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Micro-pyrites associated with organic material in ancient stromatolites: a new proxy attesting for their biogenicity

Periodic Reporting for period 5 - STROMATA (Micro-pyrites associated with organic material in ancient stromatolites: a new proxy attesting for their biogenicity)

Période du rapport: 2023-02-01 au 2023-12-31

The question of the origin of Life is one of the noblest questions we can ask in science. Understanding the conditions of the origin and evolution of life has always been an important prerequisite for answering the question of where we came from. Identifying Archean fossils from Earth's early biosphere is an ambitious task that has excited researchers for decades. Recovering traces of life in the geological record is challenging due to the scarcity of the oldest rocks (10% of the Earth's surface) and the complex post-depositional history (diagenesis, metasomatism, metamorphism) of these rocks. Moreover, the first forms of life were small (microorganisms) with micrometer dimensions and did not form macroscopic fossils, but rather ambiguous structures such as stromatolites and microbially induced sedimentary structures (MISS). The identification of the biogenicity and syngenicity of these structures is mostly based on the identification of morphological and stable geochemical signatures by comparison with modern analogs [e.g. 1]. However, the biogenicity of Archean stromatolites and MISS remains controversial [2], and these structures rarely contain definitive microbial body fossils [3]. Furthermore, it remains difficult to relate Archean microbial structures to specific metabolic pathways such as oxygenic photosynthesis, microbial sulfate reduction or taxonomic groups [2]. Therefore, the question remains open and requires a new approach to approach it from a new angle. Stromatolites and MISS can contain small sulfides (about 1 micron in size), intimately associated with the organic lamina in the case of the fossil ones, or with the microbial mat in the case of the modern ones [4, 5]. Sulfides, and in particular pyrite (FeS2), may have recorded the influence of microbial metabolisms such as sulfate reduction or iron respiration and can therefore be used as a proxy for microbial activities [6-9], although the precise role of biotic and abiotic processes in the pyrite formation pathway remains to be clarified [10]. The present project will question the origin of these sub-micron sulfides to define new and strong criteria for the identification of the biogenicity of stromatolites and MISS. STROMATA proposes new in situ analytical developments that allow the isotopic analysis of small geological objects, micropyrite grains in stromatolites or (MISS), which we propose to be more robust markers of early metabolism.

The STROMATA project aims to propose robust criteria for metabolic and biological activities, specifically for recording the first traces of life. This can be subdivided into several sub-questions:
Were Archean stromatolites and MISS produced by significant and diverse biological activities?
Do the Fe and S isotope compositions of micro-pyrites associated with organic material record metabolic signatures?
Were the isotopic and mineralogical biosignatures of micro-pyrite modified by environmental or post-depositional processes?

We have conducted a comparative study of Precambrian and modern stromatolites, as well as experimentally produced abiotic pyrites. We have performed detailed mineralogical characterization on a small scale, conducted in-situ investigations of various stable isotope proxies (Fe, S), and chemically identified the organic material. This original approach combines isotopic analyses, chemical characterization, and mineralogical description using state-of-the-art techniques such as NanoSIMS, SIMS, Raman, FIB-TEM, and XANES. STROMATA provided new constraints on the potential evolution of important metabolic pathways, such as microbial sulfate reduction and iron respiration, and their connection with anoxygenic or oxygenic photosynthesis.
We have developed new SIMS and NanoSIMS methodologies (Marin Carbonne et al., 2018, Decraene et al. 2019) to investigate the presence of metabolic isotope signatures recorded in ancient stromatolite and sediments. These protocols have been calibrated on different instruments and have been published. We also have discovered that a Fe isotope pyrite standard contains two different isotopic compositions (Pasquier et al., accepted at Geostandards), that have induced minor errors in two articles that have been corrected (Dupeyron et al., 2023, Decraene et al., 2023).
During the project, we conducted one field campaign in South Africa in 2019, the others were canceled due to the pandemic. However various collaborators have provided stromatolitic samples we have used, as the Malmani stromatolite for example. We also have conducted experimental diagenesis on different samples but we have not yet finished to characterize them.

We have demonstrated the presence of microbial sulfate reduction and iron dissimilatory reduction in the Tumbiana Formation (Australia, 2.7 Ga, Marin Carbonne et al. 2018, and Decraene et al., 2019), in the Mendon Formation (3.2 Ga. South Africa, Marin Carbonne et al., 2020). We have demonstrated that the Buck Reef Chert, despite its geological history, has preserved chemical heterogeneity in organic molecules (Alleon et al., 2021) and iron-mediated anaerobic ammonium oxidation (Pellerin et al., 2023). The study of modern stromatolite suggested the importance of microbial sulfate reduction in the biomineralization of the microbialite and that sulfide recorded near equilibrium isotope fractionation (Marin Carbonne et al., 2022). In a review article, we have identified the effect of metamorphism and diagenesis on the Fe isotope composition of sulfide (Dupeyron et al., 2023) but we were unable to identify the effect of the Great Oxygenation Event (GOE) on microbial metabolisms. We have published 18 research articles, three chapters that will be published in 2024 and 2025, and one special issue is ongoing. The results of the project have been presented at various conferences and workshops. One PhD student successfully defended her Ph.D another will finish in 2023, three post doc researchers have found permanent positions, one as a museum researcher in Japan, one as a CNRS researcher in France, and one as an assistant professor in US.

We have organized on workshop on Microbialite, M-Fed23 in October 2023 in Leysin Switzerland, this event internationally attended has been followed by an exhibition at the Palais de Rumine in Lausanne. The PI has given an opening conference, where the results of the project were presented.
We have demonstrated that micropyrite in microbialite and stromatolite records local processes rather than global conditions and thus can be an interesting proxy for recording ancient microbial metabolism.
Additionally, we have shown that ancient microbial metabolic activities can be preserved even if the sediments have undergone complex post-depositional processes. While we were able to demonstrate the biogenesis of some stromatolites, but not for all samples were studied. Our investigation will continue on the remaining samples collected during this project, to better understand their geochemistry.
Both analytical protocols developed are of interest to the scientific community. Several researchers have requested collaboration, particularly on modern microbialites.

The results have raised further questions that we will attempt to answer soon. For example, why can micropyrite be found in some stromatolites and not in others from similar environments? What controls pyrite formation in these environments?
Stromatolite from Malmani Campbellrand Platform (2.5 Ga, South Africa)
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