Ordered ferrimagnetic form of ferrihydrite reveals links among structure, composition, and magnetism F. Marc Michela,b,1, Vidal Barrónc, José Torrentc, María P. Moralesd, Carlos J. Sernad, Jean-François Boilye, Qingsong Liuf, Andrea Ambrosinig, A. Cristina Cismasua, and Gordon E. Brown Jr.a,b aSurface and Aqueous Geochemistry Group, Department of Geological & Environmental Sciences, Stanford University, Stanford, CA 94305; bStanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, CA 94025; cDepartamento de Ciencias y Recursos Agrícolas y Forestales, Universidad de Córdoba, Campus de Rabanales, 14071 Córdoba, Spain; dInstituto de Ciencia de Materiales de Madrid (CSIC), 28049 Cantoblanco, Madrid, Spain; eDepartment of Chemistry, Umeå University, SE 901 87 Umeå, Sweden; fPaleomagnetism and Geochronology Laboratory (SKL-LE), Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China; and gSandia National Laboratories, PO Box 5800, MS 1415, Albuquerque, NM 87185 Edited* by W. G. Ernst, Stanford University, Stanford, CA, and approved December 30, 2009 (received for review September 4, 2009) The natural nanomineral ferrihydrite is an important component of unequivocally by conventional crystallographic techniques. The many environmental and soil systems and has been implicated as most recent model, and arguably the most complete, was derived the inorganic core of ferritin in biological systems. Knowledge of its from analysis of the pair distribution function of x-ray total scat- basic structure, composition, and extent of structural disorder is es- tering data that suggested that the ferrihydrite structure, although sential for understanding its reactivity, stability, and magnetic be- disordered, could be described using a single structural phase (6). havior, as well as changes in these properties during aging. Here However, this model has since received criticism for giving a we investigate compositional, structural, and magnetic changes composition that is anomalously H-poor (7) as well as not fully that occur upon aging of “2-line” ferrihydrite in the presence of satisfying the observed diffraction features (7), calculated bond adsorbed citrate at elevated temperature. Whereas aging under valence sums (5), or the measured density (7, 8) of ferrihydrite. these conditions ultimately results in the formation of hematite, In addition, ferrihydrite, whether natural or synthetic, is generally analysis of the atomic pair distribution function and complemen- found to be antiferromagnetic with superparamagnetic behavior tary physicochemical and magnetic data indicate formation of an at ambient temperature [see (15) and references therein]. Several intermediate ferrihydrite phase of larger particle size with few de- studies also suggested an additional ferromagnetic-like compo- fects, more structural relaxation and electron spin ordering, and nent attributed to the presence of uncompensated surficial spins pronounced ferrimagnetism relative to its disordered ferrihydrite (16, 17), but this has been difficult to confirm due to the uncer- precursor. Our results represent an important conceptual advance tainty regarding the relationships between magnetic behavior and in understanding the nature of structural disorder in ferrihydrite basic crystal structure. The metastability of ferrihydrite, par- and its relation to the magnetic structure and also serve to validate ticularly at elevated temperatures, has led to added ambiguity a controversial, recently proposed structural model for this phase. regarding the ordering temperature (i.e., Néel or Curie) because GEOLOGY In addition, the pathway we identify for forming ferrimagnetic direct measurement is not feasible (9). Nonetheless, it is generally ferrihydrite potentially explains the magnetic enhancement that accepted that ferrihydrite’s metastability is related in part to typically precedes formation of hematite in aerobic soil and inherent structural disorder, although the nature and extent of weathering environments. Such magnetic enhancement has been this disorder remain poorly defined. attributed to the formation of poorly understood, nano-sized ferri- Understanding the relationship between the structure and magnets from a ferrihydrite precursor. Whereas elevated tempera- magnetic properties of ferrihydrite, as well as changes in both tures drive the transformation on timescales feasible for laboratory as a function of aging, is of particular importance because it pro- studies, our results also suggest that ferrimagnetic ferrihydrite vides independent constraints on ferrihydrite structure and could form naturally at ambient temperature given sufficient time. compositional variations with aging. Being antiferromagnetic at ambient temperature (15, 18) and with only a weak ferrimagnetic- crystal structure ∣ disorder ∣ nano-sized ferrimagnets ∣ soil formation ∣ like component, ferrihydrite is normally not considered in the in- strain terpretation of magnetic enhancement in soils on Earth (19) or Mars (20), nor is it considered useful in the tailoring of functional he structural and physical properties of ferrihydrite, an exclu- ferrimagnetic nanomaterials, in contrast with the ferrimagnets Tsively nano-sized ferric oxyhydroxide, are of importance in ex- magnetite (Fe3O4) and maghemite (γ-Fe2O3) (21, 22). However, plaining its chemical reactivity and wide variety of occurrences. In as will be shown below, ferrihydrite aged at different tempera- both pristine and contaminated soils and sediments, ferrihydrite tures in the presence of selected anions undergoes a significant acts as a natural filter of inorganic contaminants through sorption magnetic enhancement corresponding to the formation of an in- reactions, thus affecting their transport and fate in the environ- termediate phase preceding its transformation into hematite ment. Biomineralization of ferrihydrite as the inorganic iron core (α-Fe2O3) (11, 23–25), and this phase may play an important in ferritin—the protein mainly involved in iron storage and home- role in the magnetic enhancement of aerobic soils. Additionally, ostasis in the human body—also occurs in a vast number of or- such understanding may lead to new insights about the for- ganisms (1). Bloom-forming marine diatoms, for example, use mation of biogenic magnetic phases in organisms. For example, ferritin for enhanced iron storage (2), which suggests that ferri- hydrite may also have underlying importance in primary produc- ’ Author contributions: F.M.M. and V.B. designed research; F.M.M., V.B., J.T., M.P.M., Q.L., A. tivity in the world s oceans. A., and A.C.C. performed research; F.M.M., J.T., M.P.M., C.J.S., J.-F.B., Q.L., and A well-known example of a nanomineral (3), ferrihydrite has A.A. analyzed data; F.M.M., V.B., J.T., M.P.M., C.J.S., J.-F.B., Q.L., and G.E.B.J. wrote the no known crystalline counterpart formed in the laboratory or paper; and V.B. and J.-F.B. contributed new reagents/analytic tools. found in nature. As such, the basic crystal structure (4–7) The authors declare no conflict of interest. and physical properties of ferrihydrite [e.g., density, composition This Direct Submission article had a prearranged editor. (7, 8), and magnetic properties (9–14)] have remained controver- 1To whom correspondence should be addressed. E-mail: [email protected]. sial. A variety of structural models have been proposed for ferri- This article contains supporting information online at www.pnas.org/cgi/content/full/ hydrite (see (4) for review) but all have proven difficult to confirm 0910170107/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.0910170107 PNAS ∣ February 16, 2010 ∣ vol. 107 ∣ no. 7 ∣ 2787–2792 Downloaded by guest on September 27, 2021 ferritin-derived ferrihydrite in humans, with varying degrees of to the period of significant magnetic enhancement (Fig. 1B), an structural order, has been related to different neurodegenerative extended set of diffraction maxima develop from regions formerly diseases (26). In this regard, biogenic ferrimagnetic crystals, dominated by diffuse scattering (see SI Appendix) with no indica- identified as magnetite, that have been found in human brain tion of a structural transformation prior to that involving the for- tissues (27–29) may originate from biodegradation of a ferrihy- mation of hematite. These changes signal the formation of the drite precursor. ferrifh phase. Here we have synthesized a series of ferrihydrite samples with The transition from fh to ferrifh is accompanied by changes in differing magnetic properties and structural order that allowed us particle size and composition. Relative to the precursor fh, the to determine compositional and structural changes occurring average particle size of the nonhematite fraction, as indicated with aging and to explain the enhanced magnetic properties by transmission electron microscopy, increases by approximately mentioned above (see Methods Summary and SI Appendix). We 200% (Fig. 2A) and corresponds to an approximately 50% de- used the atomic pair distribution function (PDF) derived from syn- crease in specific surface area (Fig. 2B, see SI Appendix). In ad- chrotron high-energy x-ray total scattering to discriminate be- dition, density (Fig. 2B) and total Fe (Fig. 2C) of the solid phase tween competing structural models and detect subtle structural during the initial 8 h aging period increased by 15% and 18%, changes in the transformation of ferrihydrite to hematite. Both respectively,