Colloidally dispersed nanoparticles: a convergent evolutionary approach for the secretion of apparently soluble melanin

ABSTRACT Melanin is a heterogeneous, amorphous biopolymer widely distributed in biological systems, yet most canonical forms are intrinsically insoluble. Soluble melanins are rare and remain poorly characterized, with pyomelanin and peptidomelanin representing the best-described fungal examples. Here, we report the isolation and characterization of a distinct, polyphyletic class of soluble melanin that we term ‘colloidal melanin’. This class of polymers was isolated from four different species of Ascomycetous fungi occupying varied environmental niches. Colloidal melanin was found to be phenolic and nitrogenous, with a low amino acid content. The polymers form particles with median diameters ranging from 79 to 127 nm, suggesting that small particle size may contribute to aqueous solubility via colloidal dispersion. Using chemical inhibition of melanin biosynthesis together with whole-genome sequencing, we show that colloidal melanin can be produced through multiple distinct biochemical pathways. Further, genes identified as involved in melanin biosynthesis across species do not share any detectable common ancestry, consistent with convergent evolution. Together, these findings identify a distinct class of soluble melanin that does not conform to existing soluble melanin classifications.