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Start of funding 01.01.2011

The role of sulfur in a primordial arsenic biochemical pathway

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Life as we know it today requires phosphorus. Arsenic, which lies directly below phosphorus in the periodic table, shows sufficient chemical similarity that many organisms try to substitute arsenate for phosphate, but it is a poison to most organisms. However, recently, microorganisms have been isolated from Mono Lake - an arsenic- and sulfide-rich, oxygen-depleted, hypersaline lake - which can utilize arsenate as electron acceptor. As Mono Lake reflects primordial conditions the question arose, whether As-metabolizing life indicates that arsenic had an important biological role prior to the evolution of modern photosynthesis. We postulate that such an early arsenic cycle would have been significantly affected by sulfur. Instead of a direct oxidation of arsenite to arsenate, we propose that arsenite in sulfidic environments reacts more readily with polysulfides to yield thioarsenates which in turn can be transformed to arsenate. Identifying reaction pathways and rates of thioarsenate formation and degradation will elucidate basic mechanisms of energy gain for primitive microorganisms and yield valuable information about the development of early and potentially extraterrestrial life.

Final report:
In 2011 and 2012 we conducted research at Mono Lake, an alkaline terminal lake in California, representing primordial (“early Earth”) conditions. In detail, we investigated the role of arsenic as energy source for primitive microorganisms and the arsenic tolerance at higher trophic levels, such as Picocystis (phytoplankton) and the endemic Brine Shrimps.

Previous studies postulated that prior to formation of free oxygen microorganisms oxidized arsenite to arsenate via anoxygenic photosynthesis and created a redox cycle which delivered energy for other organisms. Our studies showed that under primordial conditions the arsenic cycle was closely coupled to the sulfur redox cycle and that arsenate was not directly microbially formed from arsenite. Rather, oxidation of sulfur lead to formation of polysulfides, forming monothioarsenate abiotically with arsenite. We were able to show that monothioarsenate is used by anaerobic arsenate reducers (strain MLMS-1) and anaerobic arsenite oxidizers (strain MLHE-1) for growth, indicating that sulfur rather than arsenic played a central role in the development of early life. Incubation experiments further showed lower arsenic uptake at higher tropic levels, such as Picocystis and Brine Shrimps, when those were exposed to aqueous thioarsenates instead of arsenite or arsenate. The presence of sulfur and its complexation of arsenic might thus also have created better starting conditions for the development of life at higher trophic levels in primordial arsenic-rich waters.

The data obtained in the present project are currently processed in three PhD and one master thesis. Two publications and a proposal to the DFG are in preparation.