The earliest evidence of life on our planet is arguably captured in early Paleoarchean fossil stromatolites and microbial mats. Today, stromatolites and microbial mats still thrive in certain extreme environments. Consequently, they are considered to be the oldest living and most resilient ecosystems known.

Most contemporary microbial mats and stromatolites are dominated by cyanobacteria, but the same ecosystems in the rock record predate oxygenic phototrophs by more than half a billion years. The lithification of microbial mats is due to the entire community metabolism including viruses, but the cyanobacteria (i.e., photosynthetic activity) play a critical role. The question arises how stromatolites formed during the first billion year of their dominance on Earth, before the presence of oxygen. Ferrous iron, hydrogen and sulfur can serve as electron donor for anoxygenic photosynthesis. However, evidence for these elements to support phototrophy is controversial in the Archean record.

Using a variety of geomicrobiological analyses, including optodes, synchrotron-based X-ray fluorescence and X-ray absorption near-edge structure, a role for arsenic cycling in Precambrian microbialites emerged: We found evidence for As metabolism in the 2.72-billion-year-old stromatolites (Tumbiana Formation, Pilbara). Sub-micrometer-size element maps indicated that not iron or sulfur but arsenic cycling was associated with organic carbon. A recent study in 3.48-billion-year-old stromatolite (Dresser Formation, Pilbara) confirmed the possibility of As cycling as a key metabolism. Furthermore, we located a modern microbial mat system in the southern Atacama Desert that was thriving under early-Earth like conditions. In the permanent absence of oxygen, cycling of sulfur and arsenic were coupled to calcium carbonate precipitation. Sulfide and arsenite oxidation were stimulated in the light and sulfate and arsenate reduction were major respiration pathways. Also, anaerobic methane oxidation was coupled to arsenate reduction in these anoxic mats. Thermodynamic calculations show that arsenic cycling is energetically preferred over sulfur when both elements are present. Interestingly, arsenic cycling has also a much greater potential to precipitate calcium carbonate, leading to more rapid stromatolite growth than sulfur cycling does.