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Some microbial eukaryotes, such as the extremophilic red alga Galdieria sulphuraria, live in hot, toxic metal-rich, acidic environments. To elucidate the underlying molecular mechanisms of adaptation, we sequenced the 13.7-megabase genome of G. sulphuraria. This alga shows an enormous metabolic flexibility, growing either photoautotrophically or heterotrophically on more than 50 carbon sources. Environmental adaptation seems to have been facilitated by horizontal gene transfer from various bacteria and archaea, often followed by gene family expansion. At least 5% of protein-coding genes of G. sulphuraria were probably acquired horizontally. These proteins are involved in ecologically important processes ranging from heavy-metal detoxification to glycerol uptake and metabolism. Thus, our findings show that a pan-domain gene pool has facilitated environmental adaptation in this unicellular eukaryote.

The thermoacidophilic, unicellular, red alga Galdieria sulphuraria possesses characteristics, including salt and heavy metal tolerance, unsurpassed by any other alga. Like most plastid bearing eukaryotes, G. sulphuraria can grow photoautotrophically. Additionally, it can also grow solely as a heterotroph, which results in the cessation of photosynthetic pigment biosynthesis. The ability to grow heterotrophically is likely correlated with G. sulphuraria's broad capacity for carbon metabolism, which rivals that of fungi. Annotation of the metabolic pathways encoded by the genome of G. sulphuraria revealed several pathways that are uncharacteristic for plants and algae, even red algae. Phylogenetic analyses of the enzymes underlying the metabolic pathways suggest multiple instances of horizontal gene transfer, in addition to endosymbiotic gene transfer and conservation through ancestry. Although some metabolic pathways as a whole appear to be retained through ancestry, genes encoding individual enzymes within a pathway were substituted by genes that were acquired horizontally from other domains of life. Thus, metabolic pathways in G. sulphuraria appear to be composed of a `metabolic patchwork', underscored by a mosaic of genes resulting from multiple evolutionary processes. Substitution of genes encoding pathway enzymes also extends to metabolic pathways in other eukaryotic organisms. Specifically, de novo NAD+ biosynthesis in eukaryotes, including those possessing a plastid, has been subjected to numerous gene transfer events, some of which were responsible for the establishment of novel metabolic pathways in plastid-bearing eukaryotes. Another characteristic of G. sulphuraria is observed when cultivating the alga in a liquid medium. Under light limiting conditions, G. sulphuraria excretes porphyrins, which fluoresce when illuminated with near-UV wavelengths of light. Examination of the absorption and emission (fluorescence) spectra of the porphyrin mixture led to the hypothesis of spectral shifting, whereby near-UV light that is unusable for photosynthesis is converted into light readily absorbed by phycocyanin, a photosynthetic pigment synthesized by G. sulphuraria. The calculated relative fluorescence quantum yield, i.e., the efficiency at which absorbed photons are re-emitted as fluoresced light, of the excreted porphyrins was lower than to be expected for counteracting light limiting conditions, possibly indicating a different biological function for porphyrin excretion in G. sulphuraria.