A dominant subgroup of marine Bathyarchaeia assimilates organic and inorganic carbon into unconventional membrane lipids

Bathyarchaeia, an abundant and ecologically versatile archaea found commonly in marine sediments, has a key role in the global carbon cycle. However, its lipid biomarkers and carbon assimilation mechanisms are poorly understood. Here, using a highly enriched Bathyarchaeia culture (>95% archaea) obtained from estuarine sediment of the East China Sea, we show that Baizosediminiarchaeum (formerly subgroup Bathy-8), the most abundant and widespread Bathyarchaeia group on Earth, synthesizes butanetriol dialkyl glycerol tetraethers (BDGTs) as its dominant membrane lipids. BDGTs are unusual archaeal tetraether lipids characterized by a butanetriol backbone instead of the typical glycerol, challenging fundamental assumptions in archaeal lipid biochemistry. Although BDGTs have been previously identified in the methanogen Methanomassiliicoccus luminyensis, we now provide direct evidence that Bathyarchaeia also synthesizes BDGTs, definitively establishing this globally abundant group as a natural BDGT producer. Stable isotope probing with 13C-bicarbonate shows that Baizosediminiarchaeum assimilates carbon into BDGTs from both inorganic carbon and lignin. These unique carbon assimilation strategies suggest the biogeochemical importance of Baizosediminarchaeum in marine carbon cycling and organic matter decomposition. Baizosediminiarchaeum, a key player in the deep biosphere, builds butanetriol dialkyl glycerol tetraether (BDGT) membrane lipids and feeds on both CO2 and lignin, revealing a survival strategy in low-energy environments and a unique lipid biomarker for this group.