Abstract
Archaea synthesize membranes of isoprenoid lipids that are ether-linked to glycerol-1-phosphate (G1P), while Bacteria/Eukarya produce membranes consisting of fatty acids ester-bound to glycerol-3-phosphate (G3P). This dichotomy in membrane lipid composition (i.e., the ‘lipid divide’) is believed to have arisen after the Last Universal Common Ancestor (LUCA). A leading hypothesis is that LUCA possessed a heterochiral ‘mixed archaeal/bacterial membrane’. However, no natural microbial representatives supporting this scenario have been shown to exist today. Here, we demonstrate that bacteria of the Fibrobacteres–Chlorobi–Bacteroidetes (FCB) group superphylum encode a putative archaeal pathway for ether-bound isoprenoid membrane lipids in addition to the bacterial fatty acid membrane pathway. Key genes were expressed in the environment and their recombinant expression in Escherichia coli resulted in the formation of a ‘mixed archaeal/bacterial membrane’. Genomic evidence and biochemical assays suggest that the archaeal-like lipids of members of the FCB group could possess either a G1P or G3P stereochemistry. Our results support the existence of ‘mixed membranes’ in natural environments and their stability over a long period in evolutionary history, thereby bridging a once-thought fundamental divide in biology.
| Original language | English |
|---|---|
| Pages (from-to) | 168-182 |
| Number of pages | 15 |
| Journal | ISME Journal |
| Volume | 15 |
| Issue number | 1 |
| DOIs | |
| Publication status | Published - Jan 2021 |
Funding
Acknowledgements We thank Melvin Siliakus for providing several of the plasmid constructs and for useful suggestions to improve the manuscript. We are also thankful to Julian Vosseberg, John van Dam, Anja Spang, and Jan de Leeuw for suggestions and constructive discussions. We acknowledge the Utrecht Sequencing Facility (USF), which is partially subsidized by the Hubrecht Institute, Utrecht University, and UMC Utrecht, for the sequencing data and service. We thank Jan Kees van Amerongen, Elda Panoto, Maartje Brouwer, Michele Grego, and Michel Koenen for providing technical support. We acknowledge the crew and scientists of the R/V Pelagia cruises 64PE371 (chief scientist Gert-Jan Reichart) and 64PE408 (chief scientist Marcel van der Meer). JSSD received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement n◦ 694569—MICROLIPIDS). LV and JSSD 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). BED is supported by the Netherlands Organization for Scientific Research (NWO) Vidi grant 864.14.004. FABvM and BED are supported by ERC Consolidator grant 865694.