title: A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake.
abstract: Numerous cellular functions including respiration require iron. Plants and phytoplankton must also maintain the iron-rich photosynthetic electron transport chain, which most likely evolved in the iron-replete reducing environments of the Proterozoic ocean [1]. Iron bioavailability has drastically decreased in the contemporary ocean [1], most likely selecting for the evolution of efficient iron acquisition mechanisms among modern phytoplankton. Mesoscale iron fertilization experiments often result in blooms dominated by diatoms [2], indicating that diatoms have adaptations that allow survival in iron-limited waters and rapid multiplication when iron becomes available. Yet the genetic and molecular bases are unclear, as very few iron uptake genes have been functionally characterized from marine eukaryotic phytoplankton, and large portions of diatom iron starvation transcriptomes are genes encoding unknown functions [3-5]. Here we show that the marine diatom Phaeodactylum tricornutum utilizes ISIP2a to concentrate Fe(III) at the cell surface as part of a novel, copper-independent and thermodynamically controlled iron uptake system. ISIP2a is expressed in response to iron limitation several days prior to the induction of ferrireductase activity, and it facilitates significant Fe(III) uptake during the initial response to Fe limitation. ISIP2a is able to directly bind Fe(III) and increase iron uptake when heterologously expressed, whereas knockdown of ISIP2a in P. tricornutum decreases iron uptake, resulting in impaired growth and chlorosis during iron limitation. ISIP2a is expressed by diverse marine phytoplankton, indicating that it is an ecologically significant adaptation to the unique nutrient composition of marine environments.
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Joe
authors.initials: J
authors.lastname: Morrissey
authors.affiliation: Department of Parasitology, Faculty of Science, Charles University, Vinicna 7, 12844 Prague, Czech Republic.
authors.forename: Robert
authors.initials: R
authors.lastname: Sutak
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Javier
authors.initials: J
authors.lastname: Paz-Yepes
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Atsuko
authors.initials: A
authors.lastname: Tanaka
authors.affiliation: Department of Biology and Biotechnology Graduate Program, American University in Cairo, New Cairo 11835, Egypt.
authors.forename: Ahmed
authors.initials: A
authors.lastname: Moustafa
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Alaguraj
authors.initials: A
authors.lastname: Veluchamy
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Yann
authors.initials: Y
authors.lastname: Thomas
authors.affiliation: Laboratoire d'Océanographie Microbienne, Observatoire Océanologique, Sorbonne Universités, Université Pierre et Marie Curie, Université Paris 06, UMR 7621, Quai Racovizta, 66650 Banyuls/mer, France.
authors.forename: Hugo
authors.initials: H
authors.lastname: Botebol
authors.affiliation: Laboratoire d'Océanographie Microbienne, Observatoire Océanologique, Sorbonne Universités, Université Pierre et Marie Curie, Université Paris 06, UMR 7621, Quai Racovizta, 66650 Banyuls/mer, France.
authors.forename: François-Yves
authors.initials: FY
authors.lastname: Bouget
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, Capricorn Lane, San Diego, CA 92037 USA.
authors.forename: Jeffrey B
authors.initials: JB
authors.lastname: McQuaid
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France.
authors.forename: Leila
authors.initials: L
authors.lastname: Tirichine
authors.affiliation: Microbial and Environmental Genomics, J. Craig Venter Institute, Capricorn Lane, San Diego, CA 92037 USA.
authors.forename: Andrew E
authors.initials: AE
authors.lastname: Allen
authors.affiliation: Institut Jacques Monod, Université Paris Diderot & CNRS, UMR7592, 15 rue Hélène Brion, 75013 Paris, France. Electronic address: lesuisse.emmanuel@ijm.univ-paris-diderot.fr.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Lesuisse
authors.affiliation: Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 INSERM U1024, 46 Rue d'Ulm, 75005 Paris, France. Electronic address: cbowler@biologie.ens.fr.
authors.forename: Chris
authors.initials: C
authors.lastname: Bowler
mesh_terms: D017377:Diatoms / Q000378:metabolism*; D020869:Gene Expression Profiling; D007501:Iron / Q000378:metabolism* / Q000493:pharmacokinetics; D008386:Marine Biology; D008565:Membrane Proteins / Q000378:metabolism*; D010839:Phytoplankton / Q000378:metabolism*; D017434:Protein Structure, Tertiary; D012623:Seawater / Q000737:chemistry*; D013045:Species Specificity
chemical_list: D008565:Membrane Proteins; D007501:Iron