In Situ Magnetic Identification of Giant, Needle-Shaped Magnetofossils in Paleocene–Eocene Thermal Maximum Sediments

In situ magnetic identification of giant, needle-shaped magnetofossils in Paleocene–Eocene Thermal Maximum sediments

Courtney L. Wagnera,1, Ramon Eglib, Ioan Lascuc, Peter C. Lipperta,d, Kenneth J. T. Livie, and Helen B. Searsf

aDepartment of Geology and Geophysics, University of Utah, Salt Lake City, UT 84112; bDivision of Data, Methods and Models, Central Institute of Meteorology and Geodynamics, 1190 Vienna, Austria; cDepartment of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560; dGlobal Change and Sustainability Center, University of Utah, Salt Lake City, UT 84112; eMaterials Characterization and Processing Center, Department of Materials Sciences and Engineering, Johns Hopkins University, Baltimore, MD 21218; and fDepartment of Geology, Colby College, Waterville, ME 04901

Edited by Lisa Tauxe, University of California San Diego, La Jolla, CA, and approved November 24, 2020 (received for review August 27, 2020) Near-shore marine sediments deposited during the Paleocene– These magnetofossils are interpreted to be the predominant Eocene Thermal Maximum at Wilson Lake, NJ, contain abundant source of the PETM magnetic enhancement of these cores (7, conventional and giant magnetofossils. We find that giant, 11–14), although alternative sources have been suggested (15–18). needle-shaped magnetofossils from Wilson Lake produce distinct Giant magnetofossils have so far only been identified in sediments magnetic signatures in low-noise, high-resolution first-order rever- from the PETM and the Middle Eocene Climatic Optimum, sal curve (FORC) measurements. These magnetic measurements on leading to the interpretation that they are unique to hyperthermal bulk sediment samples identify the presence of giant, needle- events(6,7,11–14). For example, Chang et al. (6) suggest that shaped magnetofossils. Our results are supported by micromag- giant magnetofossils are linked to oceanic deoxygenation during netic simulations of giant needle morphologies measured from the PETM. transmission electron micrographs of magnetic extracts from Wil- Previous studies, which used micromagnetic simulations, son Lake sediments. These simulations underscore the single- electron holography, or both, suggest that giant magnetofossils domain characteristics and the large magnetic coercivity associ- have distinct magnetic properties (6, 11, 14, 18, 19). These in-

ated with the extreme crystal elongation of giant needles. Giant EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES terpretations are limited, however, by assumptions regarding magnetofossils have so far only been identified in sediments deposited during global hyperthermal events and therefore may crystal arrangement, spacing, and magnetic domain structure, serve as magnetic biomarkers of environmental disturbances. and they lack independent confirmation of defining character- Our results show that FORC measurements are a nondestructive istics. Additionally, some of these methods have been applied to method for identifying giant magnetofossil assemblages in bulk only a few giant magnetofossil morphologies. sediments, which will help test their ecology and significance with Here we show independent, physical evidence of the magnetic respect to environmental change. signature of giant magnetofossils in situ (i.e., not in extracts) using low-noise, high-resolution first-order reversal curves magnetofossils | magnetotactic bacteria | first-order reversal curves | (FORCs). FORC routines measure the response of all magnetic micromagnetic modeling | biogenic needles particles, including giant magnetofossils, within a bulk sediment

he Paleocene–Eocene Thermal Maximum (PETM; ∼56 Ma) Significance Tis a geologically rapid global warming event with many characteristics that make it an analog for the Anthropocene (1, Giant magnetofossils are the preserved remains of iron- 2). These characteristics include rapid warming of the sea surface biomineralizing organisms that have so far been identified and atmosphere, increased seasonality of precipitation and only in sediments deposited during ancient greenhouse cli- temperature, and biological extinctions (1). The PETM is iden- mates. Giant magnetofossils have no modern analog, but their tified globally by a −3‰ carbon isotope excursion (CIE) in bulk association with abrupt global warming events links them to marine carbonate and is characterized by three stratigraphic in- environmental disturbances. Thus, giant magnetofossils may tervals: 1) a preonset excursion, 2) the main CIE, and 3) a re- encode information about nutrient availability and water covery toward baseline δ13C levels (1). The main CIE interval is stratification in ancient aquatic environments. Identification of further subdivided into the CIE onset and CIE core, which giant magnetofossils has previously required destructive ex- correspond to the first ∼6 to 10 kyr and 100 to 200 kyr of the traction techniques. We show that giant, needle-shaped mag- PETM (1, 3, 4). The Wilson Lake A (WL-A) core from Wilson netofossils have distinct magnetic signatures. Our results Lake, NJ, contains a continental shelf section of the PETM provide a nondestructive method for identifying giant mag- within the Marlboro Clay and, within the Marlboro Clay, an netofossil assemblages in bulk sediments, which will help test expanded and nearly complete record of the CIE onset and CIE their significance with respect to environmental change. core (1, 5). Several near-shore and offshore cores complement Author contributions: C.L.W. designed research; C.L.W., R.E., I.L., P.C.L., K.J.T.L., and H.B.S. the WL-A record and enable a broader understanding of how performed research; C.L.W., R.E., I.L., P.C.L., and K.J.T.L. analyzed data; C.L.W., P.C.L., and Paleogene coastal ecosystems responded to the rapid onset K.J.T.L. provided TEM interpretations; R.E. provided FORC interpretations; I.L. provided of global hyperthermal conditions (5–8). The New Jersey con- micromagnetic interpretations; and C.L.W., R.E., I.L., and P.C.L. wrote the paper. tinental shelf experienced an overall rapid influx of clay, min- The authors declare no competing interest. eralization of iron oxides, dinoflagellate blooms, and benthic This article is a PNAS Direct Submission. foraminifera species turnover coincident with the CIE onset Published under the PNAS license. (5,9,10). 1To whom correspondence may be addressed. Email: [email protected]. Abundant conventional and giant magnetofossils, the fossil re- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ mains of magnetotactic bacteria and other iron-biomineralizing doi:10.1073/pnas.2018169118/-/DCSupplemental. microorganisms, were identified in several New Jersey cores. Published February 1, 2021.

PNAS 2021 Vol. 118 No. 6 e2018169118 https://doi.org/10.1073/pnas.2018169118 | 1of7 Downloaded by guest on September 25, 2021 sample. We also present micromagnetic simulations of giant also been proposed (15, 16, 18, 20). One of the reasons for the needle-shaped crystals whose morphologies were characterized ambiguity in interpreting the origin of magnetic nanoparticles in with transmission electron microscopy (TEM) of magnetic ex- the Marlboro Clay is the selective extraction of magnetofossils tracts. Our results show that giant, needle-shaped magnetofossils with large magnetic moments, in contrast to abiotic iron oxides; produce a high-coercivity component distinct from conventional this selective extraction might explain their dominance in TEM magnetofossils that is identified using a specific FORC mea- observations (18, 20). Here we provide a detailed characteriza- surement protocol. We argue that these are definitive magnetic tion of the magnetofossil signature in a bulk sediment sample by signatures of giant magnetofossils, which further supports the comparing low-noise, high-resolution FORC measurements on interpretation that the magnetic enhancement of the WL-A core specimen WL35950b, from the CIE onset interval at WL-A, to has a biogenic origin. The link between giant magnetofossils, that of BAL13, a sediment sample from Lake Baldeggersee in hyperthermal events, and oceanic deoxygenation makes the Switzerland (Fig. 1), where the magnetic signature of conven- magnetic signature of giant needles a powerful tool for identifying tional magnetofossils was isolated for the first time (21). The giant magnetofossil assemblages and, by extension, testing their magnetic signature of conventional magnetofossils consists of ecological significance in the context of global change events in the two narrow coercivity components associated with single-domain geologic record. particles, referred to as biogenic soft and biogenic hard (21, 22). These magnetic characteristics have been confirmed by analysis Results of several freshwater and marine magnetofossil-rich sediments Low-Noise, High-Resolution FORCs. Previous studies suggest that (23–26) and are therefore considered representative of conven- the magnetic enhancement of the WL-A core is due to abundant tional magnetofossils. The single-domain character and nar- magnetofossils (12, 13) found in magnetic extracts. Other sour- rowness of these biogenic coercivity components reflect the ces of single-domain magnetite particles, such as debris from a tightly genetically controlled biomineralization process in pro- comet or pyrogenic magnetite produced during wildfires, have ducing highly uniform magnetic structures.

F E

Fig. 1. Low-noise, high-resolution FORC measurements for WL35950b and BAL13. (A) Three distinct coercivity distributions identified in WL35950b. Arrows indicate the coercivity components BS (biogenic soft), BH (biogenic hard), BN (biogenic needles), and HC (high coercivity). (B) Same as A for BAL13. (C) FORC diagram for WL35950b. Arrows point to the following features: doublet of positive and negative amplitudes produced by reversible magnetic moment rotation in uniaxial SD (single-domain) particles (SDR); high-coercivity SDR termination (SDRT); high-coercivity termination of flux closure annihilation (FCAT) from particles and/or aggregates of particles (clumps, collapsed chains) with vortex-like magnetization states; and FCAT for biogenic needles (FCAT [BN]). (D) FORC diagram for BAL13, plotted to scale with C.(E) Isolated central ridge contribution to the FORC diagram of WL35950b, with 10× vertical exaggeration

highlighting the vertical offset with respect to Bu = 0. The dashed line is the expected Bu value for each vertical profile of the central ridge. (F) Vertical central ridge offset for WL35950b (dashed line) and BAL13 (solid line) Bc,with1σ confidence intervals (shaded). These offsets are related inversely to the thermal activation volume of SD particles. Arrows point to coercivity ranges dominated by viscous particles (VISC), biogenic particles (BS, BH, and BN), and high- coercivity particles (HC). The SDRT marks the transition from biogenic to high-coercivity contributions.

2of7 | PNAS Wagner et al. https://doi.org/10.1073/pnas.2018169118 In situ magnetic identification of giant, needle-shaped magnetofossils in Paleocene–Eocene Thermal Maximum sediments Downloaded by guest on September 25, 2021 FORC measurements M(Br, B) are represented as two- (Mrs/Ms, the saturation remanence Mrs normalized to saturation dimensional density functions in FORC diagrams, which are magnetization Ms). Simulated hysteresis loops indicate that Bc M defined as the second mixed derivative of magnetization, , and and Bsw for needle-shaped particles with lengths of 1,000 nm and B plotted in coordinates of magnetic coercivity, c, and magnetic widths up to 100 nm reach maximum values (∼310 mT) when B SI Appendix SI Text offset or interaction, u (27, 28) (see , , for a field orientations are parallel and perpendicular, respectively, to glossary of magnetic terminology). Three coercivity distribution particle elongation (Fig. 2 and SI Appendix, Fig. S2). The average types, characterized by specific magnetization responses to Bc is ∼92 mT, and the average Bsw is ∼148 mT. Notably, however, magnetic particles with different domain states (29), were the averages for the two thinnest needles (21 and 25 nm, both A B obtained from our FORC measurements (Fig. 1 and ). The 1,000 nm long) are B ∼110 mT and B ∼165 mT. The ∼165 mT f c sw first is dcd, the first derivative of direct current demagnetization switching field value matches the peak central ridge offset at 170 M B f curves ( r, 0). The median of dcd defines the coercivity of F B B B f mT (Fig. 1 ). Generally, c and sw decrease with increasing remanence cr. The second distribution is irr, the first derivative needle width due to the emergence of nonhomogeneous of the irreversible component of the ascending hysteresis branch. switching modes (e.g., curling). B follows this trend at all field In contrast to other coercivity distributions, f is also defined for sw irr angles (ϕ), while B values are width-independent for ϕ > 60°. negative fields, where transitions between magnetic states that c The angular dependences of B and B generally track those for occur without reversing the field direction are recorded. Ac- c sw the model of coherent rotation of atomic spin moments (36) for cordingly, firr(B < 0) = 0 for uniaxial, noninteracting single- f B < A the three thinnest needle morphologies and the curling model domain particles. Nonzero values of irr( 0) in Fig. 1 and B B correspond to flux closure nucleation in FORCs beginning at (37) for the 100-nm-wide needle (Fig. 2 ). At large field angles positive reversal fields. The third coercivity distribution is f , the the spin moments continue rotating, yielding negative magneti- cr B central ridge coercivity distribution, and is defined as the integral zation values before the switching event occurs, so that sw will be larger than B . At small field angles, B coincides with B . of the central ridge over Bu. The central ridge is a sharp signature c sw c of FORC diagrams located along or close to Bu = 0 (Fig. 1 C and For the 21- to 50-nm-wide needles the switching process can D). It is produced by isolated particles or groups of particles, include a buckling or fanning component (38), whereby moments such as magnetosome chains, possessing magnetic states capable of single-domain remanence (29–32). FORC signatures typical of magnetofossil-rich sediments include the following three A characteristics: a central ridge; a doublet of positive and negative

amplitudes, nearly antisymmetric with respect to the Bu = −Bc EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES diagonal; and positive amplitudes above the central ridge with a similar distribution along Bc (31, 33) (SI Appendix, Text S1.1). The isolated central ridge of the WL35950b FORC diagram is characterized by a small, Bc-dependent vertical offset δBu (dashed line in Fig. 1E) caused by the effect of thermal activa- tions on the switching field (Bsw) of single-domain particles (34). Larger offsets are caused by smaller energy barriers which, in magnetite, correspond to smaller blocking volumes. This offset is compared with that of BAL13 in Fig. 1F. Between 0 and 10 mT, B where magnetically viscous particles contribute to the central ridge, δBu decreases sharply from 0.7 to ∼0.4 mT. It then remains nearly constant over the coercivity range of biogenic soft magnetofossils (10 to 50 mT) and increases slightly to ∼0.45 mT over the coercivity range of biogenic hard magnetofossils (50 to 100 mT). The corresponding offset observed in the FORC distribution of sample BAL13 cannot be calculated beyond 110 mT because the central ridge disappears above this Bc value. In contrast, δBu continues to increase almost linearly in WL35950b up to Bc ∼ 140 mT. Between 140 and 210 mT, a broad peak with a maximum δBu of ∼0.7 mT is observed. Above ∼210 mT, δBu returns to the ideal continuation of the linear trend observed over the coercivity range for biogenic soft and biogenic hard magnetofossils (Fig. 1). As seen with lower-resolution measurements up to Bc = 800 mT, the coercivity distribution associated with the central ridge reaches a minimum at ∼300 mT and then Fig. 2. Summary of results from micromagnetic simulations on the 21-, SI Appendix 25-, 50-, and 100-nm-wide needles observed in magnetic extracts from WL35900 increases again at higher fields ( , Fig. S1). This and WL35800 (50 and 100 nm) and inferred from our low-noise, high- minimum represents the transition from SD magnetite contri- resolution FORC measurements (21 and 25 nm). Simulations were per- butions, whose theoretical upper coercivity limit is 300 mT, to formed as a function of the angle (ϕ) between the applied field and the high-coercivity minerals (e.g., goethite) (35). particle elongation direction, which was oriented in the z direction. The angular dependence was compared to Stoner–Wohlfarth (36) calculations Micromagnetic Modeling. We performed micromagnetic simula- for coherent rotation in an infinite cylinder (dashed and solid black lines, ϕ tions of the magnetic hysteresis produced by giant, needle- S-W). (A) Magnetic squareness (Mrs/Ms) as a function of . The angular de- ϕ = ϕ shaped magnetofossils identified within the CIE onset interval pendence follows the S-W model, Mrs/Ms( ) cos . The dashed line is for = at WL-A (Fig. 4, Table S1). These simulations predict the Mrs/Ms(0°) 1, which is the case for the 21- to 50-nm-wide needles (see also SI Appendix, Fig. S2). (B) Coercivity (B ) and switching field (B ) as a function magnetic behavior and the associated FORC diagram signature c sw of ϕ.Forϕ < 60°, the symbols for Bc and Bsw overlap. The gray dashed lines of the giant needles. The key parameters extracted from the are calculations of the nucleation field for cases exhibiting fanning (S ≤.1.63) simulated hysteresis loops include the field at which the loop and curling (S > 1.63) of moments. S is a parameter that depends on particle B B magnetization reverses sign ( c), the switching field ( sw, the width, exchange constant, and Ms (see SI Appendix, Text S2, for details of field at which the magnetization state reverses), and squareness the theoretical calculations).

Wagner et al. PNAS | 3of7 In situ magnetic identification of giant, needle-shaped magnetofossils in Paleocene–Eo- https://doi.org/10.1073/pnas.2018169118 cene Thermal Maximum sediments Downloaded by guest on September 25, 2021 can have single-domain and non–single-domain magnetic structures depending on their size, shape, and arrangement in chain structures (11). Together, these observations suggest that magnetic navigation might not have been the only purpose of giant bullets, spindles, and elongate prisms. Alternatively, abundant bioavailable iron, from enhanced continental weathering during the PETM (1), may have decreased the pressure to biomineralize morphologies with the most efficient magnetic moments. Our micromagnetic simulations indicate that giant needles possess a stable single-domain–like remanence without the need for chain arrangements if their widths do not exceed ∼150 nm for particles ≥500 nm in length. This is close to the upper limit of the few available TEM observations of these crystals (e.g., Fig. 4); however, the real size distribution is likely wider and would therefore exceed the single-domain stability range of isolated crystals. We note that our few TEM observations are limited by the fact that giant needles are less abundant and they may be more difficult to dislodge from bulk sediment than conventional magnetofossils. Fig. 3. Dimensional analysis of magnetofossils identified in WL35900 and WL35800 with predicted domain states at room temperature. The theoret- Discussion ical single-domain states for individual grains and magnetofossil chains are highlighted: 1) lower limit for a six-crystal chain with intercrystal gaps of Magnetofossil Components Identified from the Central Ridge f 0 (lower curve) and 0.6 times the length of constituent crystals (41), 2) lower Coercivity Distribution ( cr). There are two principal differences limit for isolated single-domain particles (39), 3) upper limits for isolated between the three coercivity distributions obtained from our single-domain particles with long axes parallel to the 〈100〉 and 〈111〉 crys- FORC measurements for WL359050b and BAL13 (Fig. 1 A and tallographic axes (40), and 4) critical sizes for isolated crystals within a chain B). First, firr and fcr are determined by in-field (i.e., induced) of three crystals (40). Dimensions of modern magnetosomal magnetite of magnetization states, whereas fdcd probes remanent magnetization various shapes from well-characterized magnetotactic bacteria and con- states. Second, only a selected subset of micromagnetic transitions ventional magnetofossils are shown in color (for a complete list of data contribute to f , namely, those to the positive saturation state is a sources, see SI Appendix, Text S3). cr sequence of transitions that started from negative saturation (29). In single-domain particles and structures with single-domain be- at needle extremities tend to rotate at a different rate than havior, such as magnetosome chains, there is only one transition moments in the center (e.g., SI Appendix, Figs. S3 F, G, J, and K during FORC measurements, from a negative to a positive single- and S4 F, G, J, and K and Movies S1–S6). For the 100-nm-wide domain state. It is this transition that contributes to the central particle, maximum curling occurs just prior to the switching ridge, which explains its dominance in magnetofossil signatures. event (SI Appendix, Figs. S3C and S4C and Movies S7 and S8). Slightly larger particles possess a few more magnetic states (43), The angular dependence of Mrs/Ms follows the Stoner–Wohlfarth perhaps related to the nucleation of magnetic vortices (32), but model for the magnetization of single-domain particles (Fig. 2A) transitions to the positive single-domain state still contribute sig- (36) because all needles are almost homogeneously magnetized in nificantly to the central ridge. The number of magnetic states a null field. We also modeled a 150-nm-wide needle (SI Appendix, grows rapidly with particle size, and the relative contribution of Fig. S5) that switches nonhomogeneously via vortex nucleation the central ridge to the total magnetic signal decreases accord- and annihilation; this magnetic behavior will not contribute to the ingly, until it disappears fully. The contribution of magnetic central ridge signal at high fields. structures with non–single-domain behavior, such as collapsed chains, some giant magnetofossils, lithogenic magnetite, and tita- TEM. Magnetofossil dimensional measurements (Table S1) are nomagnetite, explain the smaller amplitude of fcr.Thestrong used to predict the domain state of the nine magnetofossil cat- single-domain selectivity of the central ridge is similar to that of egories preserved within the CIE onset interval at WL-A. We anhysteretic remanent magnetization (ARM) (44), so that fcr is identified nine magnetofossil categories: immature, cuboctahe- closely related to the coercivity distribution obtained from the dra, small bullets, medium bullets, elongate prisms, large bullets, alternating field demagnetization of ARM (44). giant bullets, spindles, and needles; the latter three are giant magnetofossil morphologies (11, 14). Giant magnetofossils are only identified within magnetic extracts from the CIE onset interval, so we use only measurements from extracts WL35900 and WL35800 for our analysis. Conventional magnetofossil morphologies (e.g., cuboctahedra, small bullets, medium bullets, and large bullets) are within or close to the stability range of isolated single-domain particles (Fig. 3) (39, 40). If chain geometries are considered, then the single-domain stability range is expanded by the stabilizing effect of positive magnetostatic interactions (40, 41); in this context, all particles identified as conventional magnetofossils are within the single-domain stability range. This 1 µm 1 µm is expected if magnetofossils are optimized for magnetic navigation, in which case they must provide the maximum magnetic Fig. 4. TEM images of giant needles from magnetic extract WL35900 moment with the minimum amount of iron (42). In contrast, highlighted with red arrows. Two needles are shown in the Left panel, giant bullets, spindles, and elongate prisms cluster around the whereas the Right panel shows a single needle with several conventional upper limit of the single-domain stability range. Specific micro- magnetofossils in the upper right. Needles have a cylindrical-like morphol- magnetic simulations of these morphologies indicate that they ogy (Inset in Right) and some taper toward one end of the crystal.

4of7 | PNAS Wagner et al. https://doi.org/10.1073/pnas.2018169118 In situ magnetic identification of giant, needle-shaped magnetofossils in Paleocene–Eocene Thermal Maximum sediments Downloaded by guest on September 25, 2021 Since fcr depends on fewer magnetic processes, it contains a single particle, or groups of particles with collective behavior coercivity components with smaller dispersion parameters. This (such as magnetosome chains), switching at Bc. effect helps distinguish individual coercivity components and is A small but significant central ridge offset (0.4 to 0.7 mT) is clearly visible in BAL13 (Fig. 1B): the biogenic soft and biogenic visible in both samples after careful isolation of the central ridge hard coercivity components, originally identified with ARM de- from the remaining FORC contributions using VARIFORC E SI Ap- magnetization curves (21), are clearly recognizable in fcr but are (VARIable FORC) processing (51) (Fig. 1 ; see also pendix – less evident in fdc and firr due to their strong overlap in those , Text S1.2 S1.5). The initial offset decrease originates coercivity measurements. The maximum coercivity range of the from viscous single-domain particles via the direct relationship two conventional magnetofossil components reaches ∼120 mT, between switching field and particle volume. Viscous particles, f which is also the upper limit for single-domain coherent rotation such as isolated immature magnetofossils, contribute to cr at the B → signatures in the lower half of the FORC diagram (Fig. 1D). In c 0 limit, before the onset of the biogenic soft component at contrast, the coercivity range of contributions in the upper half of ∼10 mT (21). The relatively constant offset over the coercivity the FORC diagram, which are caused by flux closure annihila- range of conventional magnetofossils is also observed in the tion, is limited mostly to 80 mT (Fig. 1D). FORC distribution for BAL13. This is consistent with a common The same biogenic components are identified in the central origin of the biogenic soft and biogenic hard components in the ridge distribution for WL35950b. However, in this case an ad- two samples. TEM results (SI Appendix, Table S1) further sug- ditional, higher-coercivity contribution dominates the 120 to 210 gest that conventional magnetofossils observed in magnetic ex- mT range (Fig. 1A). We attribute this higher-coercivity contri- tracts from WL-A can be categorized into biogenic soft or bution to the needles observed with TEM (Fig. 4) rather than biogenic hard based on relative shape anisotropy and probable other giant magnetofossil morphologies, like bullets and spin- chain structure. The maximum central ridge offset occurs in the dles, which likely exhibit vorticity and fanning/curling (thus lower coercivity range of the biogenic needle component, which is at- coercivities) (11) because of their large widths. The high- tributed to single-domain particles with a smaller activation coercivity contribution to the central ridge is not unique to volume than that of conventional magnetofossil chains. Identi- needles: it also has been observed in some igneous rocks (45) and fication of these central ridge offset signatures depends largely in sediments with silicate minerals that contain inclusions of fine- on the tight field control used for FORC measurements and enhanced signal-to-noise ratio obtained by stacking multiple sets grained single-domain magnetite (46). We note that TEM ob- Materials and Methods servations and the sedimentology of WL-A sediments (5) indi- of curves (see details in ). cate that these alternative sources do not contribute to the

Implications for Studying Hyperthermal Events. With validation by EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES magnetic signal in our specimens. Micromagnetic simulations of micromagnetic modeling and TEM imaging of magnetic extracts, conventional magnetosome chains show that some chain con- we present unequivocal identification of giant, needle-shaped figurations (i.e., >10 magnetosomes or with interparticle spac- ∼ ∼ magnetofossils derived from central ridge characteristics of ings 1 nm) may have coercivity tails that reach 180 mT (19, FORC diagrams. This confirms that the CIE magnetic en- 47), but these contributions are smaller than those of the needles hancement is caused predominately by conventional and giant described here. The uniaxial single-domain nature of this needle magnetofossils. Our FORC measurement protocol is optimized component is also identified in the FORC diagram by the larger for rigorous quantification of the vertical offset of the central field range of coherent single-domain rotation contributions ridge associated with the needle component. The needle com- (lower half plane) and by a small contribution (upper half plane) ponent, and potentially other magnetofossil signatures, is also C caused by flux closure annihilation (Fig. 1 ). A minor fraction of identified, albeit more ambiguously, using lower-resolution FORC the needles must therefore be sufficiently large to nucleate diagrams. Together, these data indicate that the magnetic signa- magnetic vortices during FORC measurements, such as the tures described here are those of in situ magnetic particles, not a 150-nm-wide needle of the micromagnetic simulation shown in subset of particles removed from their taphonomic context via SI Appendix , Fig. S5. artificial sorting and reorganization by magnetic extraction. In situ identification of central ridge components with coercivity Central Ridge Offset as a Distinct Signature of Biogenic Needles. The peaks >20 mT and small fluctuation fields ≪Bc, indicates abun- central ridge offset provides insight into the physical nature of dant single-domain particles, or chains of such particles, with the magnetic components biogenic soft, biogenic hard, and bio- strong uniaxial anisotropies compatible with those of conventional F genic needle (Fig. 1 ). The small vertical offset of the central magnetofossils and giant needles. The central ridge contributes to ridge is related to the measurement timing asymmetry of the ∼40% of the saturation remanent magnetization (Mrs). This is also FORC protocol: decreasing the applied field from positive sat- the lower limit for the total magnetofossil contribution, which is B uration to a negative reversal field r switches all single-domain significantly higher than the ∼10% estimated by Wang et al. (18). ≤−B particles with switching fields r, and these particles are The magnetization carried by magnetofossils is much larger if the B = −B switched back to positive saturation near r. Thermally FORC contributions above and below the central ridge, associated B activated switching occurs during the pause at r and during with transitions from single-domain–like to flux-closure magnetic B ∼−B B measurement at r. More time is effectively spent at r states and vice versa, are considered. As shown with selective −B B = −B than near r, which requires a slightly larger field r + chemical extraction of a magnetofossil-rich sediment, the central ΔB ΔB fluc to switch all particles back to positive saturation. fluc is ridge contributes to ∼65% of the Mrs carried by <0.3 μmmag- the difference between fluctuation fields for thermally assisted netite particles (24, 52). Using this estimate, the magnetofossil ±B switching at r (34, 48). contribution to the M of WL35950b increases to ∼66%. The ΔB rs The central ridge offset corresponds exactly to fluc and presence of nonbiogenic, isolated single-domain equidimensional depends on the amplitude of the energy barrier of single-domain or irregular magnetite particles of the type attributed to an impact particles in proximity of the switching field, with ΔBfluc → 0as (15) cannot be excluded. However, their contribution, if present, the energy barrier grows to infinity. For single-domain particles must be minor, given the absence of a coercivity peak at Bc = switching by coherent rotation, this energy barrier is proportional 0 and the viscous signatures that unavoidably occur with single- to particle volume (49). The energy barrier continues to increase domain magnetite particles lacking uniaxial anisotropy and bio- with volume in single vortex particles (50), an effect which can logical size control (52–54). also contribute to the central ridge signal. The central ridge Giant needles have so far only been found in sediments deposited offset at Bc is thus a measure of the thermal activation volume of during hyperthermal events, and they are often accompanied by

Wagner et al. PNAS | 5of7 In situ magnetic identification of giant, needle-shaped magnetofossils in Paleocene–Eo- https://doi.org/10.1073/pnas.2018169118 cene Thermal Maximum sediments Downloaded by guest on September 25, 2021 other giant magnetofossil morphologies (e.g., spearheads, spindles, averaging (ImportFORC), smoothing (CalculateFORC), and central ridge and bullets) (6, 7, 11, 14). Although the physiology and ecology of processing (IsolateCR) through VARIFORC (51). For full details on the mea- the organisms that biomineralize giant needles is unknown, the surement protocol, see SI Appendix, Text S1.2–1.5 and Figs. S6–S8.The association of these magnetofossils with the onset of rapid and large signal-to-noise ratio of processed data for WL35950b in correspondence of changes in the temperature and chemistry of marine environments the central ridge is 100 to 150 over the coercivity range covered by conventional magnetofossils; it is 60 to 100 over the coercivity range of giant suggeststheycouldbeusedtoefficiently identify environmental needles, which ensures sufficiently precise quantification of the vertical perturbations. The capability of detecting giant, needle-shaped central ridge offset. This is a FORC protocol designed specifically to charac- magnetofossils using robust, nondestructive magnetic measure- terize the distinct FORC signatures associated with the needle component. ments on bulk sediment samples, in contrast to magnetic separates, Although the resulting data are nosier, this component is also identified in is promising for scientists studying global change events. The ability lower-resolution FORC datasets that only require ∼10 h per measurement (SI to rapidly find giant magnetofossil assemblages in the geologic Appendix, Text S4 and Fig. S1). record will help identify the origin of these unusual magnetofossils and the specific ecology of the organisms that biomineralized Micromagnetic Modeling. Micromagnetic simulations for giant needle-shaped them. The needle component may help identify intervals of sub- magnetofossils were performed using MERRILL (Micromagnetic Earth Re- stantial environmental change that are more subtly expressed by lated Robust Interpreted Language Laboratory), a micromagnetics package other microorganisms and geochemical proxies. Moreover, giant optimized for rock magnetism (55). We used the default settings for mag- magnetofossils appear to be linked to oceanic deoxygenation netite at room temperature, which include magnetocrystalline anisotropy with the easy axis along the 〈111〉 crystallographic direction. Particle elon- stimulated by rapid planetary change, particularly warming events. gation was set along the 〈001〉 direction (z in our coordinate system). Shape By studying the occurrence of giant magnetofossils we can better estimates and constraints were determined from TEM images of giant understand how sensitive marine ecosystems responded to past needles and from our high-resolution FORC measurements. We performed climate change events. simulations for the following needle widths: 21, 25, 50, 100, and 150 nm. Needle length was 1,000 nm, except for the 150-nm-wide particle, which had Materials and Methods a length of 500 nm. Volumetric meshes with unit cell sizes of 5 nm were Sample Preparation for FORC Measurements. We prepared a dry, powdered generated using MEshRRILL (https://bitbucket.org/poconbhui/meshrrill/). The sediment chip (∼0.116 g) from the WL-A core (WL35950b). This specimen is three widest particle sizes were used to model the giant needle-shaped from the CIE onset interval of the PETM. Although our measurements were magnetofossils observed in extracts from WL35900 and WL35800. The two performed on disaggregated sediment, we consider the measurements narrower particle sizes were used to model giant needle-shaped magneto- in situ: we did not apply any magnetic extraction, and we have not disrupted fossils inferred from the high-resolution FORC measurements of specimen the submicron arrangement of particles at a scale relevant to magnetostatic WL35950b. Hysteresis loops were simulated in 10° increments between the z interactions. The vertical offset of the central ridge, which we conclude is a direction (parallel to elongation) and the x direction (perpendicular to characteristic of biogenic needles, is also visible in FORC diagrams of intact, elongation) for the 21-, 25-, and 50-nm needles. Loops were simulated in the unpowdered bulk sediment chips (SI Appendix, Fig. S1), despite the fact that same orientations for the 100-nm needle but in 15° increments. Only one this measurement has a lower signal-to-noise ratio than those completed on loop was simulated for the 150-nm needle, with the field along the z di- the powdered sample. Future experiments will help identify the optimal rection. Saturating fields were chosen between 100 and 500 mT, depending measurement routine to resolve the vertical offset with confidence while on grain size and orientation. The upper hysteresis loop branch was also minimizing user and instrument time. A freeze-dried sediment sample obtained at 5-mT field steps, and the lower branch was calculated by from Lake Baldeggersee (BAL13) (22) is included for comparison. This sample inverting the upper branch. corresponds to a depth interval of 13 to 14 cm in the gravity core described by Egli (22) and is characterized by approximately equal contributions of TEM. We used average magnetofossil lengths and widths of particles imaged biogenic soft, biogenic hard, and a low-coercivity detrital component. Both using TEM of magnetic extracts (Table S1) for dimensional analyses. TEM was specimens were secured inside gelatin capsules and then affixed to a vi- performed on the TECNAI TF30 scanning/TEM at John Hopkins University, in brating sample magnetometer (VSM) probe for high-resolution FORC mea- the Materials Characterization and Processing Facility, using an accelerating surements. voltage of 300 keV. Particles were measured using Gatan’s GMS 3 Digital Micrograph Software. Dimensional analyses predict the magnetic domain High-Resolution FORCs. Specimens WL35950b and BAL13 were measured state of the magnetofossils identified from magnetic extracts from the CIE using a specialized, high-resolution, low-noise FORC measurement protocol onset interval at WL-A, WL35900, and WL35800. We plotted magnetofossil with improved field precision to extract the thermal activation signature of length against the width/length of magnetofossils with the theoretical grain single-domain particles contributing to the central ridge. The Lake Shore size limits for individual particles of magnetite and chains of interacting 8600 VSM used for these measurements provides excellent field control magnetofossils from Butler and Banerjee (39), Muxworthy and Williams (40), characteristics and the possibility of zeroing the Hall probe and monitoring and Newell (41). the applied field at a 100-Hz rate. The typical reversal field overshoot <0.2 mT of the regular FORC protocol can be further decreased by a stepwise Data Availability. AVI, FRC, and PDF data have been deposited in Figshare approach to Br in which the field is ramped from saturation to Br + kΔB, where ΔB is the field step used for FORC measurements, and k ≥ 1isthe (https://doi.org/10.6084/m9.figshare.13182848). All other study data are in- number of approach steps. In this manner, field overshooting problems are cluded in the article and supporting information. eliminated. The following protocol was used for the FORC measurements of

WL35950b: Bsat = 500 mT, Bc,max = 250 mT, Bu,min = −10.2 mT, Bu,max = +80.2 ACKNOWLEDGMENTS. This research used samples collected by the U.S. Geological Survey, in part collected by P.C.L. and provided by Jim Zachos mT, ΔB = 0.4 mT, k = 3, pause at Br = 3 s. Measurements were performed in point-by-point mode (the field was stabilized for 0.1 s before a measure- (University of California, Santa Cruz) and Ellen Thomas (Yale University). ment is taken) with averaging time = 0.15 s. BAL13 was measured with the Financial support was provided by the Robert Hevey and Constance M. Filling Fellowship at the Smithsonian Institution, the N. Gary Lane Student Research same protocol, except for limiting B to 160 mT due to the lack of high- c,max Award through the Paleontological Society, an Evolving Earth Foundation coercivity components. The maximum Hall probe bias during measurements Research Grant, a P.E.O. Scholar Award, and a Schlanger Ocean Drilling μ at constant laboratory temperature was 10 T. Signal-to-noise ratios well Fellowship (all to C.L.W.). I.L. is grateful for a Smithsonian Institution above the standard of regular FORC measurements were attained by Edward and Helen Hintz Secretarial Scholarship and a National Museum of stacking 32 sets of measurements for WL35950b and 13 sets of measure- Natural History Research Grant. We thank the two reviewers for their helpful ments for BAL13. These data were processed using optimal measurement comments, which strengthened our final manuscript.

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