A light-sensing system in the common ancestor of the fungi

Abstract

Diverse light-sensing organs (i.e., eyes) have evolved across animals. Interestingly, several subcellular analogs have been found in eukaryotic microbes.1 All of these systems have a common "recipe": a light occluding or refractory surface juxtaposed to a membrane-layer enriched in type I rhodopsins.1-4 In the fungi, several lineages have been shown to detect light using a diversity of non-homologous photo-responsive proteins.5-7 However, these systems are not associated with an eyespot-like organelle with one exception found in the zoosporic fungus Blastocladiella emersonii (Be).8Be possesses both elements of this recipe: an eyespot composed of lipid-filled structures (often called the side-body complex [SBC]), co-localized with a membrane enriched with a gene-fusion protein composed of a type I (microbial) rhodopsin and guanylyl cyclase enzyme domain (CyclOp-fusion protein).8,9 Here, we identify homologous pathway components in four Chytridiomycota orders (Chytridiales, Synchytriales, Rhizophydiales, and Monoblepharidiales). To further explore the architecture of the fungal zoospore and its lipid organelles, we reviewed electron microscopy data (e.g., the works of Barr and Hartmann10 and Reichle and Fuller11) and performed fluorescence-microscopy imaging of four CyclOp-carrying zoosporic fungal species, showing the presence of a variety of candidate eyespot-cytoskeletal ultrastructure systems. We then assessed the presence of canonical photoreceptors across the fungi and inferred that the last common fungal ancestor was able to sense light across a range of wavelengths using a variety of systems, including blue-green-light detection. Our data imply, independently of how the fungal tree of life is rooted, that the apparatus for a CyclOp-organelle light perception system was an ancestral feature of the fungi.