Combined Genomic and Imaging Techniques Show Intense Arsenic Enrichment Caused by Detoxification in a Microbial Mat of the Dead Sea Shore

Abstract

Microbial mats and microbialites are essential tools for reconstructing early life and its environments. To better understand microbial trace element cycling, a microbial mat was collected from the sinkhole systems of the western shores of the Dead Sea, a dynamic environment exhibiting diverse extreme environments. Intense arsenic enrichment was measured (up to 6.5 million times higher than current concentrations in water, and 400 times the bulk concentration in the mat). Arsenic was found predominantly as As(V) in organic molecules, as shown by XANES spectra and high-resolution elemental mapping. Arsenic cycling genes obtained from metagenomic analysis were associated with arsenic detoxification, supporting an active mechanism of As(V) uptake, As(III) efflux and organoarsenic accumulation in the extracellular polymeric substances (EPS) of the mat. Thus, we propose that such localized As enrichment can be attributed to a transient increase in As(V) concentrations in the circulating subsurface water of the Dead Sea shore and its subsequent incorporation into organoarsenic molecules through microbial detoxification processes. Our data set supports the possibility of metalloid enrichment recorded in very localized facies due to rapid geogenic fluctuations in the chemistry of the water flowing over a biofilm. In this context, this example calls for caution in interpreting metal(loid) enrichment in organic matter-rich layers and microbialites of Paleoproterozoic origin. Arsenic signatures in Precambrian organic matter and carbonate rocks may host biosignatures, including evidence for extracellular polymeric substances, As-binding and detoxification processes, without supporting arsenotrophy. However, they provide clues to better assess the paleoenvironmental conditions at the time of microbial mat formation.