title: Different Functions of the Paralogs to the N-Terminal Domain of the Orange Carotenoid Protein in the Cyanobacterium Anabaena sp. PCC 7120.
abstract: The photoactive Orange Carotenoid Protein (OCP) is involved in cyanobacterial photoprotection. Its N-terminal domain (NTD) is responsible for interaction with the antenna and induction of excitation energy quenching, while the C-terminal domain is the regulatory domain that senses light and induces photoactivation. In most nitrogen-fixing cyanobacterial strains, there are one to four paralogous genes coding for homologs to the NTD of the OCP. The functions of these proteins are unknown. Here, we study the expression, localization, and function of these genes in Anabaena sp. PCC 7120. We show that the four genes present in the genome are expressed in both vegetative cells and heterocysts but do not seem to have an essential role in heterocyst formation. This study establishes that all four Anabaena NTD-like proteins can bind a carotenoid and the different paralogs have distinct functions. Surprisingly, only one paralog (All4941) was able to interact with the antenna and to induce permanent thermal energy dissipation. Two of the other Anabaena paralogs (All3221 and Alr4783) were shown to be very good singlet oxygen quenchers. The fourth paralog (All1123) does not seem to be involved in photoprotection. Structural homology modeling allowed us to propose specific features responsible for the different functions of these soluble carotenoid-binding proteins.
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Rocío
authors.initials: R
authors.lastname: López-Igual
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Adjélé
authors.initials: A
authors.lastname: Wilson
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Ryan L
authors.identifier: 0000-0002-0349-1779
authors.initials: RL
authors.lastname: Leverenz
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Matthew R
authors.identifier: 0000-0001-5952-0674
authors.initials: MR
authors.lastname: Melnicki
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Céline
authors.initials: C
authors.lastname: Bourcier de Carbon
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Markus
authors.initials: M
authors.lastname: Sutter
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Aiko
authors.initials: A
authors.lastname: Turmo
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: François
authors.identifier: 0000-0001-7873-9866
authors.initials: F
authors.lastname: Perreau
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.).
authors.forename: Cheryl A
authors.identifier: 0000-0002-9977-8482
authors.initials: CA
authors.lastname: Kerfeld
authors.affiliation: Institute for Integrative Biology of the Cell (I2BC), Commissariat à l'Energie Atomique, CNRS, Université Paris-Sud, Université Paris-Saclay, 91198 Gif sur Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);Institut de Biologie et Technologies de Saclay (iBiTec-S), Commissariat à l'Energie Atomique, 91191 Gif-sur-Yvette, France (R.L.-I., A.W., C.B.d.C., D.K.);MSU-DOE Plant Research Laboratory and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824 (R.L.L., M.S., A.T., C.A.K.);Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (M.R.M., C.A.K.);Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (M.R.M., M.S., C.A.K.); andINRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, F-78026 Versailles, France (F.P.) diana.kirilovsky@cea.fr.
authors.forename: Diana
authors.identifier: 0000-0003-2146-3103
authors.initials: D
authors.lastname: Kirilovsky
mesh_terms: D017033:Anabaena / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism*; D002338:Carotenoids / Q000378:metabolism; D004578:Electron Spin Resonance Spectroscopy; D004926:Escherichia coli / Q000235:genetics; D005453:Fluorescence; D015964:Gene Expression Regulation, Bacterial; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D045524:Phycobilisomes / Q000737:chemistry / Q000378:metabolism; D000072417:Protein Domains
chemical_list: D001426:Bacterial Proteins; D045524:Phycobilisomes; D049452:Green Fluorescent Proteins; D002338:Carotenoids