Emmanuelle Javaux

Eukaryotic organisms in Proterozoic oceans

The geological record of protists begins well before the Ediacaran and Cambrian diversification of animals, but the antiquity of that history, its reliability as a chronicle of evolution and the causal inferences that can be drawn from it remain subjects of debate. Well-preserved protists are known from a relatively small number of Proterozoic formations, but taphonomic considerations suggest that they capture at least broad aspects of early eukaryotic evolution. A modest diversity of problematic, possibly stem group protists occurs in ca 1800–1300 Myr old rocks. 1300–720 Myr fossils document the divergence of major eukaryotic clades, but only with the Ediacaran–Cambrian radiation of animals did diversity increase within most clades with fossilizable members. While taxonomic placement of many Proterozoic eukaryotes may be arguable, the presence of characters used for that placement is not. Focus on character evolution permits inferences about the innovations in cell biology and development that underpin the taxonomic and morphological diversification of eukaryotic organisms.

Morphological and ecological complexity in early eukaryotic ecosystems

Molecular phylogeny and biogeochemistry indicate that eukaryotes differentiated early in Earth history. Sequence comparisons of small-subunit ribosomal RNA genes suggest a deep evolutionary divergence of Eukarya and Archaea; C27–C29 steranes (derived from sterols synthesized by eukaryotes) and strong depletion of 13C (a biogeochemical signature of methanogenic Archaea) in 2,700 Myr old kerogens independently place a minimum age on this split. Steranes, large spheroidal microfossils, and rare macrofossils of possible eukaryotic origin occur in Palaeoproterozoic rocks. Until now, however, evidence for morphological and taxonomic diversification within the domain has generally been restricted to very late Mesoproterozoic and Neoproterozoic successions. Here we show that the cytoskeletal and ecological prerequisites for eukaryotic diversification were already established in eukaryotic microorganisms fossilized nearly 1,500 Myr ago in shales of the early Mesoproterozoic Roper Group in northern Australia.

Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits.

Although the notion of an early origin and diversification of life on Earth during the Archaean eon has received increasing support in geochemical, sedimentological and palaeontological evidence, ambiguities and controversies persist regarding the biogenicity and syngeneity of the record older than Late Archaean. Non-biological processes are known to produce morphologies similar to some microfossils, and hydrothermal fluids have the potential to produce abiotic organic compounds with depleted carbon isotope values, making it difficult to establish unambiguous traces of life. Here we report the discovery of a population of large (up to about 300 μm in diameter) carbonaceous spheroidal microstructures in Mesoarchaean shales and siltstones of the Moodies Group, South Africa, the Earth’s oldest siliciclastic alluvial to tidal-estuarine deposits. These microstructures are interpreted as organic-walled microfossils on the basis of petrographic and geochemical evidence for their endogenicity and syngeneity, their carbonaceous composition, cellular morphology and ultrastructure, occurrence in populations, taphonomic features of soft wall deformation, and the geological context plausible for life, as well as a lack of abiotic explanation falsifying a biological origin. These are the oldest and largest Archaean organic-walled spheroidal microfossils reported so far. Our observations suggest that relatively large microorganisms cohabited with earlier reported benthic microbial mats in the photic zone of marginal marine siliciclastic environments 3.2 billion years ago.

Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago

The evidence for macroscopic life during the Palaeoproterozoic era (2.5–1.6 Gyr ago) is controversial. Except for the nearly 2-Gyr–old coil-shaped fossil Grypania spiralis, which may have been eukaryotic, evidence for morphological and taxonomic biodiversification of macroorganisms only occurs towards the beginning of the Mesoproterozoic era (1.6–1.0 Gyr). Here we report the discovery of centimetre-sized structures from the 2.1-Gyr-old black shales of the Palaeoproterozoic Francevillian B Formation in Gabon, which we interpret as highly organized and spatially discrete populations of colonial organisms. The structures are up to 12 cm in size and have characteristic shapes, with a simple but distinct ground pattern of flexible sheets and, usually, a permeating radial fabric. Geochemical analyses suggest that the sediments were deposited under an oxygenated water column. Carbon and sulphur isotopic data indicate that the structures were distinct biogenic objects, fossilized by pyritization early in the formation of the rock. The growth patterns deduced from the fossil morphologies suggest that the organisms showed cell-to-cell signalling and coordinated responses, as is commonly associated with multicellular organization. The Gabon fossils, occurring after the 2.45–2.32-Gyr increase in atmospheric oxygen concentration, may be seen as ancient representatives of multicellular life, which expanded so rapidly 1.5 Gyr later, in the Cambrian explosion.

The Early Eukaryotic Fossil Record

The Precambrian era records the evolution of the domain Eucarya. Although the taxonomy of fossils is often impossible to resolve beyond the level of domain, their morphology and chemistry indicate the evolution of major biological innovations. The late Archean record for eukaryotes is limited to trace amounts of biomarkers. Morphological evidence appears in late Paleoproterozoic and early Mesoproterozoic (1800-1300 Ma) rocks. The moderate diversity of preservable eukaryotic organisms includes cell walls without surface ornament (but with complex ultrastructure), with regularly distributed surface ornamentation, and with irregularly or regularly arranged processes. Collectively, these fossils suggest that eukaryotes with flexible membranes and cytoskeletons existed in mid-Proterozoic oceans. The late Mesoproterozoic-early Neoproterozoic (1300-750 Ma) is a time of diversification and evolution when direct evidence for important biological innovations occurs in the fossil record such as multicellularity, sex, photosynthesis, biomineralization, predation, and heterotrophy. Members of extant clades can be recognized and include bangiophyte red algae, xanthophyte algae, cladophorale green algae, euglyphid, lobose, and filose amoebae and possible fungi. In the late Neoproterozoic, besides more diversification of ornamented fossils, florideophyte red algae and brown algae diversify, and animals take the stage. The record of biological innovations documented by the fossils shows that eukaryotes had evolved most cytological and molecular complexities very early in the Proterozoic but environmental conditions delayed their diversification within clades until oxygen level and predation pressure increased significantly.

Early evolution of large micro-organisms with cytological complexity revealed by microanalyses of 3.4 Ga organic-walled microfossils

The Strelley Pool Formation (SPF) is widely distributed in the East Pilbara Terrane (EPT) of the Pilbara Craton, Western Australia, and represents a Paleoarchean shallow-water to subaerial environment. It was deposited ~3.4 billion years ago and displays well-documented carbonate stromatolites. Diverse putative microfossils (SPF microfossils) were recently reported from several localities in the East Strelley, Panorama, Warralong, and Goldsworthy greenstone belts. Thus, the SPF provides unparalleled opportunities to gain insights into a shallow-water to subaerial ecosystem on the early Earth. Our new micro- to nanoscale ultrastructural and microchemical studies of the SPF microfossils show that large (20-70 μm) lenticular organic-walled flanged microfossils retain their structural integrity, morphology, and chain-like arrangements after acid (HF-HCl) extraction (palynology). Scanning and transmitted electron microscopy of extracted microfossils revealed that the central lenticular body is either alveolar or hollow, and the wall is continuous with the surrounding smooth to reticulated discoidal flange. These features demonstrate the evolution of large micro-organisms able to form an acid-resistant recalcitrant envelope or cell wall with complex morphology and to form colonial chains in the Paleoarchean era. This study provides evidence of the evolution of very early and remarkable biological innovations, well before the presumed late emergence of complex cells.

Micropaleontology of the lower Mesoproterozoic Roper Group, Australia, and implications for early eukaryotic evolution.

Abstract. Well-preserved microfossils occur in abundance through more than 1000m of lower Mesoproterozoic siliciclastic rocks composing the Roper Group, Northern Territory, Australia. The Roper assemblage includes 34 taxa, five interpreted unambiguously as eukaryotes, nine as possible eukaryotes (including Blastanosphaira kokkoda new genus and new species, a budding spheromorph with thin chagrinate walls), eight as possible or probable cyanobacteria, and 12 incertae sedis. Taxonomic richness is highest in inshore facies, and populations interpreted as unambiguous or probable eukaryotes occur most abundantly in coastal and proximal shelf shales. Phylogenetic placement within the Eukarya is difficult, and molecular clock estimates suggest that preserved microfossils may belong, in part or in toto, to stem group eukaryotes (forms that diverged before the last common ancestor of extant eukaryotes, or LECA) or stem lineages within major clades of the eukaryotic crown group (after LECA). Despite this, Roper fossils provide direct or inferential evidence for many basic features of eukaryotic biology, including a dynamic cytoskeleton and membrane system that enabled cells to change shape, life cycles that include resting cysts coated by decay-resistant biopolymers, reproduction by budding and binary division, osmotrophy, and simple multicellularity. The diversity, environmental range, and ecological importance of eukaryotes, however, were lower than in later Neoproterozoic and Phanerozoic ecosystems.

Iron minerals within specific microfossil morphospecies of the 1.88 Ga Gunflint Formation

Problematic microfossils dominate the palaeontological record between the Great Oxidation Event 2.4 billion years ago (Ga) and the last Palaeoproterozoic iron formations, deposited 500–600 million years later. These fossils are often associated with iron-rich sedimentary rocks, but their affinities, metabolism, and, hence, their contributions to Earth surface oxidation and Fe deposition remain unknown. Here we show that specific microfossil populations of the 1.88 Ga Gunflint Iron Formation contain Fe-silicate and Fe-carbonate nanocrystal concentrations in cell interiors. Fe minerals are absent in/on all organically preserved cell walls. These features are consistent with in vivo intracellular Fe biomineralization, with subsequent in situ recrystallization, but contrast with known patterns of post-mortem Fe mineralization. The Gunflint populations that display relatively large cells (thick-walled spheres, filament-forming rods) and intra-microfossil Fe minerals are consistent with oxygenic photosynthesizers but not with other Fe-mineralizing microorganisms studied so far. Fe biomineralization may have protected oxygenic photosynthesizers against Fe2+ toxicity during the Palaeoproterozoic.

THE END OF A MYTH: ARPYLORUS ANTIQUUS PALEOZOIC DINOFLAGELLATE CYST

Abstract Arpylorus antiquus, erected by Calandra in 1964, was isolated from upper Silurian sedimentary rocks from the Mechiguig 1 borehole in southern Tunisia, with other palynomorphs. The folded vesicle and the quadrangular form of the aperture break down into platelike fragments, resembling the tabulation of dinoflagellates. The presence of these elements has been used to interpret A. antiquus as a dinoflagellate cyst. The morphology and affinity of A. antiquus is reinterpreted herein based on investigation of larger sets of samples, including material from the type locality, together with material of Algeria, Saudi Arabia, and Brazil. More complete specimens than those previously described have been observed using gentle laboratory techniques, showing a large development of a fine membrane at the periphery of vesicles. This element was destroyed using classical palynological treatments, implying that the holotype is an incomplete specimen. The membrane at the periphery of vesicles and dorsoventral differentiation of these vesicles suggest that A. antiquus is a part of a more complex biological structure. We suggest a possible relationship with eurypterids, arthropods related to phyllocarids, represented by abundant fragments in the assemblages. Arpylorus antiquus is possibly a structure of storage. The chemical composition of A. antiquus using a Fourier transform infrared FTIR microspectroscopy analysis, reveals a wall composed of biopolymer that is not consistent with dinosporin. We conclude that Arpylorus antiquus is definitively not a dinoflagellate cyst. Although dinoflagellates may have older Paleozoic or even Proterozoic ancestors as the biomarker record may suggest, the dinoflagellate tabulation evolved only in the early Mesozoic.

DESCRIPTION AND MICROSCALE ANALYSIS OF SOME ENIGMATIC PALYNOMORPHS FROM THE MIDDLE DEVONIAN (GIVETIAN) OF LIBYA

Abstract Large acritarchs were recovered from the Awaynat Wanin II Formation in the A1-69 borehole, western Libya at 394.4 m. This sample has been dated by acritarchs and spores as Givetian (Middle Devonian). Two species of acanthomorph acritarchs were recovered that are unusually large for the Paleozoic. The first type, represented by a single specimen, is a new occurrence of a previously described but unnamed form from the Middle Devonian of the Sahara. The second type, which is more abundant, is named as Vanguestainidium cucurbitulum gen. et sp. nov. Biogeochemical analysis using infrared microspectroscopy shows that the wall composition of this new taxon is close to algaenans isolated from the green alga Botryococcus braunii Kützing 1849 although these forms are not morphologically similar. The presence of well-preserved fragile palynomorphs, abundant terrestrially-derived palynomorphs including large megaspores, and rare marine palynomorphs suggests deposition in a low-energy nearshore environment such as a coastal swamp.