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

ABSTRACT

Many Archaea produce membrane-spanning lipids that enable life in extreme environments. These isoprenoid glycerol dibiphytanyl glycerol tetraethers (GDGTs) may contain up to eight cyclopentyl and one cyclohexyl ring, where higher degrees of cyclization are associated with more acidic, hotter or energy-limited conditions. Recently, the genes encoding GDGT ring synthases, grsAB, were identified in two Sulfolobaceae; however, the distribution and abundance of grs homologs across environments inhabited by these and related organisms remain a mystery. To address this, we examined the distribution of grs homologs in relation to environmental temperature and pH, from thermal springs across Earth, where sequences derive from metagenomes, metatranscriptomes, single-cell and cultivar genomes. The abundance of grs homologs shows a strong negative correlation to pH, but a weak positive correlation to temperature. Archaeal genomes and metagenome-assembled genomes (MAGs) that carry two or more grs copies are more abundant in low pH springs. We also find grs in 12 archaeal classes, with the most representatives in Thermoproteia, followed by MAGs of the uncultured Korarchaeia, Bathyarchaeia and Hadarchaeia, while several Nitrososphaeria encodes >3 copies. Our findings highlight the key role of grs-catalysed lipid cyclization in archaeal diversification across hot and acidic environments.