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 I. Katsaros; Carl J. Carrano; Hendrik  Küpper; Frithjof Kuepper

doi:10.1093/mtomcs/mfad058

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 I. Katsaros, Carl J. Carrano, Hendrik Küpper, Frithjof Kuepper^* (Corresponding Author)

^*Corresponding author for this work

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Abstract

The sea is a generally 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 XRF tomography to explore the localization of iron, arsenic, strontium and zinc, and µXANES to study Fe binding. Fe distribution in frozen-hydrated environmental samples of both algae shows higher accumulation in the cortex with symplastic subcellular
localisation. This should be seen in the context of recent ultrastructural insight by cryofixation – freeze substitution that found a new type of cisternae which may have a storage function but differs from the apoplastic Fe accumulation found by conventional chemical fixation. Zn distribution colocalizes 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 found mostly 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.

Original language	English
Article number	mfad058
Number of pages	9
Journal	Metallomics
Volume	15
Issue number	10
Early online date	22 Sept 2023
DOIs	https://doi.org/10.1093/mtomcs/mfad058
Publication status	Published - 1 Oct 2023

Bibliographical note

Funding
Funding from the UK Natural Environment Research Council (NERC) through grants NE/D521522/1, NE/F012705/1, and Oceans 2025 (WP4.5) programs to FCK; the National Science Foundation (CHE-1664657) and the National Oceanic & Atmospheric Administration to CJC and FCK; and the MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; grant reference HR09011) is gratefully acknowledged by FCK. PK would like to thank the European Commission for her postdoctoral fellowship (EC-Horizon 2020-MSCA-IF, grant no. 839151).
AM and HK thank the Ministry of Education, Youth and Sports of the Czech Republic with co-financing from the European Union (grant "KOROLID",
CZ.02.1.01/0.0/0.0/15_003/0000336) and the Czech Academy of Sciences (RVO: 60077344).
AM, FK and HK are grateful for support from the European Community in the
framework of the Access to Research Infrastructure Action of the Improving Human Potential Program to the ESRF (experiment LS-2772, beamline ID16AI). AM and HK thank Czech Government funding (Členství v European Synchrotron Radiation Facility, MŠMT – 33914/2017-1) supporting their work at the ESRF. GeoSoilEnviroCARS is supported by the
National Science Foundation – Earth Sciences (EAR – 1634415) and Department of EnergyGeoSciences (DE-FG02-94ER14466). This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. Computational resources were supplied by the project "e-Infrastruktura CZ" (e-INFRA CZ LM2018140) supported by the Ministry of Education, Youth and Sports of the Czech
Republic.

Data Availability Statement

Data are available upon reasonable request to the corresponding author. Raw data collected at ESRF is available from data portal. Kuepper, F. C., Kuepper, H., & Mijovilovich, A. E. (2021). Exploring the localization and potential functional links between stored iodine and iron in brown algae [dataset]. European Synchrotron Radiation Facility. https://doi.org/10.15151/ESRF-ES-102373644.

Supplementary data are available at Metallomics online.

Keywords

algae
iron
strontium
tomography
XANES
ferritin

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Cite this

Mijovilovich, A., Cloetens, P., Lanzirotti, A., Newville, M., Wellenreuther, G., Kumari, P., Katsaros, C. I., Carrano, C. J., Küpper, H., & Kuepper, F. (2023). Synchrotron X-rays reveal the modes of Fe binding and trace metal storage in the brown algae Laminaria digitata and Ectocarpus siliculosus. Metallomics, 15(10), Article mfad058. https://doi.org/10.1093/mtomcs/mfad058

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abstract = "The sea is a generally 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 XRF tomography to explore the localization of iron, arsenic, strontium and zinc, and µXANES to study Fe binding. Fe distribution in frozen-hydrated environmental samples of both algae shows higher accumulation in the cortex with symplastic subcellular localisation. This should be seen in the context of recent ultrastructural insight by cryofixation – freeze substitution that found a new type of cisternae which may have a storage function but differs from the apoplastic Fe accumulation found by conventional chemical fixation. Zn distribution colocalizes 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 found mostly 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.",

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note = "Funding Funding from the UK Natural Environment Research Council (NERC) through grants NE/D521522/1, NE/F012705/1, and Oceans 2025 (WP4.5) programs to FCK; the National Science Foundation (CHE-1664657) and the National Oceanic & Atmospheric Administration to CJC and FCK; and the MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; grant reference HR09011) is gratefully acknowledged by FCK. PK would like to thank the European Commission for her postdoctoral fellowship (EC-Horizon 2020-MSCA-IF, grant no. 839151). AM and HK thank the Ministry of Education, Youth and Sports of the Czech Republic with co-financing from the European Union (grant {"}KOROLID{"}, CZ.02.1.01/0.0/0.0/15_003/0000336) and the Czech Academy of Sciences (RVO: 60077344). AM, FK and HK are grateful for support from the European Community in the framework of the Access to Research Infrastructure Action of the Improving Human Potential Program to the ESRF (experiment LS-2772, beamline ID16AI). AM and HK thank Czech Government funding ({\v C}lenstv{\'i} v European Synchrotron Radiation Facility, M{\v S}MT – 33914/2017-1) supporting their work at the ESRF. GeoSoilEnviroCARS is supported by the National Science Foundation – Earth Sciences (EAR – 1634415) and Department of EnergyGeoSciences (DE-FG02-94ER14466). This research used resources of the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. Computational resources were supplied by the project {"}e-Infrastruktura CZ{"} (e-INFRA CZ LM2018140) supported by the Ministry of Education, Youth and Sports of the Czech Republic.",

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AU - Lanzirotti, Antonio

AU - Newville, Matt

AU - Wellenreuther, Gerd

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AU - Katsaros, Christos I.

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KW - strontium

KW - tomography

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ER -

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

Abstract

Bibliographical note

Data Availability Statement

Keywords

Access to Document

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