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.

Department of Biology and Biotechnology Graduate Program American University in Cairo New Cairo 11835 Egypt

Department of Parasitology Faculty of Science Charles University Vinicna 7 12844 Prague Czech Republic

Institut de Biologie de l'Ecole Normale Supérieure UMR 8197 INSERM U1024 46 Rue d'Ulm 75005 Paris France

Institut Jacques Monod Université Paris Diderot and CNRS UMR7592 15 rue Hélène Brion 75013 Paris France

Laboratoire d'Océanographie Microbienne Observatoire Océanologique Sorbonne Universités Université Pierre et Marie Curie Université Paris 06 UMR 7621 Quai Racovizta 66650 Banyuls mer France

Microbial and Environmental Genomics J Craig Venter Institute Capricorn Lane San Diego CA 92037 USA

References provided by Crossref.org

In vivo localization of iron starvation induced proteins under variable iron supplementation regimes in Phaeodactylum tricornutum

Proximity proteomics in a marine diatom reveals a putative cell surface-to-chloroplast iron trafficking pathway

Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

Iron Uptake Mechanisms in Marine Phytoplankton

Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms

Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms

Ostreococcus tauri is a new model green alga for studying iron metabolism in eukaryotic phytoplankton

Central role for ferritin in the day/night regulation of iron homeostasis in marine phytoplankton