Phosphate biomineralization in mid-Neoproterozoic protists Phoebe A. Cohen1*, J. William Schopf2,4, Nicholas J. Butterfi eld3, Anatoliy B. Kudryavtsev4, and Francis A. Macdonald1 1Department of Earth and Planetary Sciences, Harvard University, Cambridge, Massachusetts 02138, USA 2Department of Earth and Space Sciences, and Molecular Biology Institute, University of California–Los Angeles, Los Angeles, California 90095, USA 3Department of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, UK 4Institute of Geophysics and Planetary Physics (Center for the Study of Evolution and the Origin of Life), University of California– Los Angeles, Los Angeles, California 90095, USA, and National Aeronautics and Space Administration Astrobiology Institute, Pennsylvania State University Astrobiology Research Center, University Park, Pennsylvania 16802, USA ABSTRACT teenmile Group (formerly lower Tindir Group) The origin and expansion of biomineralization in eukaryotes played a critical role in Earth (Macdonald et al., 2010a, 2011). The age of history, linking biological and geochemical processes. However, the onset of this phenome- the fossiliferous upper carbonate unit of the non is poorly constrained due to a limited early fossil record of biomineralization. Although Fifteenmile Group is determined as between macroscopic evidence for biomineralization is not known until the late Ediacaran, we here 811.5 ± 0.2 Ma and 717.4 ± 0.1 Ma by U-Pb report biologically controlled phosphatic biomineralization of scale microfossils from mid- isotope dilution–thermal ionization mass spec- Neoproterozoic (pre-Sturtian) strata of northwest Canada. Primary biological control on trometry ages on zircons from volcanic hori- mineralization is supported by the identifi cation of apatite in both chert-hosted and lime- zons in sections ~75 km to the east of Mount stone-hosted specimens, the conspicuously rigid original morphology of the scale microfossils Slipper (Macdonald et al., 2010b). relative to co-occurring organic-walled cyanobacteria and acritarchs, and the microstruc- ture of the constituent phosphate. Cell-enveloping mineralized scales occur in a wide range MATERIAL AND METHODS of extant protists, but the apparent restriction of phosphate scales to one modern taxon of Chert thin sections were prepared at thick- green algae suggests a possible affi liation for these fossils. Documentation of primary phos- nesses of 60 or 100 µm for light microscopy, phate biomineralization in Fifteenmile Group (Yukon Territory, Canada) microfossils greatly confocal laser scanning microscopy (CLSM), extends the known record of biologically controlled mineralization and provides a unique and Raman and fl uorescence spectroscopy. In window into the diversity of early eukaryotes. addition to the fossils present in black chert nodules (Macdonald et al., 2010a), we also dis- INTRODUCTION a mid-Neoproterozoic (717–812 Ma) depo- covered abundant specimens preserved in three- Biomineralization plays a critical role in sitional age for scale-bearing horizons of the dimensional submicron-scale detail in acid- understanding evolutionary history, as organ- Fifteenmile Group (Macdonald et al., 2010a, resistant residues of the associated limestone. isms that form mineralized components become 2010b, 2011). Here we present new data from Limestone hand samples were broken into fossilized much more commonly than those that analyses by Raman and fl uorescence spectros- ~2 cm3 pieces and dissolved in 30% acetic acid; do not; biomineralizing eukaryotes also play a copy and energy dispersive X-ray spectroscopy the resulting macerates were fi ltered through a major role in biogeochemical cycles. Although (EDS) that show the scales to be composed of 30 µm mesh, dry mounted on copper tape, and the fi rst conspicuous records of biologically calcium phosphate produced through biologi- coated with Pt/Pd or Au for study by scanning controlled mineralization are found in multicel- cally controlled mineralization. electron microscopy (SEM), focused ion beam lular fossils from the late Ediacaran (Germs, (FIB)-SEM, and EDS (for additional informa- 1972; Grotzinger et al., 2000), it is not until the GEOLOGIC SETTING tion, see the Data Repository). Mesozoic and Cenozoic that unicellular organ- Fossiliferous samples were collected from isms adopted a comparable level of biominer- outcrops of the Fifteenmile Group from Mount MORPHOLOGY AND COMPOSITION alization, potentially in response to escalated Slipper (Yukon, Canada, N65°16′, W140°57′), Diverse scale microfossils were identifi ed in ecological pressures (Hamm et al., 2003). Even exposed on the west limb of a broad anti- both chert and limestone lithologies. Three of so, phylogenetic and molecular clock analy- cline that straddles the Yukon-Alaska border. the most common morphotypes are illustrated ses (e.g., Sperling et al., 2010), combined with Microfossils were recovered from organic- here: (1) imperforate circular scales 14–27 µm variably problematic paleontological reports rich, chert-bearing limestone micrite that was in diameter (Archeoxybaphon; Figs. 1H and 1I); (Horodyski and Mankiewicz, 1990; Porter et deposited below fairweather wave base (Mac- (2) ovoid scales 30–45 µm in diameter having al., 2003), point to a signifi cant pre-Ediacaran donald et al., 2010a) (Fig. DR1 in the GSA regularly perforated concave sidewalls (Bicor- record of biologically controlled mineralization. Data Repository1). Although these exposures niculum; Figs. 1E–1G); and (3) ovoid perfo- Diverse scale-like microfossils from the Fifteen- were originally assigned to the upper Tindir rated shield-like scales 26–52 µm in diameter, mile Group (Yukon Territory, Canada; formerly Group and interpreted variously as late Cryo- composed of a hexagonal network of struts, the Tindir Group; Macdonald et al., 2011) have genian to early Cambrian in age (Allison and from one surface of which arises a central shaft often been noted as instances of early biomin- Awramik, 1989; Kaufman et al., 1992), recent that terminates in a four- or six-pronged struc- eralization, most likely utilizing silica (Allison mapping and chemostratigraphic analyses have ture (Characodictyon; Figs. 1A–1D). CLSM and Hilgert, 1986; Knoll, 2003), though neither reassigned the fossiliferous strata to the Fif- and SEM of Characodictyon show these scales their age nor original composition was reliably to be 1–2 µm thick with the hexagonal lattice- constrained. Recent work has now confi rmed 1GSA Data Repository item 2011174, Fig- work defi ning 0.5–1.5-µm-diameter perfora- ures DR1−DR7 and extended Materials and Meth- tions (Fig. 1D). On the shaft-bearing surface, ods, is available online at www.geosociety.org/pubs/ *Current address: NASA Astrobiology Institute, ft2011.htm, or on request from editing@geosociety 1–2-µm-long rigid, regularly oriented spines Massachusetts Institute of Technology, Cambridge, .org or Documents Secretary, GSA, P.O. Box 9140, protrude from the intersecting nodes of the lat- Massachusetts 02139, USA; E-mail: [email protected]. Boulder, CO 80301, USA. ticework (Fig. DR2A in the Data Repository), © 2011 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or [email protected]. GEOLOGY,Geology, June June 2011; 2011 v. 39; no. 6; p. 539–542; doi:10.1130/G31833.1; 3 fi gures; Data Repository item 2011174. 539 Figure 1. Optical, confo- cal laser scanning mi- croscopy (CLSM), and scanning electron mi- croscopy (SEM) images of Tindir scale fossils. A: SEM image of Chara- codictyon. B: SEM image of shield-fringing spines and fi brous microstruc- ture of Characodictyon. C: CLSM image of Chara- codictyon. D: Photomi- crograph of Characodic- tyon. E: Photomicrograph of Bicorniculum. F: CLSM image of Bicorniculum. G: SEM image of Bicor- niculum. H: SEM image of Archaeoxybaphon sp. I: SEM image of Archae- oxybaphon showing pe- ripheral triangular teeth. Scale bar represents 5 µm in A, 2 µm in B, 15 µm in C and D, 12 μm in E and F, 8 µm in G, 10 µm in H, and 3 µm in I. whereas similar spines fringe the shield perim- counterparts, indicating that the fossils were not the preservation of more recalcitrant features, eter (Figs. 1A and 1B). A similarly fringing originally biomineralized silica. The Sm+3 sig- including the cell walls of Ediacaran acritarchs array of triangular tooth-like structures, lying nal in the fl uorescence spectra of chert-hosted and cuticles of Cambrian ecdysozoans, but fl at against the scale surface, is present in Arche- scales derives from Sm replacement of Ca-1 these fossils all exhibit evidence of original oxybaphon (Figs. 1H and 1I). The narrow spines ions in the apatite, a characteristic of substitu- plastic deformation and secondary encrusta- of Characodictyon and the tooth-like structures tion under anoxic conditions (Gaft et al., 2001). tion. Paleozoic “mazuelloid” acritarchs display of Archeoxybaphon have been observed only by These analyses show that the scale microfos- a somewhat similar style of deformation, and SEM in acid-isolated specimens. In addition to sils are consistently composed of apatite and combined with the presence of discrete car- these primary biological features, some speci- organic carbon, in both host-rock lithologies. bonaceous walls composed of zoned arrays of mens of Characodictyon exhibit a microfabric perpendicularly oriented crystallites, indicate a of oriented crystallites parallel to the latticework ORIGINAL COMPOSITION diagenetic origin of phosphate (Kremer, 2005). construction (Figs. 1B; Fig. DR2).