Synchrotron X-rays reveal the modes of Fe binding and trace metal storage in the brown algae Laminaria digitata and Ectocarpus siliculosus.

Ana Mijovilovich, Peter Cloetens, Antonio Lanzirotti, Matt Newville, Gerd Wellenreuther, Puja Kumari, Christos Katsaros, Carl J Carrano, Hendrik Küpper, Frithjof C Küpper

Journal: Metallomics : integrated biometal science 2023;15(10):mfad058

PMID: 37740572

Abstract

Iron is accumulated symplastically in kelp in a non-ferritin core that seems to be a general feature of brown algae. Microprobe studies show that Fe binding depends on tissue type. The sea is generally an iron-poor environment and brown algae were recognized in recent years for having a unique, ferritin-free iron storage system. Kelp (Laminaria digitata) and the filamentous brown alga Ectocarpus siliculosus were investigated using X-ray microprobe imaging and nanoprobe X-ray fluorescence tomography to explore the localization of iron, arsenic, strontium, and zinc, and micro-X-ray absorption near-edge structure (μXANES) to study Fe binding. Fe distribution in frozen hydrated environmental samples of both algae shows higher accumulation in the cortex with symplastic subcellular localization. This should be seen in the context of recent ultrastructural insight by cryofixation-freeze substitution that found a new type of cisternae that may have a storage function but differs from the apoplastic Fe accumulation found by conventional chemical fixation. Zn distribution co-localizes with Fe in E. siliculosus, whereas it is chiefly located in the L. digitata medulla, which is similar to As and Sr. Both As and Sr are mostly found at the cell wall of both algae. XANES spectra indicate that Fe in L. digitata is stored in a mineral non-ferritin core, due to the lack of ferritin-encoding genes. We show that the L. digitata cortex contains mostly a ferritin-like mineral, while the meristoderm may include an additional component.

© The Author(s) 2023. Published by Oxford University Press.

Address: Czech Academy of Sciences, Biology Centre, Institute of Plant Molecular Biology, Laboratory of Plant Biophysics and Biochemistry, Branišovska 1160/31, 370 05 Česke Budějovice, Czech Republic.; ESRF-The European Synchrotron Radiation Facility, Beamline ID16A, 71, avenue des Martyrs CS 40220 38043 Grenoble Cedex 9, France.; Argonne National Laboratory, The University of Chicago, Building 434A, 9700 South Cass Avenue, Lemont, IL 60439, USA.; European XFEL GmbH, Holzkoppel 4, 22869 Schenefeld, Germany.; School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK.; Department of Biology, National and Kapodistrian University of Athens, Panepistimiopolis, Athens 157 84, Hellas, Greece.; Department of Chemistry and Biochemistry, San Diego State University, CA 92182-1030,USA.; Department of Experimental Plant Biology, University of South Bohemia, Branišovská 31/1160, 370 05 České Budějovice, Czech Republic.; Marine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Aberdeen AB24 3UE, UK.
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