid, and vitamin biosynthesis, suggesting a deep remodeling in the microalgal metabolism triggered by photoadaptation. In particular, high light intensity is shown to affect lipid biosynthesis, inducing the accumulation of diacylglyceryl-N,N,N-trimethylhomo-Ser and triacylglycerols, together with the up-regulation of genes involved in their biosynthesis. Chloroplast polar lipids are instead decreased. This situation correlates with the induction of genes coding for a putative cytosolic fatty acid synthase of type 1 (FAS1) and polyketide synthase (PKS) and the down-regulation of the chloroplast fatty acid synthase of type 2 (FAS2). Lipid accumulation is accompanied by the regulation of triose phosphate/inorganic phosphate transport across the chloroplast membranes, tuning the carbon metabolic allocation between cell compartments, favoring the cytoplasm, mitochondrion, and endoplasmic reticulum at the expense of the chloroplast. These results highlight the high flexibility of lipid biosynthesis in N. gaditana and lay the foundations for a hypothetical mechanism of regulation of primary carbon partitioning by controlling metabolite allocation at the subcellular level.
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Alessandro
0000-0003-4818-7778
A
Alboresi
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Giorgio
0000-0002-9204-4080
G
Perin
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Nicola
N
Vitulo
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Gianfranco
G
Diretto
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Maryse
M
Block
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Juliette
J
Jouhet
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Andrea
A
Meneghesso
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Giorgio
G
Valle
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Giovanni
G
Giuliano
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.).
Eric
E
Maréchal
PAR-Lab_Padua Algae Research Laboratory, Department of Biology (A.A., G.P., A.M., T.M.), and Innovative Biotechnologies Interdepartmental Research Center (CRIBI; N.V., G.V.), University of Padova, 35121 Padova, Italy;Laboratoire de Biologie Cellulaire et Végétale, UMR 5168 CNRS, CEA, INRA, Université Grenoble Alpes, BIG, CEA-Grenoble, 38054 Grenoble, Cedex 9, France (M.B., J.J., E.M.);Department of Biotechnology, University of Verona, 37134 Verona, Italy (N.V.); andItalian National Agency for New Technologies, Energy, and Sustainable Economic Development (ENEA), Casaccia Research Centre, 00123 Roma, Italy (G.D., G.G.) tomas.morosinotto@unipd.it.
Tomas
0000-0002-0803-7591
T
Morosinotto
D002244:Carbon / Q000378:metabolism*; D002736:Chloroplasts / Q000378:metabolism / Q000528:radiation effects; D015536:Down-Regulation / Q000528:radiation effects; D005786:Gene Expression Regulation / Q000528:radiation effects*; D008027:Light; D050356:Lipid Metabolism / Q000528:radiation effects*; D058086:Microalgae; D010788:Photosynthesis / Q000528:radiation effects*; D058009:Stramenopiles / Q000378:metabolism* / Q000528:radiation effects; D014280:Triglycerides / Q000378:metabolism; D015854:Up-Regulation / Q000528:radiation effects
D014280:Triglycerides; D002244:Carbon