title: No evidence for intracellular magnetite in putative vertebrate magnetoreceptors identified by magnetic screening.
abstract: The cellular basis of the magnetic sense remains an unsolved scientific mystery. One theory that aims to explain how animals detect the magnetic field is the magnetite hypothesis. It argues that intracellular crystals of the iron oxide magnetite (Fe3O4) are coupled to mechanosensitive channels that elicit neuronal activity in specialized sensory cells. Attempts to find these primary sensors have largely relied on the Prussian Blue stain that labels cells rich in ferric iron. This method has proved problematic as it has led investigators to conflate iron-rich macrophages with magnetoreceptors. An alternative approach developed by Eder et al. [Eder SH, et al. (2012) Proc Natl Acad Sci USA 109(30):12022-12027] is to identify candidate magnetoreceptive cells based on their magnetic moment. Here, we explore the utility of this method by undertaking a screen for magnetic cells in the pigeon. We report the identification of a small number of cells (1 in 476,000) with large magnetic moments (8-106 fAm(2)) from various tissues. The development of single-cell correlative light and electron microscopy (CLEM) coupled with electron energy loss spectroscopy (EELS) and energy-filtered transmission electron microscopy (EFTEM) permitted subcellular analysis of magnetic cells. This revealed the presence of extracellular structures composed of iron, titanium, and chromium accounting for the magnetic properties of these cells. Application of single-cell CLEM to magnetic cells from the trout failed to identify any intracellular structures consistent with biogenically derived magnetite. Our work illustrates the need for new methods to test the magnetite hypothesis of magnetosensation.
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
authors.forename: Nathaniel B
authors.initials: NB
authors.lastname: Edelman
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Tanja
authors.initials: T
authors.lastname: Fritz
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Simon
authors.initials: S
authors.lastname: Nimpf
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Paul
authors.initials: P
authors.lastname: Pichler
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Mattias
authors.initials: M
authors.lastname: Lauwers
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Robert W
authors.initials: RW
authors.lastname: Hickman
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Artemis
authors.initials: A
authors.lastname: Papadaki-Anastasopoulou
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria;
authors.forename: Lyubov
authors.initials: L
authors.lastname: Ushakova
authors.affiliation: Campus Science Support Facilities, 1030 Vienna, Austria; and.
authors.forename: Thomas
authors.initials: T
authors.lastname: Heuser
authors.affiliation: Campus Science Support Facilities, 1030 Vienna, Austria; and.
authors.forename: Guenter P
authors.initials: GP
authors.lastname: Resch
authors.affiliation: Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, Perth, WA 6009, Australia.
authors.forename: Martin
authors.initials: M
authors.lastname: Saunders
authors.affiliation: Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, Perth, WA 6009, Australia.
authors.forename: Jeremy A
authors.initials: JA
authors.lastname: Shaw
authors.affiliation: Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), 1030 Vienna, Austria; keays@imp.ac.at.
authors.forename: David A
authors.initials: DA
authors.lastname: Keays
mesh_terms: D000818:Animals; D048430:Cell Shape; D003051:Cochlea / Q000166:cytology / Q000648:ultrastructure; D010856:Columbidae; D052203:Ferrosoferric Oxide / Q000378:metabolism*; D042541:Intracellular Space / Q000378:metabolism*; D060328:Magnetic Phenomena; D011956:Receptors, Cell Surface / Q000378:metabolism*; D013347:Subcellular Fractions / Q000378:metabolism; D014337:Trout; D014714:Vertebrates / Q000378:metabolism*
chemical_list: D011956:Receptors, Cell Surface; D052203:Ferrosoferric Oxide
keywords: magnetite; magnetoreception; pigeons