A possible billion-year-old holozoan with differentiated multicellularity.

Sediments of the Torridonian sequence of the Northwest Scottish Highlands contain a wide array of microfossils, documenting life in a non-marine setting a billion years ago (1 Ga).1-4 Phosphate nodules from the Diabaig Formation at Loch Torridon preserve microorganisms with cellular-level fidelity,5,6 allowing for partial reconstruction of the developmental stages of a new organism, Bicellum brasieri gen. et sp. nov. The mature form of Bicellum consists of a solid, spherical ball of tightly packed cells (a stereoblast) of isodiametric cells enclosed in a monolayer of elongated, sausage-shaped cells. However, two populations of naked stereoblasts show mixed cell shapes, which we infer to indicate incipient development of elongated cells that were migrating to the periphery of the cell mass. These simple morphogenetic movements could be explained by differential cell-cell adhesion.7,8 In fact, the basic morphology of Bicellum is topologically similar to that of experimentally produced cell masses that were shown to spontaneously segregate into two distinct domains based on differential cadherin-based cell adhesion.9 The lack of rigid cell walls in the stereoblast renders an algal affinity for Bicellum unlikely: its overall morphology is more consistent with a holozoan origin. Unicellular holozoans are known today to form multicellular stages within complex life cycles,10-13 so the occurrence of such simple levels of transient multicellularity seen here is consistent with a holozoan affinity. Regardless of precise phylogenetic placement, these fossils demonstrate simple cell differentiation and morphogenic processes that are similar to those seen in some metazoans today.

Ichnological evidence for meiofaunal bilaterians from the terminal Ediacaran and earliest Cambrian of Brazil.

The evolutionary events during the Ediacaran-Cambrian transition (~541 Myr ago) are unparalleled in Earth history. The fossil record suggests that most extant animal phyla appeared in a geologically brief interval, with the oldest unequivocal bilaterian body fossils found in the Early Cambrian. Molecular clocks and biomarkers provide independent estimates for the timing of animal origins, and both suggest a cryptic Neoproterozoic history for Metazoa that extends considerably beyond the Cambrian fossil record. We report an assemblage of ichnofossils from Ediacaran-Cambrian siltstones in Brazil, alongside U-Pb radioisotopic dates that constrain the age of the oldest specimens to 555-542 Myr. X-ray microtomography reveals three-dimensionally preserved traces ranging from 50 to 600 µm in diameter, indicative of small-bodied, meiofaunal tracemakers. Burrow morphologies suggest they were created by a nematoid-like organism that used undulating locomotion to move through the sediment. This assemblage demonstrates animal-sediment interactions in the latest Ediacaran period, and provides the oldest known fossil evidence for meiofaunal bilaterians. Our discovery highlights meiofaunal ichnofossils as a hitherto unexplored window for tracking animal evolution in deep time, and reveals that both meiofaunal and macrofaunal bilaterians began to explore infaunal niches during the late Ediacaran.

Quantitative study of developmental biology confirms Dickinsonia as a metazoan.

The late Ediacaran soft-bodied macroorganism Dickinsonia (age range approx. 560-550 Ma) has often been interpreted as an early animal, and is increasingly invoked in debate on the evolutionary assembly of eumetazoan body plans. However, conclusive positive evidence in support of such a phylogenetic affinity has not been forthcoming. Here we subject a collection of Dickinsonia specimens interpreted to represent multiple ontogenetic stages to a novel, quantitative method for studying growth and development in organisms with an iterative body plan. Our study demonstrates that Dickinsonia grew via pre-terminal 'deltoidal' insertion and inflation of constructional units, followed by a later inflation-dominated phase of growth. This growth model is contrary to the widely held assumption that Dickinsonia grew via terminal addition of units at the end of the organism bearing the smallest units. When considered alongside morphological and behavioural attributes, our developmental data phylogenetically constrain Dickinsonia to the Metazoa, specifically the Eumetazoa plus Placozoa total group. Our findings have implications for the use of Dickinsonia in developmental debates surrounding the metazoan acquisition of axis specification and metamerism.

Changing the picture of Earth's earliest fossils (3.5-1.9 Ga) with new approaches and new discoveries.

New analytical approaches and discoveries are demanding fresh thinking about the early fossil record. The 1.88-Ga Gunflint chert provides an important benchmark for the analysis of early fossil preservation. High-resolution analysis of Gunflintia shows that microtaphonomy can help to resolve long-standing paleobiological questions. Novel 3D nanoscale reconstructions of the most ancient complex fossil Eosphaera reveal features hitherto unmatched in any crown-group microbe. While Eosphaera may preserve a symbiotic consortium, a stronger conclusion is that multicellular morphospace was differently occupied in the Paleoproterozoic. The 3.46-Ga Apex chert provides a test bed for claims of biogenicity of cell-like structures. Mapping plus focused ion beam milling combined with transmission electron microscopy data demonstrate that microfossil-like taxa, including species of Archaeoscillatoriopsis and Primaevifilum, are pseudofossils formed from vermiform phyllosilicate grains during hydrothermal alteration events. The 3.43-Ga Strelley Pool Formation shows that plausible early fossil candidates are turning up in unexpected environmental settings. Our data reveal how cellular clusters of unexpectedly large coccoids and tubular sheath-like envelopes were trapped between sand grains and entombed within coatings of dripstone beach-rock silica cement. These fossils come from Earth's earliest known intertidal to supratidal shoreline deposit, accumulated under aerated but oxygen poor conditions.

Haootia quadriformis n. gen., n. sp., interpreted as a muscular cnidarian impression from the Late Ediacaran period (approx. 560 Ma).

Muscle tissue is a fundamentally eumetazoan attribute. The oldest evidence for fossilized muscular tissue before the Early Cambrian has hitherto remained moot, being reliant upon indirect evidence in the form of Late Ediacaran ichnofossils. We here report a candidate muscle-bearing organism, Haootia quadriformis n. gen., n. sp., from approximately 560 Ma strata in Newfoundland, Canada. This taxon exhibits sediment moulds of twisted, superimposed fibrous bundles arranged quadrilaterally, extending into four prominent bifurcating corner branches. Haootia is distinct from all previously published contemporaneous Ediacaran macrofossils in its symmetrically fibrous, rather than frondose, architecture. Its bundled fibres, morphology, and taphonomy compare well with the muscle fibres of fossil and extant Cnidaria, particularly the benthic Staurozoa. Haootia quadriformis thus potentially provides the earliest body fossil evidence for both metazoan musculature, and for Eumetazoa, in the geological record.

Enhanced cellular preservation by clay minerals in 1 billion-year-old lakes.

Organic-walled microfossils provide the best insights into the composition and evolution of the biosphere through the first 80 percent of Earth history. The mechanism of microfossil preservation affects the quality of biological information retained and informs understanding of early Earth palaeo-environments. We here show that 1 billion-year-old microfossils from the non-marine Torridon Group are remarkably preserved by a combination of clay minerals and phosphate, with clay minerals providing the highest fidelity of preservation. Fe-rich clay mostly occurs in narrow zones in contact with cellular material and is interpreted as an early microbially-mediated phase enclosing and replacing the most labile biological material. K-rich clay occurs within and exterior to cell envelopes, forming where the supply of Fe had been exhausted. Clay minerals inter-finger with calcium phosphate that co-precipitated with the clays in the sub-oxic zone of the lake sediments. This type of preservation was favoured in sulfate-poor environments where Fe-silicate precipitation could outcompete Fe-sulfide formation. This work shows that clay minerals can provide an exceptionally high fidelity of microfossil preservation and extends the known geological range of this fossilization style by almost 500 Ma. It also suggests that the best-preserved microfossils of this time may be found in low-sulfate environments.

Giving the early fossil record of sponges a squeeze.

Twenty candidate fossils with claim to be the oldest representative of the Phylum Porifera have been re-analysed. Three criteria are used to assess each candidate: (i) the diagnostic criteria needed to categorize sponges in the fossil record; (ii) the presence, or absence, of such diagnostic features in the putative poriferan fossils; and (iii) the age constraints for the candidate fossils. All three criteria are critical to the correct interpretation of any fossil and its placement within an evolutionary context. Our analysis shows that no Precambrian fossil candidate yet satisfies all three of these criteria to be a reliable sponge fossil. The oldest widely accepted candidate, Mongolian silica hexacts from c. 545 million years ago (Ma), are here shown to be cruciform arsenopyrite crystals. The oldest reliable sponge remains are siliceous spicules from the basal Cambrian (Protohertzina anabarica Zone) Soltanieh Formation, Iran, which are described and analysed here in detail for the first time. Extensive archaeocyathan sponge reefs emerge and radiate as late as the middle of the Fortunian Stage of the Cambrian and demonstrate a gradual assembly of their skeletal structure through this time coincident with the evolution of other metazoan groups. Since the Porifera are basal in the Metazoa, their presence within the late Proterozoic has been widely anticipated. Molecular clock calibration for the earliest Porifera and Metazoa should now be based on the Iranian hexactinellid material dated to c. 535 Ma. The earliest convincing fossil sponge remains appeared at around the time of the Precambrian-Cambrian boundary, associated with the great radiation events of that interval.

Nanoscale analysis of pyritized microfossils reveals differential heterotrophic consumption in the ~1.9-Ga Gunflint chert.

The 1.88-Ga Gunflint biota is one of the most famous Precambrian microfossil lagerstätten and provides a key record of the biosphere at a time of changing oceanic redox structure and chemistry. Here, we report on pyritized replicas of the iconic autotrophic Gunflintia-Huroniospora microfossil assemblage from the Schreiber Locality, Canada, that help capture a view through multiple trophic levels in a Paleoproterozoic ecosystem. Nanoscale analysis of pyritic Gunflintia (sheaths) and Huroniospora (cysts) reveals differing relic carbon and nitrogen distributions caused by contrasting spectra of decay and pyritization between taxa, reflecting in part their primary organic compositions. In situ sulfur isotope measurements from individual microfossils (δ(34)S(V-CDT) +6.7‰ to +21.5‰) show that pyritization was mediated by sulfate-reducing microbes within sediment pore waters whose sulfate ion concentrations rapidly became depleted, owing to occlusion of pore space by coeval silicification. Three-dimensional nanotomography reveals additional pyritized biomaterial, including hollow, cellular epibionts and extracellular polymeric substances, showing a preference for attachment to Gunflintia over Huroniospora and interpreted as components of a saprophytic heterotrophic, decomposing community. This work also extends the record of remarkable biological preservation in pyrite back to the Paleoproterozoic and provides criteria to assess the authenticity of even older pyritized microstructures that may represent some of the earliest evidence for life on our planet.

Pumice as a remarkable substrate for the origin of life.

The context for the emergence of life on Earth sometime prior to 3.5 billion years ago is almost as big a puzzle as the definition of life itself. Hitherto, the problem has largely been addressed in terms of theoretical and experimental chemistry plus evidence from extremophile habitats like modern hydrothermal vents and meteorite impact structures. Here, we argue that extensive rafts of glassy, porous, and gas-rich pumice could have had a significant role in the origin of life and provided an important habitat for the earliest communities of microorganisms. This is because pumice has four remarkable properties. First, during eruption it develops the highest surface-area-to-volume ratio known for any rock type. Second, it is the only known rock type that floats as rafts at the air-water interface and then becomes beached in the tidal zone for long periods of time. Third, it is exposed to an unusually wide variety of conditions, including dehydration. Finally, from rafting to burial, it has a remarkable ability to adsorb metals, organics, and phosphates as well as to host organic catalysts such as zeolites and titanium oxides. These remarkable properties now deserve to be rigorously explored in the laboratory and the early rock record.

Earth's earliest non-marine eukaryotes.

The existence of a terrestrial Precambrian (more than 542 Myr ago) biota has been largely inferred from indirect chemical and geological evidence associated with palaeosols, the weathering of clay minerals and microbially induced sedimentary structures in siliciclastic sediments. Direct evidence of fossils within rocks of non-marine origin in the Precambrian is exceedingly rare. The most widely cited example comprises a single report of morphologically simple mineralized tubes and spheres interpreted as cyanobacteria, obtained from 1,200-Myr-old palaeokarst in Arizona. Organic-walled microfossils were first described from the non-marine Torridonian (1.2-1.0 Gyr ago) sequence of northwest Scotland in 1907. Subsequent studies found few distinctive taxa-a century later, the Torridonian microflora is still being characterized as primarily nondescript "leiospheres". We have comprehensively sampled grey shales and phosphatic nodules throughout the Torridonian sequence. Here we report the recovery of large populations of diverse organic-walled microfossils extracted by acid maceration, complemented by studies using thin sections of phosphatic nodules that yield exceptionally detailed three-dimensional preservation. These assemblages contain multicellular structures, complex-walled cysts, asymmetric organic structures, and dorsiventral, compressed organic thalli, some approaching one millimetre in diameter. They offer direct evidence of eukaryotes living in freshwater aquatic and subaerially exposed habitats during the Proterozoic era. The apparent dominance of eukaryotes in non-marine settings by 1 Gyr ago indicates that eukaryotic evolution on land may have commenced far earlier than previously thought.

On biogenicity criteria for endolithic microborings on early Earth and beyond.

Micron-sized cavities created by the actions of rock-etching microorganisms known as euendoliths are explored as a biosignature for life on early Earth and perhaps Mars. Rock-dwelling organisms can tolerate extreme environmental stresses and are excellent candidates for the colonization of early Earth and planetary surfaces. Here, we give a brief overview of the fossil record of euendoliths in both sedimentary and volcanic rocks. We then review the current understanding of the controls upon the distribution of euendolithic microborings and use these to propose three lines of approach for testing their biogenicity: first, a geological setting that demonstrates a syngenetic origin for the euendolithic microborings; second, microboring morphologies and distributions that are suggestive of biogenic behavior and distinct from ambient inclusion trails; and third, elemental and isotopic evidence suggestive of biological processing. We use these criteria and the fossil record of terrestrial euendoliths to outline potential environments and techniques to search for endolithic microborings on Mars.

Questioning the evidence for Earth's oldest fossils.

Structures resembling remarkably preserved bacterial and cyanobacterial microfossils from about 3,465-million-year-old Apex cherts of the Warrawoona Group in Western Australia currently provide the oldest morphological evidence for life on Earth and have been taken to support an early beginning for oxygen-producing photosynthesis. Eleven species of filamentous prokaryote, distinguished by shape and geometry, have been put forward as meeting the criteria required of authentic Archaean microfossils, and contrast with other microfossils dismissed as either unreliable or unreproducible. These structures are nearly a billion years older than putative cyanobacterial biomarkers, genomic arguments for cyanobacteria, an oxygenic atmosphere and any comparably diverse suite of microfossils. Here we report new research on the type and re-collected material, involving mapping, optical and electron microscopy, digital image analysis, micro-Raman spectroscopy and other geochemical techniques. We reinterpret the purported microfossil-like structure as secondary artefacts formed from amorphous graphite within multiple generations of metalliferous hydrothermal vein chert and volcanic glass. Although there is no support for primary biological morphology, a Fischer--Tropsch-type synthesis of carbon compounds and carbon isotopic fractionation is inferred for one of the oldest known hydrothermal systems on Earth.