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

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. Protein divergence between the two Galdieria taxa is similar to that between human and teleost fishes (Figure 1A) and about twice that between the unicellular green alga Chlamydomonas reinhardtii and its multicellular sister Volvox carteri (Figure S1A, see Supplemental Information). This suggests that genome-wide impacts of adaptation to different environments should be discernible in the Galdieria genomes. Comparison of genome data from Cyanidiophytina with complete (Porphyridium purpureum [7]) or partial (Calliarthron tuberculosum and Porphyra umbilicalis) genome data from mesophilic Rhodophytina shows that of the 6801 orthologous gene families present in the most recent common ancestor of Rhodophyta (Figure 1B), 1448 were lost in the Cyanidiophytina common ancestor, compared to 456 in Rhodophytina. This pattern is most evident in Cyanidioschyzon merolae that underwent 1312 additional gene losses resulting in a gene-poor lineage (4775 nuclear protein coding genes) [8] restricted to aqueous environments [9]. Given severe genome reduction, we postulated that HGT provides a mechanism to gain adaptive functions in G. phlegrea. Consistent with this idea, BLASTp and phylogenetic analysis of the G. phlegrea predicted proteins turned up 11 instances of prokaryote-derived HGT unique to this taxon within Cyanidiophytina (Figures S1B–S1G). These transferred genes include seven urease genes (i.e., UreA– G; Figures S1C–S1G) that encode all components of urease, a multi-subunit enzyme that catalyzes the hydrolysis of urea into carbon dioxide and ammonia. This reaction provides an alternative source of nitrogen in N-limited environments. In eubacteria, the seven genes are typically encoded in a single operon (Figure 1C). However, in G. phlegrea, urease genes are located on independent DNA contigs except for the linked UreB and UreC (Figure S1C). Phylogenetic analysis shows that all urease genes have a eubacterial 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 …