Pumping Iron: A Multi-omics Analysis of Two Extremophilic Algae Reveals Mechanisms of Iron Economy

Marine algae are responsible for half of the world’s primary productivity, but this critical carbon sink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, is remarkable for its ability to maintain photosynthesis and thrive in low-iron environments. A related species, Dunaliella salina Bardawil, shares this attribute but is an extremophile found in hyper-saline environments. To elucidate the strategies that marine algae deploy to manage their iron requirements, we produced high quality genome assemblies and transcriptomes for both Dunaliella species to serve as a foundation for a comparative multi-omics analysis. We identified a host of iron-uptake proteins in both species that includes a massive expansion of iron-binding transferrin proteins and a novel family of siderophore-iron uptake proteins. Complementing these multiple iron-uptake routes, ferredoxin functions as a large iron reservoir that can be released by replacement of ferredoxin with flavodoxin. Our analysis revealed reduced investment in the photosynthetic apparatus coupled with remodeling of antenna proteins by dramatic iron-deficiency induction of TIDI1, an LHCA-related protein found also in other chlorophytes. These combinatorial iron scavenging and sparing strategies make Dunaliella unique among photosynthetic organisms.