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ABSTRACT Presented are five genomes from the polyextremophilic (optimal temperature of >65°C and optimal pH of <3.5) archaeal family Sulfolobaceae , greatly expanding order-wide genomic diversity. Included are the only obligate anaerobic species, several facultative sulfur utilizers, two metal mobilizers, one facultative chemolithoautotroph with robust metabolic versatility, and some of the most thermophilic thermoacidophiles reported to date. 

ABSTRACT Thermoacidophilic archaea belonging to the order Sulfolobales thrive in extreme biotopes, such as sulfuric hot springs and ore deposits. These microorganisms have been model systems for understanding life in extreme environments, as well as for probing the evolution of both molecular genetic processes and central metabolic pathways. Thermoacidophiles, such as the Sulfolobales, use typical microbial responses to persist in hot acid (e.g. motility, stress response, biofilm formation), albeit with some unusual twists. They also exhibit unique physiological features, including iron and sulfur chemolithoautotrophy, that differentiate them from much of the microbial world. Although first discovered >50 years ago, it was not until recently that genome sequence data and facile genetic tools have been developed for species in the Sulfolobales. These advances have not only opened up ways to further probe novel features of these microbes but also paved the way for their potential biotechnological applications. Discussed here are the nuances of the thermoacidophilic lifestyle of the Sulfolobales, including their evolutionary placement, cell biology, survival strategies, genetic tools, metabolic processes and physiological attributes together with how these characteristics make thermoacidophiles ideal platforms for specialized industrial processes. 

The orderSulfolobaleswas one of the first named Archaeal lineages, with globally distributed members from terrestrial thermal acid springs (pH < 4;T > 65°C). TheSulfolobalesrepresent broad metabolic capabilities, ranging from lithotrophy, based on inorganic iron and sulfur biotransformations, to autotrophy, to chemoheterotrophy in less acidophilic species. Components of the 3‐hydroxypropionate/4‐hydroxybutyrate carbon fixation cycle, as well as sulfur oxidation, are nearly universally conserved, although dissimilatory sulfur reduction and disproportionation (Acidianus,StygiolobusandSulfurisphaera) and iron oxidation (Acidianus,Metallosphaera,Sulfurisphaera,SulfuracidifexandSulfodiicoccus) are limited to fewer lineages. Lithotrophic marker genes appear more often in highly acidophilic lineages. Despite the presence of facultative anaerobes and one confirmed obligate anaerobe, oxidase complexes (fox,sox,doxand a new putative cytochrome bd) are prevalent in many species (even facultative/obligate anaerobes), suggesting a key role for oxygen among theSulfolobales. The presence offoxgenes tracks with a putative antioxidant OsmC family peroxiredoxin, an indicator of oxidative stress derived from mixing reactive metals and oxygen. Extreme acidophily appears to track inversely with heterotrophy but directly with lithotrophy. Recent phylogenetic re‐organization efforts are supported by the comparative genomics here, although several changes are proposed, including the expansion of the genusSaccharolobus.