539-542_geoy3906_cohen.indd

ABSTRACT The origin and expansion of biomineralization in eukaryotes played a critical role in Earth history, linking biological and geochemical processes. However, the onset of this phenomenon is poorly constrained due to a limited early fossil record of biomineralization. Although macroscopic evidence for biomineralization is not known until the late Ediacaran, we here report biologically controlled phosphatic biomineralization of scale microfossils from midNeoproterozoic (pre-Sturtian) strata of northwest Canada. Primary biological control on mineralization is supported by the identifi cation of apatite in both chert-hosted and limestone-hosted specimens, the conspicuously rigid original morphology of the scale microfossils relative to co-occurring organic-walled cyanobacteria and acritarchs, and the microstructure of the constituent phosphate. Cell-enveloping mineralized scales occur in a wide range of extant protists, but the apparent restriction of phosphate scales to one modern taxon of green algae suggests a possible affi liation for these fossils. Documentation of primary phosphate biomineralization in Fifteenmile Group (Yukon Territory, Canada) microfossils greatly extends the known record of biologically controlled mineralization and provides a unique window into the diversity of early eukaryotes. Raman and fl uorescence spectroscopic analyses reveal the presence of morphology-defi ning apatite (shown in fl uorescence spectra to contain minor concentrations of Sm +3 ) and kerogen, surrounded by the permineralizing quartz of the chert matrix ( ORIGINAL COMPOSITION The consistently undistorted morphology of the scale microfossils in both chert and limestone combined with the intact, fully threedimensional specimens recovered from compacted limestone point to an original rigidity that is typically associated with biomineralization. Even the delicate marginal spines of specimens isolated from the limestone show no deformation. By contrast, the walls of co-occurring organic-walled acritarchs, coccoids, and cellular fi laments in silicifi ed samples were originally pliable, as evidenced by their deformation during early, precompactional, diagenesis. Despite such arguments, any defi nitive identifi cation of biomineralization must rule out the possibility of secondary, early diagenetic mineralization. Phosphate replacement is common throughout the fossil record, including instances of precompactional soft tissue phosphatization. None of these, however, is comparable to the preservation of Fifteenmile Group scales. In the best known examples, i.e., apatite-permineralized Ediacaran embryos, middle Cambrian mid-gut glands, and Cretaceous muscle, there is a clear histological selectivity to mineralization, with early phosphate preferentially replacing only the most labile cellular tissues The presence of nanometer-scale crystallites in some specimens of Characodictyon The fossiliferous lithologies of the Fifteenmile Group show no evidence of background GEOLOGY, June 2011 541 phosphogenesis or phosphatic overgrowths, as would be expected in sediments hosting phosphate-replaced fossils. Taken together, the chemical, textural, and distributional expression of the scales indicate primary biologically controlled calcium phosphate biomineralization. TAXONOMIC AFFINITY Taxonomic assignment of the Fifteenmile Group scale microfossils has been frustrated by the disparate range of extant protists that develop comparable armatures of scale-like plates, including prasinophytes, chrysophytes, Raphidiophrys (members of the centrohelid heliozoans), haptophytes, ciliates, and testate amoebae The use of phosphate in cell-enveloping scales is much less common among extant unicellular eukaryotes than that of other biominerals such as silica and calcium carbonate DISCUSSION The data presented here indicate that the Fifteenmile Group scale microfossils represent the earliest compelling evidence of biologically controlled eukaryotic biomineralization known in the fossil record. Although two other records of comparable age Like their modern analogs, the Fifteenmile Group scales were likely formed intracellularly in specialized endomembrane-derived vesicles and then extruded to the surface of the cell The approach of isolating mineralic microfossils from limestone using weak acid maceration has rarely been applied to the Precambrian in the search for such small-sized objects as the Fifteenmile Group scale microfossils. The success of this technique illustrated here and the new search image provided by the scale microfossils' phosphatic composition provides a promising new approach to studies of the Precambrian fossil record. CONCLUSION Our evidence of biologically controlled mineralization in a putative green alga indicates that a capacity for biologically controlled biomineralization existed among eukaryotes relatively early in the Neoproterozoic, but suggests that the selective pressures necessary for its widespread development were not met until the Phanerozoic. In addition, the calcium phosphate composition of the scale microfossils indicates that some early biomineralizing protists did not utilize the mineralogies dominant in their modern analogs, a fi nding consistent with the wide variation in biominerals found across the eukaryotic tree. Continued work on the Precambrian fossil record, further research on the selective pressures leading to biomineralization in modern protists, and more refi ned reconstructions of Neoproterozoic ecosystems will be required to fully understand the biology of these intricate biomineralized fossils. ACKNOWLEDGMENTS We thank A. Knoll, G. Walker, D. Johnston, S. Porter, S. Xiao, C. Marshall, N. Tosca, J. Creveling, B. Kotrc, and B. Gill for helpful discussions and comments on earlier drafts; J. Schiffbauer and two anonymous reviewers provided constructive comments. Scanning electron microscope and energy-dispersive X-ray spectroscopy studies were carried out at the Harvard Center for Nanoscale Systems. Raman and confocal laser scanning microscopy studies were carried out at the University of California-Los Angeles Center for the Study of Evolution and the Origin of Life (CSEOL)