BAGEL · Bacterial Formation of Glycerol (di)Ether Lipids: Biogeochemical, (paleo)environmental and evolutionary implications

Bacterial Formation of Glycerol (di)Ether Lipids: Biogeochemical, (paleo)environmental and evolutionary implications

In this project, we investigated in detail the first isolate of marine mesophilic sulphate-reducing bacterium (SRB) able of producing non-isoprenoid dialkyl glycerol diethers (DGD) (strain 1), and compared this microorganism with other bacterial strains able to produce related lipid structures. These lipids exhibit an intriguing combination of structural characteristics of Bacteria and Archaea and have mostly been reported in extremophilic bacteria, while they are widespread in non-extreme actual and ancient ecosystems. The reasons why ether lipid biosynthesis has evolved in bacteria are presently unknown. The presence of such lipids in mesophilic bacteria may help elucidating some more details of the early events in the evolution of cellular life, including the divergence of Archaea and Bacteria. For this purpose, we have combined organic geochemistry (analysis of lipid biomarkers) with microbial ecology (bacterial ecophysiology based on ultrastructure) approaches, and applied them to living and/or decaying bacteria in relation to various environmental parameters. Following the objectives that were initially planned based on strain 1, a second strain (strain 2) of mesophilic SRB was also shown to produce non-isoprenoid DGD. Both strains were thus considered for studying the production of alkylglycerols, especially in relation to various parameters such as salinity and nutrient limitation (phosphorus and nitrate). Moreover, the influence of oxygen on the long-term stability of alkylglycerol lipids and cell ultrastructure of alkylglycerol-forming bacteria was also investigated. Our results showed that different nutrient (P and N-limitation) and salinity stressing conditions induce variable responses in cell ultrastructure and lipid content. Most important changes were observed under low salinity and nitrogen concentrations, under which mono- and dialkylglycerols (MGM and DGD) seem to play a similar role than classical fatty acids in membrane adaptation. However, the potential role of alkylglycerols, and to a lesser extent fatty acids, in membrane adaptation to P-limitation was evidenced for strain 1 only. This suggests that the physiological response to P-limitation is specific to any physiologically-distinct bacterial strain, even for phylogenetically-close species. Exposure to oxygen for several days to months of cells of strain 2 not only showed a complete preservation of DGD but also suggested that these lipids did not play a role in maintaining membrane integrity during an oxidative stress. However, the unexpected long-term preservation of cells under oxygenated conditions would suggest alternative mechanisms that protect cells from oxidative damage. Cells showed an atypical division process, i.e., initiated by invagination leading to two subsequent cytoplasmic spaces within a unique outer membrane, which resembles that observed in the archaeon, Ignococcus hospitalis. This latter shares similarities with strain 2 in terms of lipid composition and cell division mode. Such unique membrane specificity might constitute an evolutionary link between Archaea and Bacteria. While studying the influence of the growth substrate on the alkylglycerol composition of strains 1 and 2, we observed the unprecedented accumulation of wax esters (WE) in cells grown on n-alkyl compounds (e.g., unsaturated hydrocarbons, primary alcohols). So far, this metabolic process has been widely studied in aerobic prokaryotes and facultative anaerobic eukaryotes (e.g., Euglena gracilis) but has never been shown to occur in strictly anaerobic microorganisms. In addition to WE, thiowax esters (TWE) were also identified among cellular lipids of strains 1 and 2; such organic sulfur compounds have never been observed to be formed by bacteria under natural conditions. The ability to produce WE and TWE seems thus to be a characteristic of specific mesophilic SRB. Our findings open new perspectives for the search of biocatalytic potential of WE and TWE.

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