Siderophore production by the lichen fungus Xanthoria parietina supports its algal symbiont.

Abstract

Lichens are symbiotic associations between a fungal mycobiont and a photosynthetic photobiont. They thrive in nutrient-poor environments; yet the mechanisms underlying their adaptation to iron limitation remained largely unknown. Here, we characterize the iron acquisition system of Xanthoria parietina, a globally distributed lichen-forming fungus associated with the microalgal photobiont Trebouxia decolorans. We demonstrate that the mycobiont produces the siderophore ferrichrome and possesses the full genetic repertoire not only for siderophore biosynthesis, but also reductive iron assimilation, iron detoxification, and regulation. The ferrichrome-synthesizing non-ribosomal peptides synthetase exhibits a lichen-specific compact architecture but retains functionality when heterologously expressed in a non-lichenized ascomycete. Transcriptomic analysis and ferrichrome quantification reveal substrate-dependent regulation of the siderophore system. Importantly, ferrichrome promotes photobiont growth independent of extracellular iron reduction, indicating direct utilization. These findings provide the functional evidence of siderophore-mediated iron acquisition in a lichen symbiosis and highlight ferrichrome as a key mediator of mutualistic nutrient exchange.