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A New Approach in Deciphering Early Protist Paleobiology and Evolution: Combined Microscopy and Microchemistry of Single Proterozoic Acritarchs ⁎ E.J

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A New Approach in Deciphering Early Protist Paleobiology and Evolution: Combined Microscopy and Microchemistry of Single Proterozoic Acritarchs ⁎ E.J Review of Palaeobotany and Palynology 139 (2006) 1–15 www.elsevier.com/locate/revpalbo A new approach in deciphering early protist paleobiology and evolution: Combined microscopy and microchemistry of single Proterozoic acritarchs ⁎ E.J. Javaux a, , C.P. Marshal b a Department of Geology, Geophysics, Oceanography, University of Liège, 4000 Liège Sart-Tilman, Belgium b Australian Centre for Astrobiology, Macquarie University, NSW 2109 Sydney, Australia Available online 3 March 2006 Abstract Beside a few cases, the biological affinities of Proterozoic and Paleozoic acritarchs remain, by definition, largely unknown. However, these fossils record crucial steps in the early evolution of microorganisms and diversification of complex ecosystems. We present how combining microscopy (light microscopy, scanning and transmitted electron microscopy) with microchemical analyses of individual microfossils may offer further insights into the paleobiology and evolution of early microorganisms. We use our ongoing work on early Mesoproterozoic and Neoproterozoic assemblages, as well as other published work, as examples to illustrate how this approach may clarify the evolution of early microorganisms and we underline how useful this approach could be for palynologists working on younger material. Such a multidisciplinary approach offers new possibilities to investigate the biological affinities of acritarchs and the record of early life on Earth and beyond. © 2006 Elsevier B.V. All rights reserved. Keywords: acritarchs; biological affinities; microscopy; microchemistry; Proterozoic; Paleozoic 1. Introduction acritarchs record crucial steps in the early evolution and diversification of the biosphere. Identifying the Acritarchs are organic-walled microfossils of un- biological affinities of these microscopic organisms will known biological affinities. They are conventionally clarify Proterozoic and Paleozoic microbial paleobiol- interpreted as algal cysts but most probably include a ogy and food webs (see Butterfield, 1997, 2000 for larger range of organisms such as prokaryotic sheaths, discussions on plankton food webs and ecological heterotroph protists or even parts of multicellular beings tiering in the late Proterozoic). It will also contribute (Van Waveren, 1992; Martin, 1993; Colbath and to phylogenetic reconstructions and improve our Grenfell, 1995; Butterfield, 2005). Biologists easily understanding of early evolutionary mechanisms and differentiate between prokaryotic and eukaryotic organ- patterns, and the early interactions between environment isms using molecular and cell biology, but these and life. characters rarely survive fossilization and so are not Comparative biology is useful when organisms generally available to the paleontologist. However, display characteristic morphological attributes, but this rarely occurs among acritarchs (for example early ⁎ Corresponding author. Fax: +32 4 366 2921. dinoflagellates might not show tabulation). Most acri- E-mail address: [email protected] (E.J. Javaux). tarchs have relatively simple morphologies; basically a 0034-6667/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.revpalbo.2006.01.005 2 E.J. Javaux, C.P. Marshal / Review of Palaeobotany and Palynology 139 (2006) 1–15 microscopic organic ball or tube (often flattened to single or very few microfossils allows characteriza- when preserved in shales) with or without various tion of the fine ultrastructure and microchemistry of the ornaments, that make comparison with recent clades material studied. In some cases, it is possible to relate difficult. New approaches are necessary to elucidate these with similar known features of recent organisms their paleobiology. and clarify the paleobiology of the fossils. Ideally, this Study of the wall ultrastructure can differentiate approach should be conducted within a good geological between prokaryotic and eukaryotic acid-resistant framework, in well-dated successions, with detailed microfossils and, in some cases, even identify particular sedimentological reconstruction of paleoenvironments. clades (review in Javaux et al., 2003, 2004a). Combin- This paper focus on techniques that can be applied to ing microscopy (light microscopy, scanning and trans- isolated acid-resistant organic-walled microfossils mitted electron microscopy) with microchemical extracted from shales, in order to characterize their analyses of individual microfossils offers further morphology, wall ultrastructure and chemistry and to insights into the paleobiology and evolution of early reconstruct their paleobiology (Table 1). Other techni- microorganisms. A combination of techniques applied ques (briefly mentioned in the text) can be used for visualizing microfossils still embedded in a mineral matrix (and too fragile to withstand extraction) and for Table 1 characterizing their elemental composition and their Summary of techniques that can be applied on single acritarchs distribution in the rock, and the biological–mineral extracted from shales by acid-maceration and possible paleobiological information interactions. Techniques Data Paleobiological information 2. Materials Transmitted Morphology Assemblage diversity light (ornamentation, color, microscopy branching, etc.) Most of the fossils used as examples here come from No. of specimens Characteristic morphology carbonaceous shales of the early Mesoproterozoic Roper No. of species Cell division patterns Group, northern Australia (Fig. 1). The sedimentary Reproduction mode architecture of the Roper Basin is well characterized Wall thickness, flexibility (Abbott and Sweet, 2000). The shales preserve abundant Taphonomy Multicellularity and exquisite organic-walled microfossils distributed in Biological affinities in assemblages showing an onshore–offshore pattern of some cases decreasing abundance, declining diversity and changing Scanning Detailed outer and Wall ornamentation and dominance (Javaux et al., 2001). U–Pb SHRIMP electron inner wall features structure sometimes analyses of zircons from an ash bed in the Mainoru microscope indicative of eukaryotc complexity Formation fix an age of 1492±3 Ma for early Roper Wall thickness deposition (Page et al., 2000). A 1429±31 Ma Rb–Sr Transmission Wall ultrastructure Biological affinities at age for illite in dolomitic siltstones near the top of the electron level of kingdom, succession is consistent with the zircon age, even if less microscopy class in some cases reliable (Kralik, 1982). Highly carbonaceous shales in Fluorescence Fluorescence of Linked to wall chemistry, confocal wall polymers applicable on very basinal deposits of the Velkerri Formation, near the top microscopy immature material of the Roper Group, also contain low abundances of EDEX Elemental Details on steranes sourced by eukaryotic organisms (Summons et composition preservation mode, al., 1988). The Roper microfossils have been variously FT-infrared Biopolymer Biological interpreted as the oldest unambiguous evidence for spectrometry composition affinities in some cases eukaryotes (Javaux et al., 2001, 2003), as complex FT-Raman Aromaticity and To use in prokaryotes (Cavalier-Smith, 2002) and as fungi spectrometry thermal maturity of combination with (Butterfield, 2005). Their exquisite preservation and organic matter FTIR for further their age makes them ideally suited for paleobiological characterization investigations. of wall chemistry Pyrolysis Biomarker Biological affinities One highly ornamented fossil also treated here, GC/MS composition in some cases Shuiyousphaeridium macroreticulatum, comes from SIMS C isotopes Metabolism in some shales of the top of the Ruyang Group, northern China cases, in combination (Yin, 1998). Ruyang deposition is not well constrained with morphology by radiometric dates, but appears to be at least broadly E.J. Javaux, C.P. Marshal / Review of Palaeobotany and Palynology 139 (2006) 1–15 3 2.1. Characterization of acritarch morphology and ultrastructure 2.1.1. Light microscopy Light microscopy is routinely used to examine the morphology of the fossils mounted on glass slides with transmitted light, as well as for determining the diversity of assemblages. In some cases, comparative morphology with extant groups might reveal a division or reproduction pattern or other morpholog- ical feature (for example, tabulation in dinoflagellates) unique to certain biological groups, therefore permit- ting the phylogenetic positioning of the specimens. Butterfield (2000) compared the division patterns of cells in various groups of algae and bacteria and concluded to a bangiophyte affiliation for a population of 1.2–1 Ga (gigayear-old) fossil preserved in cherts of the Hunting Formation, arctic Canada. This careful study identified the earliest eukaryote so far that can be related to an extant lineage. This approach has also been very successful in other cases, identifying cyanobacteria genera ranging from the Proterozoic to now (Knoll and Golubic, 1992). Examination of a large population of well-preserved specimens from a single bedding plane might also permit to unify seemingly unicellular disparate forms into a multicel- Fig. 1. Location and generalized stratigraphy of the Roper Group, northern Australia, showing stratigraphic distribution of facies and lular organism (for example, a diverse Neoproterozoic microfossils. Modified from Javaux et al. (2001). assemblage has been shown to be the disarticulated remains of a single vaucheriacean metaphyte, Butter- field, 2004). coeval with Roper sedimentation.
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