Dataset Information

Biosynthesis of membrane-spanning ether lipids in Thermotoga maritima.

ABSTRACT: This study was conducted to identify the proteins involved in the synthesis of membrane-spanning ether lipids in Thermotoga maritima.

INSTRUMENT(S): Q Exactive HF-X

ORGANISM(S): Thermotoga Maritima Msb8

SUBMITTER: Sjef Boeren

LAB HEAD: Sjef Boeren

PROVIDER: PXD035794 | Pride | 2023-10-03

REPOSITORIES: Pride

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Publications

Disentangling the lipid divide: Identification of key enzymes for the biosynthesis of membrane-spanning and ether lipids in Bacteria.

Sahonero-Canavesi Diana X DX Siliakus Melvin F MF Abdala Asbun Alejandro A Koenen Michel M von Meijenfeldt F A Bastiaan FAB Boeren Sjef S Bale Nicole J NJ Engelman Julia C JC Fiege Kerstin K Strack van Schijndel Lora L Sinninghe Damsté Jaap S JS Villanueva Laura L

Science advances 20221216 50

Bacterial membranes are composed of fatty acids (FAs) ester-linked to glycerol-3-phosphate, while archaea have membranes made of isoprenoid chains ether-linked to glycerol-1-phosphate. Many archaeal species organize their membrane as a monolayer of membrane-spanning lipids (MSLs). Exceptions to this "lipid divide" are the production by some bacterial species of (ether-bound) MSLs, formed by tail-to-tail condensation of FAs resulting in the formation of (iso) diabolic acids (DAs), which are the l ...[more]

PMID: 36525503

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Project description:Membrane-spanning lipids are present in a wide variety of archaea, but they are rarely in bacteria. Nevertheless, the (hyper)thermophilic members of the order Thermotogales harbor tetraester, tetraether, and mixed ether/ester membrane-spanning lipids mostly composed of core lipids derived from diabolic acids, C30, C32, and C34 dicarboxylic acids with two adjacent mid-chain methyl substituents. Lipid analysis of Thermotoga maritima across growth phases revealed a decrease of the relative abundance of fatty acids together with an increase of diabolic acids with independence of growth temperature. We also identified isomers of C30 and C32 diabolic acids, i.e., dicarboxylic acids with only one methyl group at C-15. Their distribution suggests they are products of the condensation reaction but are preferably produced when the length of the acyl chains is not optimal. Compared with growth at the optimal temperature of 80°C, an increase of glycerol ether-derived lipids was observed at 55°C. Our analysis only detected diabolic acid-containing intact polar lipids with phosphoglycerol (PG) head groups. Considering these findings, we hypothesize a biosynthetic pathway for the synthesis of membrane-spanning lipids based on PG polar lipid formation, suggesting that the protein catalyzing this process is a membrane protein. We also identified, by genomic and protein domain analyses, a gene coding for a putative plasmalogen synthase homologue in T. maritima that is also present in other bacteria producing sn-1-alkyl ether lipids but not plasmalogens, suggesting it is involved in the conversion of the ester-to-ether bond in the diabolic acids bound in membrane-spanning lipids. IMPORTANCE Membrane-spanning lipids are unique compounds found in most archaeal membranes, but they are also present in specific bacterial groups like the Thermotogales. The synthesis and physiological role of membrane-spanning lipids in bacteria represent an evolutionary and biochemical open question that points to the differentiation of the membrane lipid composition. Understanding the formation of membrane-spanning lipids is crucial to solving this question and identifying the enzymatic and biochemical mechanism performing this procedure. In the present work, we found changes at the core lipid level, and we propose that the growth phase drives the biosynthesis of these lipids rather than temperature. Our results identified physiological conditions influencing the membrane-spanning lipid biosynthetic process, which can further clarify the pathway leading to the biosynthesis of these compounds.

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