Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago.

Evidence for macroscopic life in the Paleoproterozoic Era comes from 1.8 billion-year-old (Ga) compression fossils [Han TM, Runnegar B (1992) Science 257:232-235; Knoll et al. (2006) Philos Trans R Soc Lond B 361:1023-1038], Stirling biota [Bengtson S et al. (2007) Paleobiology 33:351-381], and large colonial organisms exhibiting signs of coordinated growth from the 2.1-Ga Francevillian series, Gabon. Here we report on pyritized string-shaped structures from the Francevillian Basin. Combined microscopic, microtomographic, geochemical, and sedimentologic analyses provide evidence for biogenicity, and syngenicity and suggest that the structures underwent fossilization during early diagenesis close to the sediment-water interface. The string-shaped structures are up to 6 mm across and extend up to 170 mm through the strata. Morphological and 3D tomographic reconstructions suggest that the producer may have been a multicellular or syncytial organism able to migrate laterally and vertically to reach food resources. A possible modern analog is the aggregation of amoeboid cells into a migratory slug phase in cellular slime molds at times of starvation. This unique ecologic window established in an oxygenated, shallow-marine environment represents an exceptional record of the biosphere following the crucial changes that occurred in the atmosphere and ocean in the aftermath of the great oxidation event (GOE).

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.

Oxygen dynamics in the aftermath of the Great Oxidation of Earth's atmosphere.

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 δ(13)C 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.

Characterization of Sulfur-Rich Microbial Organic Matter in Jurassic Carbonates Using Laser-Assisted Mass Spectrometry.

Laser desorption-ionization mass spectrometry (MS) shows great potential for in situ molecular analysis of planetary surfaces and microanalysis of space-returned samples or (micro)fossils. Coupled with pyrolysis gas chromatography-mass spectrometry (Py-GC-MS) in ESA's ExoMars project, this technique could help assess further the origin of sulfur-bearing organic matter (OM) recently detected on Mars. To unravel this potential, we analyzed sulfurized microbial OM from ca. 150 million year-old carbonates with laser desorption-ionization mass spectrometry (single- and two-step: LDI-MS and L2MS), in comparison with time-of-flight secondary-ion mass spectrometry (ToF-SIMS), gas chromatography-mass spectrometry (GC-MS), and Py-GC-MS. We show that LDI-MS and L2MS readily detect sulfur-bearing moieties such as (alkyl)thiophenes and (alkyl)benzothiophenes. The mineral matrix, however, made the identification of sulfur-bearing molecules challenging in our L2MS experiment. The dominance of small aromatic hydrocarbons (≤14 carbons) in the LDI-MS and L2MS of the extracted soluble and insoluble OM and of the bulk rock is consistent with the low thermal maturity of the sediment and contrasts with the predominance of larger polycyclic aromatic structures commonly observed in meteorites with these techniques. We detected inorganic ions, in particular VO+, in demineralized OM that likely originate from geoporphyrins, which derive from chlorophylls during sediment diagenesis. Finally, insoluble OM yielded distinct compositions compared with extracted soluble OM, with a greater abundance of ions of mass-to-charge ratio (m/z) over 175 and additional N-moieties. This highlights the potential of laser-assisted MS to decipher the composition of macromolecular OM, in particular to investigate the preservation of biomacromolecules in microfossils. Studies comparing diverse biogenic and abiogenic OM are needed to further assess the use of this technique to search for biosignatures.

New preparation techniques for molecular and in-situ analysis of ancient organic micro- and nanostructures.

Organic microfossils preserved in three dimensions in transparent mineral matrices such as cherts/quartzites, phosphates, or carbonates are best studied in petrographic thin sections. Moreover, microscale mass spectrometry techniques commonly require flat, polished surfaces to minimize analytical bias. However, contamination by epoxy resin in traditional petrographic sections is problematic for the geochemical study of the kerogen in these microfossils and more generally for the in situ analysis of fossil organic matter. Here, we show that epoxy contamination has a molecular signature that is difficult to distinguish from kerogen with time-of-flight secondary ion mass spectrometry (ToF-SIMS). This contamination appears pervasive in organic microstructures embedded in micro- to nano-crystalline carbonate. To solve this problem, a new semi-thin section preparation protocol without resin medium was developed for micro- to nanoscale in situ investigation of insoluble organic matter. We show that these sections are suited for microscopic observation of Proterozoic microfossils in cherts. ToF-SIMS reveals that these sections are free of pollution after final removal of a <10 nm layer of contamination using low-dose ion sputtering. ToF-SIMS maps of fragments from aliphatic and aromatic molecules and organic sulfur are correlated with the spatial distribution of organic microlaminae in a Jurassic stromatolite. Hydrocarbon-derived ions also appeared correlated with kerogenous microstructures in Archean cherts. These developments in analytical procedures should help future investigations of organic matter and in particular, microfossils, by allowing the spatial correlation of microscopy, spectroscopy, precise isotopic microanalyses, and novel molecular microanalyses such as ToF-SIMS.

Author Correction: Microbially induced potassium enrichment in Paleoproterozoic shales and implications for reverse weathering on early Earth.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Microbially induced potassium enrichment in Paleoproterozoic shales and implications for reverse weathering on early Earth.

Illitisation requires potassium incorporation into a smectite precursor, a process akin to reverse weathering. However, it remains unclear whether microbes facilitate K+ uptake to the sediments and whether illitisation was important in the geological past. The 2.1 billion-year-old Francevillian Series of Gabon has been shown to host mat-related structures (MRS) and, in this regard, these rocks offer a unique opportunity to test whether ancient microbes induced illitisation. Here, we show high K content confined to illite particles that are abundant in the facies bearing MRS, but not in the host sandstone and black shale. This observation suggests that microbial biofilms trapped K+ from the seawater and released it into the pore-waters during respiration, resulting in illitisation. The K-rich illite developed exclusively in the fossilized MRS thus provides a new biosignature for metasediments derived from K-feldspar-depleted rocks that were abundant crustal components on ancient Earth.

Unusual microbial mat-related structural diversity 2.1 billion years ago and implications for the Francevillian biota.

The 2.1-billion-year-old (Ga) Francevillian series in Gabon hosts some of the oldest reported macroscopic fossils of various sizes and shapes, stimulating new debates on the origin, evolution and organization of early complex life. Here, we document ten representative types of exceptionally well-preserved mat-related structures, comprising "elephant-skin" textures, putative macro-tufted microbial mats, domal buildups, flat pyritized structures, discoidal microbial colonies, horizontal mat growth patterns, wrinkle structures, "kinneyia" structures, linear patterns and nodule-like structures. A combination of petrographic analyses, scanning electron microscopy, Raman spectroscopy and organic elemental analyses of carbon-rich laminae and microtexture, indicate a biological origin for these structures. The observed microtextures encompass oriented grains, floating silt-sized quartz grains, concentrated heavy minerals, randomly oriented clays, wavy-crinkly laminae and pyritized structures. Based on comparisons with modern analogues, as well as an average δ13 C organic matter (Corg ) composition of -32.94 ± 1.17‰ (1 standard deviation, SD) with an outlier of -41.26‰, we argue that the mat-related structures contain relicts of multiple carbon pathways including heterotrophic recycling of photosynthetically derived Corg . Moreover, the relatively close association of the macroscopic fossil assemblages to the microbial mats may imply that microbial communities acted as potential benthic O2 oases linked to oxyphototrophic cyanobacterial mats and grazing grounds. In addition, the mat's presence likely improved the preservation of the oldest large colonial organisms, as they are known to strongly biostabilize sediments. Our findings highlight the oldest community assemblage of microscopic and macroscopic biota in the aftermath of the "Great Oxidation Event," widening our understanding of biological organization during Earth's middle age.

The 2.1 Ga old Francevillian biota: biogenicity, taphonomy and biodiversity.

The Paleoproterozoic Era witnessed crucial steps in the evolution of Earth's surface environments following the first appreciable rise of free atmospheric oxygen concentrations ∼2.3 to 2.1 Ga ago, and concomitant shallow ocean oxygenation. While most sedimentary successions deposited during this time interval have experienced thermal overprinting from burial diagenesis and metamorphism, the ca. 2.1 Ga black shales of the Francevillian B Formation (FB2) cropping out in southeastern Gabon have not. The Francevillian Formation contains centimeter-sized structures interpreted as organized and spatially discrete populations of colonial organisms living in an oxygenated marine ecosystem. Here, new material from the FB2 black shales is presented and analyzed to further explore its biogenicity and taphonomy. Our extended record comprises variably sized, shaped, and structured pyritized macrofossils of lobate, elongated, and rod-shaped morphologies as well as abundant non-pyritized disk-shaped macrofossils and organic-walled acritarchs. Combined microtomography, geochemistry, and sedimentary analysis suggest a biota fossilized during early diagenesis. The emergence of this biota follows a rise in atmospheric oxygen, which is consistent with the idea that surface oxygenation allowed the evolution and ecological expansion of complex megascopic life.