A two-week journey to Mars: Investigating changes in thiophene-bearing quinones of the extremely thermoacidophilic archaeon Acidianus manzaensis

In the search for reliable biomarker in other planetary environments such as Mars, we need molecules that are stable over geological timescales while preserving indicative information about their potential biological origin. Thiophene-bearing quinones fulfill these requirements, and thiophenes, which are their basic moieties, have been found on Mars. However, thiophenes can be produced abiotically and have been found in meteorites. Furthermore, the Martian environment may alter their molecular structure over time. To evaluate whether there could be a distinction between biotically and abiotically produced thiohenes considering the harsh environmental conditions on Mars, we cultivated the extremophilic archaeon Acidianus manzaensis on ESA01-E Mars analog material. We then exposed the cell-mineral material to one month of desiccation and Mars-like conditions in a Mars simulation chamber to analyze changes in the composition of thiophene-bearing quinones using mass spectrometry-based metabolomics, and evaluated their potential for cell recovery after exposure to extreme conditions. Recultivations after one month of desiccation and two weeks of exposure to Mars-like conditions was successful, proving the durability of the organism and its potential for cell recovery. Analysis of their thiophene-bearing quinone composition showed a heterogeneous distribution of possible oxidation states used as an adaptation to environmental stressors. While additional analysis of the headgroup moieties might clarify the traces of biologically produced thiophene remnants, this study showed the durability of Acidianus manzaensis to recover after exposure to extreme conditions, paving the way for further investigation.