Distribution and abundance of tetraether lipid cyclization genes in terrestrial hot springs reflects pH

Abstract

Many Archaea produce membrane-spanning glycerol dibiphytanyl glycerol tetraether (GDGTs) lipids that serve as unique biomarkers of past environments. These lipids can contain up to eight cyclopentane rings, where an increase in ring cyclization is generally associated with growth in more acidic, higher temperature, or more energy limited conditions. Recently the genes that encode GDGT ring synthases, grsAB, were identified and characterized in model thermoacidophiles Sulfolobus acidocaldarius and Saccharolobus solfataricus. However, the distribution and abundance of grs homologs across environments inhabited by these and related Archaea remains unknown. To address this, we examined the distribution of grs homologs in archaeal and bacterial cultivar genomes, single cell genomes, metagenomes, and metatranscriptomes from thermal springs across the planet, where temperature, pH, and geochemical data take at time of sampling. The relative abundance of grs in these microbial communities exhibits a strong negative correlation with pH, and weak positive correlation with temperature. Genomes and metagenome-assembled genomes (MAGs) from Archaea that encode two or more copies of grs are significantly more widespread in low pH springs. Homologs of grs were detected in MAGs from 12 archaeal classes, with the most well-represented being the Thermoproteia. Homologs of grs were also detected among several classes of uncultured Archaea, including the Korarchaeia, Bathyarchaeia, and Hadarchaeia. Several Nitrososphaeria MAGs had high copy numbers of grs (> 3), and the functional role of these copies cannot yet be explained. Notably, grs genes were also found in MAGs from the bacterial class Acidobacteria. Based on phylogenetic analyses, it is likely that Acidobacteria acquired these genes horizontally from Archaea. Broadly, our results highlight the key role of grs-catalyzed lipid cyclization in the diversification of Archaea in hot and acidic environments.