Stefan Bengtson

Synchrotron X-ray tomographic microscopy of fossil embryos

Fossilized embryos from the late Neoproterozoic and earliest Phanerozoic have caused much excitement because they preserve the earliest stages of embryology of animals that represent the initial diversification of metazoans. However, the potential of this material has not been fully realized because of reliance on traditional, non-destructive methods that allow analysis of exposed surfaces only, and destructive methods that preserve only a single two-dimensional view of the interior of the specimen. Here, we have applied synchrotron-radiation X-ray tomographic microscopy (SRXTM), obtaining complete three-dimensional recordings at submicrometre resolution. The embryos are preserved by early diagenetic impregnation and encrustation with calcium phosphate, and differences in X-ray attenuation provide information about the distribution of these two diagenetic phases. Three-dimensional visualization of blastomere arrangement and diagenetic cement in cleavage embryos resolves outstanding questions about their nature, including the identity of the columnar blastomeres. The anterior and posterior anatomy of embryos of the bilaterian worm-like Markuelia confirms its position as a scalidophoran, providing new insights into body-plan assembly among constituent phyla. The structure of the developing germ band in another bilaterian, Pseudooides, indicates a unique mode of germ-band development. SRXTM provides a method of non-invasive analysis that rivals the resolution achieved even by destructive methods, probing the very limits of fossilization and providing insight into embryology during the emergence of metazoan phyla.

Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales

Over the past 25 years the discovery and study of Cretaceous plant mesofossils has yielded diverse and exquisitely preserved fossil flowers that have revolutionized our knowledge of early angiosperms, but remains of other seed plants in the same mesofossil assemblages have so far received little attention. These fossils, typically only a few millimetres long, have often been charred in natural fires and preserve both three-dimensional morphology and cellular detail. Here we use phase-contrast-enhanced synchrotron-radiation X-ray tomographic microscopy to clarify the structure of small charcoalified gymnosperm seeds from the Early Cretaceous of Portugal and North America. The new information links these seeds to Gnetales (including Erdtmanithecales, a putatively closely related fossil group), and to Bennettitales—important extinct Mesozoic seed plants with cycad-like leaves and flower-like reproductive structures. The results suggest that the distinctive seed architecture of Gnetales, Erdtmanithecales and Bennettitales defines a clade containing these taxa. This has significant consequences for hypotheses of seed plant phylogeny by providing support for key elements of the controversial anthophyte hypothesis, which links angiosperms, Bennettitales and Gnetales.

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.

Cambrian predators; possible evidence from boreholes

Boreholes in Cambrian shells are rarely reported but are a potentially significant source of information on levels of predation in early metazoan communities. This paper documents boreholes in a wide variety of Cambrian organisms. Particular attention is devoted to two species of the inarticulate brachiopod Linnarssonia (informally L. sp. A and L. sp. B) from the Middle Cambrian of southern Sweden (Brantevik, Forsemolla) and Bornholm (Laesa, ⊘lea). Both successful and abortive holes occur, and both brachial and pedicle valves were attacked. Almost 20 percent of the valves of Linnarssonia sp. B from ⊘lea have successful boreholes, whereas in L. sp. A from Brantevik only 1.4 percent of the valves are bored. The proportion of successful bores in brachial and pedicle valves also varies widely, from 0.8:1 in L. sp. A (Forsemolla) to 5.8:1 in L. sp. B (Laesa), although taphonomic bias caused by preferential removal of pedicle valves of L. sp. B may have distorted this ratio. The abundance and distribution of abortive holes also shows variation, with a maximum of 16.3 percent of L. sp. B from Forsemolla and a minimum of 1 percent in L. sp. B from Laesa. Preference for brachial or pedicle valves among abortive holes is variable, ranging from 0.3:1 in L. sp. B (Laesa) to 6.9:1 in the same species from ⊘lea. With one exception ( L. sp. B from Forsemolla) successful bores always outnumber abortives, but the ratio in brachial and pedicle valves varies widely with a maximum in favor of successful bores being reached in brachial valves of L. sp. A from Laesa (6:1). Boreholes are nonrandomly distributed. In L. sp. A and L sp. B successful attacks on brachial valves were concentrated in a central zone. Attacks were more scattered in the pedicle valves, although in L. sp. A boreholes tended to occur on the left-hand side. Abortive and successful bores in the enigmatic fossil Mobergella holsti, from the Lower Cambrian of Skaggenas, southern Sweden, show a conspicuous concentration in the apical region. In addition, boreholes in Lower Cambrian material from Australia (the pseudobrachiopod Aroonia, the tommotiid Micrina ) and eastern Siberia (brachiopods, and possibly echinoderms and the tommotiid Lapworthella ) are reported. All these bores are attributed to the activity of predators, whose systematic affinities remain uncertain. Holes in tubicolous torellellids from northern Tamdytau, however, may alternatively represent attachment scars of other torellellids.

Fossilized nuclei and germination structures identify Ediacaran "animal embryos" as encysting protists

High-resolution imaging of 570-million-year-old fossils suggests that they were not remnants of early animals. Globular fossils showing palintomic cell cleavage in the Ediacaran Doushantuo Formation, China, are widely regarded as embryos of early metazoans, although metazoan synapomorphies, tissue differentiation, and associated juveniles or adults are lacking. We demonstrate using synchrotron-based x-ray tomographic microscopy that the fossils have features incompatible with multicellular metazoan embryos. The developmental pattern is comparable with nonmetazoan holozoans, including germination stages that preclude postcleavage embryology characteristic of metazoans. We conclude that these fossils are neither animals nor embryos. They belong outside crown-group Metazoa, within total-group Holozoa (the sister clade to Fungi that includes Metazoa, Choanoflagellata, and Mesomycetozoea) or perhaps on even more distant branches in the eukaryote tree. They represent an evolutionary grade in which palintomic cleavage served the function of producing propagules for dispersion.

Chronology of early Cambrian biomineralization

Data on the first appearances of major animal groups with mineralized skeletons on the Siberian Platform and worldwide are revised and summarized herein with references to an improved carbon isotope stratigraphy and radiometric dating in order to reconstruct the Cambrian radiation (popularly known as the ‘Cambrian explosion’) with a higher precision and provide a basis for the definition of Cambrian Stages 2 to 4. The Lophotrochozoa and, probably, Chaetognatha were first among protostomians to achieve biomineralization during the Terreneuvian Epoch, mainly the Fortunian Age. Fast evolutionary radiation within the Lophotrochozoa was followed by radiation of the sclerotized and biomineralized Ecdysozoa during Stage 3. The first mineralized skeletons of the Deuterostomia, represented by echinoderms, appeared in the middle of Cambrian Stage 3. The fossil record of sponges and cnidarians suggests that they acquired biomineralized skeletons in the late Neoproterozoic, but diversification of both definite sponges and cnidarians was in parallel to that of bilaterians. The distribution of calcium carbonate skeletal mineralogies from the upper Ediacaran to lower Cambrian reflects fluctuations in the global ocean chemistry and shows that the Cambrian radiation occurred mainly during a time of aragonite and high-magnesium calcite seas.

Embryo fossilization is a biological process mediated by microbial biofilms.

Fossilized embryos with extraordinary cellular preservation appear in the Late Neoproterozoic and Cambrian, coincident with the appearance of animal body fossils. It has been hypothesized that microbial processes are responsible for preservation and mineralization of organic tissues. However, the actions of microbes in preservation of embryos have not been demonstrated experimentally. Here, we show that bacterial biofilms assemble rapidly in dead marine embryos and form remarkable pseudomorphs in which the bacterial biofilm replaces and exquisitely models details of cellular organization and structure. The experimental model was the decay of cleavage stage embryos similar in size and morphology to fossil embryos. The data show that embryo preservation takes place in 3 distinct steps: (i) blockage of autolysis by reducing or anaerobic conditions, (ii) rapid formation of microbial biofilms that consume the embryo but form a replica that retains cell organization and morphology, and (iii) bacterially catalyzed mineralization. Major bacterial taxa in embryo decay biofilms were identified by using 16S rDNA sequencing. Decay processes were similar in different taphonomic conditions, but the composition of bacterial populations depended on specific conditions. Experimental taphonomy generates preservation states similar to those in fossil embryos. The data show how fossilization of soft tissues in sediments can be mediated by bacterial replacement and mineralization, providing a foundation for experimentally creating biofilms from defined microbial species to model fossilization as a biological process.

Fossilized embryos are widespread but the record is temporally and taxonomically biased

SUMMARY We report new discoveries of embryos and egg capsules from the Lower Cambrian of Siberia, Middle Cambrian of Australia and Lower Ordovician of North America. Together with existing records, embryos have now been recorded from four of the seven continents. However, the new discoveries highlight secular and systematic biases in the fossil record of embryonic stages. The temporal window within which the embryos and egg capsules are found is of relatively short duration; it ends in the Early Ordovician and is roughly coincident with that of typical “Orsten”‐type faunas. The reduced occurrence of such fossils has been attributed to reducing levels of phosphate in marine waters during the early Paleozoic, but may also be owing to the increasing depth of sediment mixing by infaunal metazoans. Furthermore, most records younger than the earliest Cambrian are of a single kind—large eggs and embryos of the priapulid‐like scalidophoran Markuelia. We explore alternative explanations for the low taxonomic diversity of embryos recovered thus far, including sampling, size, anatomy, ecology, and environment, concluding that the preponderance of Markuelia embryos is due to its precocious development of cuticle at an embryonic stage, predisposing it to preservation through action as a substrate on which microbially mediated precipitation of authigenic calcium phosphate may occur. The fossil record of embryos may be limited to a late Neoproterozoic to early Ordovician snapshot that is subject to dramatic systematic bias. Together, these biases must be considered seriously in attempts to use the fossil record to arbitrate between hypotheses of developmental and life history evolution implicated in the origin of metazoan clades.

The controversial “Cambrian” fossils of the Vindhyan are real but more than a billion years older

The age of the Vindhyan sedimentary basin in central India is controversial, because geochronology indicating early Proterozoic ages clashes with reports of Cambrian fossils. We present here an integrated paleontologic–geochronologic investigation to resolve this conundrum. New sampling of Lower Vindhyan phosphoritic stromatolitic dolomites from the northern flank of the Vindhyans confirms the presence of fossils most closely resembling those found elsewhere in Cambrian deposits: annulated tubes, embryo-like globules with polygonal surface pattern, and filamentous and coccoidal microbial fabrics similar to Girvanella and Renalcis. None of the fossils, however, can be ascribed to uniquely Cambrian or Ediacaran taxa. Indeed, the embryo-like globules are not interpreted as fossils at all but as former gas bubbles trapped in mucus-rich cyanobacterial mats. Direct dating of the same fossiliferous phosphorite yielded a Pb–Pb isochron of 1,650 ± 89 (2σ) million years ago, confirming the Paleoproterozoic age of the fossils. New U–Pb geochronology of zircons from tuffaceous mudrocks in the Lower Vindhyan Porcellanite Formation on the southern flank of the Vindhyans give comparable ages. The Vindhyan phosphorites provide a window of 3-dimensionally preserved Paleoproterozoic fossils resembling filamentous and coccoidal cyanobacteria and filamentous eukaryotic algae, as well as problematic forms. Like Neoproterozoic phosphorites a billion years later, the Vindhyan deposits offer important new insights into the nature and diversity of life, and in particular, the early evolution of multicellular eukaryotes.

Oxygen dynamics in the aftermath of the Great Oxidation of Earth’s atmosphere

Significance The Great Oxidation of Earth’s atmosphere about 2.3 billion years ago began a series of geochemical events leading to elevated oxygen levels for the next 200 million years, with a collapse to much lower levels as these events played their course. This sequence of events is represented in rocks from the Republic of Gabon. We show oxygenation of the deep oceans when oxygen levels were likely their highest. By 2.08 billion years ago, however, oxygen dropped to levels possibly as low as any time in the last 2.3 billion years. These fluctuations can be explained as a direct consequence of the initial oxygenation of the atmosphere during the Great Oxidation Event. The oxygen content of Earth’s atmosphere has varied greatly through time, progressing from exceptionally low levels before about 2.3 billion years ago, to much higher levels afterward. In the absence of better information, we usually view the progress in Earth’s oxygenation as a series of steps followed by periods of relative stasis. In contrast to this view, and as reported here, a dynamic evolution of Earth’s oxygenation is recorded in ancient sediments from the Republic of Gabon from between about 2,150 and 2,080 million years ago. The oldest sediments in this sequence were deposited in well-oxygenated deep waters whereas the youngest were deposited in euxinic waters, which were globally extensive. These fluctuations in oxygenation were likely driven by the comings and goings of the Lomagundi carbon isotope excursion, the longest–lived positive δ13C excursion in Earth history, generating a huge oxygen source to the atmosphere. As the Lomagundi event waned, the oxygen source became a net oxygen sink as Lomagundi organic matter became oxidized, driving oxygen to low levels; this state may have persisted for 200 million years.