Life in hot acid: a genome‐based reassessment of the archaeal order Sulfolobales

Abstract

The order Sulfolobales was one of the first named Archaeal lineages, with globally distributed members from terrestrial thermal acid springs (pH < 4; T > 65 C). The Sulfolobales represent 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, Stygiolobus and Sulfurisphaera) and iron oxidation (Acidianus, Metallosphaera, Sulfurisphaera, Sulfuracidifex and Sulfodiicoccus) 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, dox and a new putative cytochrome bd) are prevalent in many species (even facultative/obligate anaerobes), suggesting a key role for oxygen among the Sulfolobales. The presence of fox genes 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 reorganization efforts are supported by the comparative genomics here, although several changes are proposed, including the expansion of the genus Saccharolobus.

New insights into the diversity and evolution of the archaeal mobilome from three complete genomes of Saccharolobus shibatae

“…Members of the order Sulfolobales are particularly abundant in such habitats and thrive in sulfuric thermal springs and solfataras around the globe (Kvist et al ., 2007; Kozubal et al ., 2012; Munson‐McGee et al ., 2018b; Liu et al ., 2019). The order Sulfolobales includes seven genera ( Acidianus , Metallosphaera , Saccharolobus , Sulfolobus , Sulfurisphaera , Stygiolobus , Sulfodiicoccus and Sulfuracidifex ) with more than 30 species in total (Counts et al ., 2020). Besides variation in optimal growth temperature (65–88°C) and pH (0.7–4.5), Sulfolobales members are characterized by different morphological and genetic features, and metabolic capacities, such as oxidation/reduction of sulfur and iron, oxygen tolerance, sugar catabolism, and more.…”

Physiology, Taxonomy, and Sulfur Metabolism of the Sulfolobales, an Order of Thermoacidophilic Archaea

“…Average amino acid identity (AAI) and conserved multi-locus sequence alignment (MLSA) also indicate that Sulfol. acidocaldarius is distinct from the other species of Sulfolobus ( Counts et al, 2021 ).…”

Metagenome Assembly and Metagenome-Assembled Genome of “ Candidatus Aramenus sulfurataquae” from Thermal Sediments from the Los Azufres Volcanic Complex

“…Previously, we obtained a genome assembly for the “ Candidatus Aramenus” genus from a hot spring metagenome from water samples (65°C, pH 3.6) ( 3 ). The phylogenetic relationship of the Aramenus genus within Sulfolobales has been investigated recently ( 4 ). Interestingly, current diversity studies have detected Aramenus archaea at the El Chichón volcano in Chiapas, Mexico ( 5 ).…”