Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea

Summary Thriving in the hot, acidic, and metal-rich environments associated with geothermal areas is possible for only a few eukaryotes, with the Cyanidiophytina red algae ( Cyanidium , Galdieria , and Cyanidioschyzon ) being a famous example. These unicellular taxa can live in pH 0–4 and temperatures reaching up to 56°C [1,2]. Because Cyanidiophytina is sister to a vast array of mesophilic red algae (the Rhodophytina), such as the unicellular Porphyridium and the seaweed Chondrus [3], the genetic basis of their adaptation to extreme environments is of great interest from both the perspective of biotechnology and of evolution. The recently completed 13.7 Mbp genome sequence from the hot-spring dwelling Galdieria sulphuraria demonstrated that horizontal gene transfer (HGT) from prokaryotic sources provided this taxon with remarkable metabolic versatility ( e.g ., glycerol metabolism) and the ability to survive in its hostile environment ( e.g. , genes to detoxify mercury and arsenic) [4]. To explore the role of HGT in other members of this genus, we generated an 11.4 Mbp draft genome assembly from the sister taxon G. phlegrea DBV 009 [5]. In contrast to G. sulphuraria, this species is adapted to dry habitats near fumaroles such as fissures between rocks or cryptoendolithic environments [5,6]. Here, we provide evidence for extensive gene loss in the common ancestor of Cyanidiophytina that includes the eukaryote-derived loci required for urea utilization. Surprisingly, we find that G. phlegrea has regained the complete set of genes required for urea hydrolysis through HGT from eubacteria. The unlinked nature of these genes is likely explained by multiple gene transfers that resulted in assembly of the pathway in G . phlegrea . Our study demonstrates that genome reduction, a common outcome in eukaryotes for adaptation to a specialized niche, can be ameliorated by the gain of once lost, or novel functions through HGT.