Iron acquisition strategies of the rock-inhabiting fungus Knufia petricola reveal vulnerability to chelator-based mitigation

Abstract

Fungal iron acquisition has mostly been studied for pathogens living in competitive environments where securing iron from the host is critical for proliferation. How fungi from stress-rich but competition-free material surfaces handle iron uptake is, however, unknown. We studied these processes in rock-inhabiting fungi, known for their constitutive melanin-production, extremotolerant lifestyle and colonization of exposed surfaces such as solar panels and marble monuments, by choosing Knufia petricola to represent this group. The characterization of targeted mutants showed that K. petricola produces an extracellular - yet undefined - siderophore on which it relies less than on the ferroxidase-iron permease complex for reductive iron assimilation. By disrupting melanin synthesis, it was demonstrated that this pigment can reduce and adsorb iron but nevertheless does not contribute significantly to iron acquisition. Moreover, growth towards an iron source was found to be siderophore-dependent. Ferric citrate could not be directly assimilated. Finally, it was found that K. petricola and other rock-inhabiting fungi exhibited high sensitivity to strong iron chelators such as EDTA. These observations not only offer a potential mitigation strategy for preventing fungal colonization of subaerial materials using iron chelators, but also highlight the specialized adaptations of these fungi to low-competition environments. ImportanceThe rock-inhabiting fungus Knufia petricola acquires iron primarily via reductive iron assimilation, independently of the iron-adsorbing and -reducing melanin. Its siderophore, although extracellular and allowing chemotropism towards an iron source, is not able to obtain iron from strong iron chelators such as BPS and EDTA. This sensitivity to iron sequestration opens avenues to mitigate the fungal colonization of materials such as solar panels.