Cell-type-specific expression of a DCYTB ortholog enables the choanoflagellate Salpingoeca rosetta to utilize ferric colloids

The dynamic life histories of microeukaryotes present a challenge for determining their role in the nutrient cycles that support marine ecosystems. For instance, cellular differentiation is one life history strategy that enables a single celled microeukaryotic species to produce morphologically and physiologically distinct types of cells with different ecological functions. Here we report that cell differentiation in the marine choanoflagellate Salpingoeca rosetta endows one of its cell types with the ability to utilize insoluble ferric colloids for improved growth through the expression of a cytochrome b561 iron reductase ( cytb561a ). This gene is an ortholog of the mammalian duodenal cytochrome b561 ( DCYTB ) that reduces ferric cations prior to their uptake in gut epithelia and is part of an iron utilization toolkit that choanoflagellates and their closest living relatives, the animals, inherited from a last common eukaryotic ancestor. In a database of oceanic metagenomes, the abundance of cytb561a transcripts from choanoflagellates positively correlates with upwellings, which are a major source of ferric colloids in marine environments. As this predominant form of iron is largely inaccessible to cell-walled microbes, choanoflagellates and other phagotrophic eukaryotes may serve critical ecological roles by first acquiring ferric colloids through phagocytosis and then cycling this essential nutrient through iron utilization pathways. These findings provide insight into the ecological roles choanoflagellates perform and may inform reconstructions of early animal evolution where functionally distinct cell types became an integrated whole at the origin of animal multicellularity.