Modern activity and ancient signatures preserved by metals in microbial mats of lake environments

Exopolymeric Substances (EPS) form biofilms in which the vast majority of prokaryotic organisms develop and thrive. They are ubiquitous,  harbor metal and chemical species binding properties and can be the matrix for bio/orgamineralizations. Because of these properties, EPS have also been proposed as some of the most ancient traces of microbial life on Earth. They form sedimentary structures diagnostic of biological activity in some of the most ancient sedimentary rocks of the Archean. However, the metabolisms hosted by such ecosystems remain poorly understood given poor preservation and specificity of the available molecular, isotopic or fossilized signatures. Deep time paleobiological research therefore needs for new ways to unlock the history of the rare and variably preserved sedimentary rocks of these ages, by looking for new proxies that could help characterizing microbial ecosystems and better understand the co-evolution of the geosphere and the biosphere.

We here attempt to describe trace metal signatures of a modern, arsenic-rich lacustrine microbial mat fueled by oxygenic and anoxygenic photosynthesis as an analog to better understand how microbial mats and their sedimentary and chemical signatures can be preserved in the Archean sedimentary record. We coupled in-situ imaging of a microbial mat from modern Dead Sea shore with SEM, Raman spectroscopy, and X-ray mapping, to (meta)genomics data and chemical analyses. Arsenic enrichments in the anoxygenic photosynthetic layer of the mat reached a 10’000-fold level, and was associated to Mg-Si-rich EPS. The latter ultimately mineralized into aragonite clusters with a co-enrichment of Sr, Mn and Mo. At the mat scale, the mineralized zone (rich in Fe, Sr and Ca from authigenic calcium carbonates and detrital clay) is clearly located above the As-enrichment layer, in association with Mn. These data support a chemically dynamic microbial mat where microbial activity, EPS chemical affinity and environmental processes lead to specific organic and mineralized chemical signatures linked to metabolic activity. Metagenomics and synchrotron-based speciation analyses shall confirm the links between elemental enrichments and the microbial metabolic pathways.

We parallel this study to a well characterized microbial system of the Archean, the stromatolitic units of the Tumbiana Lake (2.72 Ga, Pilbara, Western Australia). In this environment, microbial mat accretionary behaviour has formed limestone stromatolites harboring layered nanopyrites embedded in carbonaceous material and chlorite (Marin-Carbonne et al., 2018). C, N and S isotopes of mineral fractions have suggested a connection of photosynthetic activity, sulfate reduction and methane cycling, potentially influenced by arsenotrophy (e.g. Thomazo et al., 2009; Sforna et al., 2014; Lepot et al., 2019). This is likely the most diverse undisputed microbial environment of the Archean. Our trace-elemental mapping using PIXE suggests co-enrichment of Mo and As in association to the nanopyrite-OM layer, that could be attributed to arsenotrophic and anoxygenic photosynthetic activity, in a similar fashion than argued for in the Dead Sea mat. Simulated diagenesis experiments are planned and should be able to provide chemical insights into the transformation of microbial mats to their fossilized counterparts at the microscale, to further validate the promises of metal biosignatures for reconstructing Archean ecosystems.