Methylation of Archaeal Lipid Backbone as a Strategy to Face Energy Limitation

Abstract:

A recent census of the biomass on Earth revealed that microorganisms are the second largest contributors of biomass, predominantly inhabiting deep biosphere environments. These intriguing findings pose an intellectual challenge to natural scientists. How can life sustain in such hostile environments where energy and nutrients are scarce? Among the adaptation options available to microorganisms, membrane lipid modification is a common mechanism for prokaryotes to adapt to external stresses by, for example, regulating the number of double bounds or rings in the aliphatic part of the lipids. Recently, a novel group of archaeal membrane lipids, the butanetriol and pentanetriol dialkyl glycerol tetraethers (BDGTs and PDGTs respectively), were discovered in marine sediments. Unlike the most common archaeal lipids – the so-called glycerol dibiphytanyl glycerol tetraethers (GDGTs) – the new lipid types possess one or two additional methyl groups on the molecule backbone. They were predominantly observed in anoxic environments as well as in the methanogen Methanomassiliicoccus luminyensis. However, neither their role in the membrane nor their biosynthetic pathway have been elucidated so far. In this study, the use of position specific stable isotope labelling and analysis by high resolution mass spectrometry revealed that BDGTs and PDGTs in M. luminyensis are the result of post-synthesis methylations of regular GDGTs. This methylation is likely performed by one or two radical-SAM enzyme(s) which were investigated through bioinformatics study of the genomes of M. luminyensis and of relative strains. Eventually, the degree of backbone methylation was compared in M. luminyensis and in a set of marine sediments sampled in the Mediterranean Sea and Black Sea. The relative abundance of PDGTs was found to increase with growth stage and with sediment age. We thus hypothesize that backbone methylation(s) could be an adaptive trait developed by certain Archaea to cope with energy and/or nutrient limitation.