Archaea synthesize membranes of isoprenoid lipids that are ether-linked to glycerol, while Bacteria/Eukarya produce membranes consisting of ester-bound fatty acids. This dichotomy in membrane lipid composition or 'lipid divide' is believed to have arisen after the Last Universal Common Ancestor (LUCA). A leading hypothesis is that LUCA possessed a 'mixed heterochiral archaeal/bacterial membrane', however no natural microbial representatives supporting this scenario have been shown to exist today. Here, we demonstrate that bacteria of the Fibrobacteres-Chlorobi-Bacteroidetes (FCB) group superphylum and related candidate phyla encode a complete pathway for archaeal membrane lipid biosynthesis in addition to the bacterial fatty acid membrane pathway. Key genes were expressed in the environment and their recombinant expression in E. coli resulted in the formation of a 'mixed archaeal/bacterial membrane'. Our results support the existence of 'mixed membranes' in natural environments and their stability over large evolutionary timescales, thereby bridging a once-thought fundamental divide in biology.