Bridging the divide: bacteria synthesizing archaeal membrane lipids

Abstract

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.

Why the Lipid Divide? Membrane Proteins as Drivers of the Split between the Lipids of the Three Domains of Life

“…This elicits the question of why members of the bacterial FCB superphylum would carry genes to synthesize the lipids typically associated with archaeal membranes. Whether these genes were acquired horizontally at the base of the group or were always there since LUCA and have since been lost in all other groups, it remains an unusual example of heterotypic membranes that calls for an explanation.…”

“…A recent study reports that members of the bacterial Fibrobacteres/Chlorobi/Bacteroidetes (FCB) superphylum contain an almost complete set of genes for synthesizing archaeal membrane lipids, in addition to the traditional bacterial lipids . The initial results came from a metagenomic study of strains that are yet to be cultured in the laboratory, but were then shown to extend to multiple members of the FCB superphylum sequenced previously.…”

“…Separate results have since confirmed the presence of the full archaeal lipid‐biosynthesis machinery in multiple members of the FCB group, including homologs of the lipid headgroup‐synthesizing enzyme sn ‐glycerol‐1‐phosphate dehydrogenase (G1PDH) in Fibrobacteres . Moreover, expressing the relevant genes heterologously in E. coli produced archaeal‐like lipids, even in the absence of any known G1PDH homologs . The original cells themselves, however, are yet to be grown in the laboratory, so additional experimental tests are needed to determine exactly how archaeal‐like the lipids of these bacteria are, and how much of them the membranes contain.…”

“…However, this would make the host unlike any archaeon known at present. No such case is known in bacteria either: the members of the FCB superphylum that carry genes to synthesize archaeal‐like lipids retain those for the traditional bacterial lipids as well …”

Resolving the origins of membrane phospholipid biosynthesis genes using outgroupfree rooting

“…In these species lacking G1PDH, it is unclear whether GGGPS and DGGGPS are active and if so, what they are used for; one possibility is that they catalyse the reverse reaction, catabolising archaeal lipids as an energy source. However, a very recent report (Villanueva et al 2018) has shown that the GGGPS and DGGGPS genes from one FCB lineage, Cloacimonetes, support the production of archaeal-type membrane phospholipids and a mixed membrane when heterologously expressed in E. coli. This suggests that both E. coli and perhaps Cloacimonetes have an alternative, as yet unknown mechanism for making G1P, and that some FCB members may have mixed archaeal and bacterial membranes Orthologues of the canonical bacterial genes are less widespread in Archaea (Table 1).…”