Changes in the distribution of membrane lipids during growth of Thermotoga maritima at different temperatures: Indications for the potential mechanism of biosynthesis of ether-bound diabolic acid (membrane-spanning) lipids

Diana X. Sahonero-Canavesi, Laura Villanueva, Nicole J. Bale, Jade Bosviel, Michel Koenen, Ellen C. Hopmans, Jaap S. Sinninghe Damsté

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

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 membranespanning 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.

Original languageEnglish
Article numbere01763-21
Pages (from-to)1-17
Number of pages17
JournalApplied and Environmental Microbiology
Volume88
Issue number2
DOIs
Publication statusPublished - 25 Jan 2022

Funding

This project received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement no. 694569-MICROLIPIDS) to J.S.S.D. L.V. and J.S.S.D. receive funding from the Soehngen Institute for Anaerobic Microbiology (SIAM) through a Gravitation Grant (024.002.002) from the Dutch Ministry of Education, Culture, and Science (OCW).

FundersFunder number
European Research Council (ERC) under the European Union694569-MICROLIPIDS
Soehngen Institute for Anaerobic Microbiology (SIAM) from the Dutch Ministry of Education, Culture, and Science (OCW)024.002.002

    Keywords

    • Biosynthesis
    • Diabolic acid
    • Ether lipids
    • Growth phase
    • Lipid biosynthesis
    • Membrane-spanning lipids
    • Thermotoga
    • Thermotoga maritima

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