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

• Published in: Geochemistry, geophysics, geosystems : G3 Vol. 25; no. 3
• Main Authors: Thomas, C., Filella, M., Ionescu, D., Sorieul, S., Pollier, C. G. L., Oehlert, A. M., Zahajská, P., Gedulter, N., Agnon, A., Ferreira Sanchez, D., Ariztegui, D.
• Format: Journal Article
• Language: English
• Published: Washington John Wiley & Sons, Inc 01-03-2024; Wiley
• Subjects: Arsenic; biofilm; Biofilms; Carbonate rocks; Carbonates; Chemical analysis; Detoxification; Enrichment; Genes; geomicrobiology; Imaging techniques; metagenomics; Metals; Microbial mats; microbialite; Organic matter; Precambrian; Seawater; Sinkholes; Subsurface water; synchrotron; trace element; Trace elements; Water analysis; Dead Sea
• ISSN: 1525-2027; 1525-2027
• DOI: 10.1029/2023GC011239

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.
Plain Language Summary
Microbial mats and microbialites are like time machines helping us learn about ancient life and its environments. We collected a microbial mat from the unique Dead Sea’s sinkholes, where life thrives in extreme conditions. In this mat, we found for the first time in this area a staggering 6.5 million‐fold increase in arsenic, an element toxic to life. By closely studying the genes and chemistry of this microbial mat, we discovered that microbes were striving to clean up this excess arsenic in a sort of natural detoxification process. It seems that a temporary spike in arsenic levels in the Dead Sea water triggered this clean‐up work, which eventually stored the arsenic safely in the mat away from the microbial cells. Our findings suggest that in the past, when microbial mats were one of the only ecosystems on Earth, changes in the water flowing over mats like this one could have caused similar accumulations of metals. Therefore, when scientists study ancient fossilized microbial layers, these discoveries can help us look into the past and understand the chemical and biological conditions under which these ancient microbial mats formed.
Key Points
Intense arsenic enrichment is detected for the first time around the Dead Sea
Arsenic is accumulated in the organic matter of a microbial mat as methylated organoarsenic
The enrichment results from microbial detoxification and may be fossilized