Abstract
Archaea synthesize membranes of isoprenoid lipids that are ether-linked to glycerol-1-phosphate (G1P), while Bacteria/Eukarya produce membranes consisting of fatty acids ester-bound to glycerol-3-phosphate (G3P). This dichotomy in membrane lipid composition (i.e., the ‘lipid divide’) is believed to have arisen after the Last Universal Common Ancestor (LUCA). A leading hypothesis is that LUCA possessed a heterochiral ‘mixed 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 encode a putative archaeal pathway for ether-bound isoprenoid membrane lipids in addition to the bacterial fatty acid membrane pathway. Key genes were expressed in the environment and their recombinant expression in Escherichia coli resulted in the formation of a ‘mixed archaeal/bacterial membrane’. Genomic evidence and biochemical assays suggest that the archaeal-like lipids of members of the FCB group could possess either a G1P or G3P stereochemistry. Our results support the existence of ‘mixed membranes’ in natural environments and their stability over a long period in evolutionary history, thereby bridging a once-thought fundamental divide in biology.
Highlights
These authors contributed : Laura Villanueva, F
We present the discovery of living bacteria of the phylum Candidatus Cloacimonetes of the Fibrobacteres–Chlorobi–Bacteroidetes (FCB) group superphylum, which are highly abundant in the deep anoxic waters of the Black Sea, harboring a putative ‘mixed archaeal/bacterial membrane’
To determine the presence and expression of the geranylgeranylglyceryl phosphate (GGGP) synthase, DGGGP synthase, and polyprenyl synthase coding genes, PCRs targeting a fragment of the genes were tested with DNA and cDNA from the Suspended particulate matter (SPM) samples recovered at 1000 and 2000m depth from the Black Sea 2013 campaign as a template with the same PCR master mix as described above but with half amount of dNTPs and Taq Polymerase
Summary
These authors contributed : Laura Villanueva, F. [35]) and Lokiarchaeota of the Asgard superphylum, contain archaeal lipid biosynthesis genes alongside bacterial-like fatty acid and ester-bond formation genes, but seem to lack the capacity to synthesize the G1P backbone via glycerol-1-P-dehydrogenase (G1PDH), while they do have the genetic ability to produce G3P [36] This observation is exciting as the Asgard archaea are currently considered as the closest descendants of the archaeal ancestor leading to eukaryotes [37]. There is no further evidence to date that the presence of these genes in those two archaeal groups leads to the synthesis of ‘mixed membranes’, i.e., membranes containing both ‘bacterial’ fatty acid ester-linked lipids and ‘archaeal’ isoprenoid ether-linked lipids, either heterochiral (containing G1P and G3P) or homochiral Taken together, these observations expose a ‘lipid divide’ that is not as clearcut as originally thought. Cloacimonetes genomes, and in other genomes of the FCB group superphylum and related candidate phyla, indicating that the ability to produce ‘mixed membranes’ might be widespread in the tree of life
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