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.