Fungal-Mineral Interaction: Astrobiology Insights from Iron-Rich Mineral Alteration by an Extremophile Black Fungus.

Iron-rich minerals, such as hematite (α-Fe2O3), are prominent constituents of the Martian surface; they are considered to be potential indicators of past aqueous activity and habitability. This study investigated the interaction between the extremophilic black fungus Rhinocladiella similis LaBioMMi 1217 and hematite under simulated laboratory conditions on Mars, focusing on redox-mediated dissolution processes, metabolic adaptations, and biosignature formation. The fungus was cultivated with powdered and polished hematite substrates, and mineral alteration was monitored through physicochemical measurements and scanning electron microscopy (SEM). Genome mining was performed to identify and map genes involved in iron metabolism. The metabolic profile of the fungus under hematite treatment was assessed via untargeted metabolomics. Over 15 days, the cultures exhibited marked acidification (pH decreased from 7.0 to 4.7) and a 10-fold increase in the dissolved Fe2+ ion concentration (26-270 mg/L), indicating metabolically driven iron reduction. SEM revealed surface etching and localized roughening consistent with microbially induced weathering, whereas these changes were absent in the abiotic controls. Genes linked to siderophore biosynthesis (sidA, sidC, sidD, sidF, sidH, sidI, and sidL) and reductive iron assimilation (FET3, FTR1, and FRE1) were identified. Untargeted metabolomics confirmed the secretion of organic acids, iron-chelating siderophores (e.g., ferrichrome C), and redox-active aromatic compounds in the presence of hematite, supporting a multifaceted strategy that combines acidification, chelation, and redox mediation. Collectively, these results show that the fungus actively promotes hematite dissolution through organic molecule-mediated mechanisms. Such interactions hold astrobiological relevance, as fungal modification of hematite might lead to the production of diagnostic chemical and mineralogical biosignatures, informing future life-detection strategies on Mars.