BActerial production of Glycerol (di)Ether Lipids : Biogeochemical, (palaeo)environmental and evolutionary implications – BAGEL

The BAGEL project involves three complementary partners and combines a unique set of methods (microbiology, lipid chemistry, electron microscopy, proteomics, phylogenomics, bioinformatics) to study in detail unprecedented bacterial strains capable of producing non-isoprenoid glycerol ethers, identical to those synthesized by hyperthermophilic bacteria. Pure bacterial biomass of anaerobic bacteria was grown under various conditions (variations of the physico-chemical parameters of the culture medium) and is actually being analyzed in detail using analytical chemistry and electron microscopy to understand the ecophysiological interest of glycerol ethers. The analysis and comparison of genomes of strains capable of producing or not glycerol ethers should allow identifying candidate genes involved in the biosynthesis of these specific lipids.

The first results obtained after 6 months of project are very promising. Studies are under development but some encouraging results already indicate: - Original biosynthetic pathways, showing similarities with eukaryotic cells, of bacterial glycerol ethers; the involvement of glycerol ethers in the adaptation of bacterial cells to changes in salinity, pH and temperature; the definition of a new index (based on some specific bacterial glycerol ethers) to reconstruct temperatures in ancient environments; the annotation of the first genome of a non-thermophilic bacterium capable of producing glycerol ethers. The value and the relevance of the BAGEL project have helped obtaining two additional research grants (one from the French ministery and one from Europe) to fund a PhD student and a post-doctoral fellow who will work full-time on the project starting from September 1st 2013.

The results obtained so far relate to various fundamental aspects of the biosynthesis and modes of formation of glycerol ethers in bacteria. Some applications can be considered in the context of biogeochemical and (paleo)environmental studies, including the use of certain glycerol ethers lipids produced by mesophilic bacteria as indicators of past environmental conditions.

Master 2 report (2013), Arnauld Vinçon-Laugier: Influence of environmental parameters and of the growth substrate on the lipid composition of mesophilic bacteria.

The three domains of life on Earth comprise the two prokaryotic groups Archaea and Bacteria. In addition to their distinct genetic composition, a major distinguishing feature between Archaea and Bacteria is the chemical composition of their cell-wall. Like in eukaryotes, bacterial phospholipids generally consist of a glycerol moiety linked to fatty acids via ester bonds (acylglycerols) whereas archaeal membrane lipids consist of isoprenoid chains bound to glycerol through ether bonds (isoprenoid ether lipids or alkylglycerols). Other major distinctive features are the stereochemistry of the glycerol backbone and the nature of the polar head group linked to glycerol. These differences in lipid structures confer variation in physical and physiological properties of the membranes of Bacteria and Archaea with potential implications in term of ecology and evolution. They are considered to have an ancient origin in the evolution of life on Earth, and may have originated from the divergence between the two prokaryotic domains.
Non-isoprenoid alkylglycerols constitute an exception to the aforementioned chemical distinctions as they exhibit an intriguing combination of structural characteristics of Bacteria/Eucarya and Archaea. Compounds with one ether-linked alkyl chain and one ester-bound fatty acid (monoalkyl/monoacyl glycerols or GMM) have been detected in some aerobic and anaerobic bacteria and are widespread in eukaryotes (so-called “plamalogens”) where they can have important biological activities. Even more remarkable is the existence of non-isoprenoid dialkylglycerols (with two ether connections to glycerol or GDD) which have been reported only in few (hyper)thermophilic bacteria and in rare planctomycetes.
This limited occurrence of non-isoprenoid GDD in bacterial isolates contrasts with their ubiquity and their structural diversity in actual and ancient (several millions years old) non-extremophilic ecosystems. The biological origin of non-isoprenoid ether lipids in such settings remains speculative and the modes of formation of these lipids are still unknown, strongly limiting the interpretation of their identification in situ and their use as biogeochemical/ecological proxies.
Unlike to Archaea, very few information is currently available regarding the biosynthesis and the physiological role of glycerol ether lipids in bacteria. The reasons why ether lipid biosynthesis has evolved in Bacteria are also puzzling. Do they represent an adaptation to (extreme) environmental conditions? If so why are such structures omnipresent in non-extreme environments? The evolutionary genesis of lipid membranes is still a mystery, and lipids are often omitted in early evolutionary models. Identifying some of the missing links in the evolution of ether lipid metabolic pathways might help to elucidate some details of the early events in the evolution of cellular life.
The BAGEL project is based on stimulating preliminary results obtained during an exploratory project funded in 2011 by the CNRS (INTERRVIE-INSU). It involves 3 complementary partners and combines an outstanding set of methods (classical microbiology, molecular and isotopic lipid chemistry, electronic microscopy, proteomics, phylogenomics, bioinformatics) to investigate in detail unprecedented isolates of mesophilic sulphate-reducing bacteria able of producing mono- and dialkylglycerol lipids (GMM and GDD) similar to those produced by thermophilic bacteria. The project should considerably increase our knowledge on the biosynthesis, the modes of formation (qualitative and quantitative distributions depending on the environmental conditions), the physiological role, the origin and the evolutionary history of (di)ether lipids in bacteria. Results from BAGEL could have major implications in fundamental scientific disciplines such as Environmental Microbiology, Biogeochemistry, Geobiology and Evolutionary Biology but also potentially (on a longer term) in Biotechnology and Biomedicine.