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Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids

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...

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Autores principales: Villanueva, Laura, von Meijenfeldt, F. A. Bastiaan, Westbye, Alexander B., Yadav, Subhash, Hopmans, Ellen C., Dutilh, Bas E., Damsté, Jaap S. Sinninghe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7852524/
https://www.ncbi.nlm.nih.gov/pubmed/32929208
http://dx.doi.org/10.1038/s41396-020-00772-2
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author Villanueva, Laura
von Meijenfeldt, F. A. Bastiaan
Westbye, Alexander B.
Yadav, Subhash
Hopmans, Ellen C.
Dutilh, Bas E.
Damsté, Jaap S. Sinninghe
author_facet Villanueva, Laura
von Meijenfeldt, F. A. Bastiaan
Westbye, Alexander B.
Yadav, Subhash
Hopmans, Ellen C.
Dutilh, Bas E.
Damsté, Jaap S. Sinninghe
author_sort Villanueva, Laura
collection PubMed
description 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.
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spelling pubmed-78525242021-02-08 Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids Villanueva, Laura von Meijenfeldt, F. A. Bastiaan Westbye, Alexander B. Yadav, Subhash Hopmans, Ellen C. Dutilh, Bas E. Damsté, Jaap S. Sinninghe ISME J Article 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. Nature Publishing Group UK 2020-09-14 2021-01 /pmc/articles/PMC7852524/ /pubmed/32929208 http://dx.doi.org/10.1038/s41396-020-00772-2 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Villanueva, Laura
von Meijenfeldt, F. A. Bastiaan
Westbye, Alexander B.
Yadav, Subhash
Hopmans, Ellen C.
Dutilh, Bas E.
Damsté, Jaap S. Sinninghe
Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title_full Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title_fullStr Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title_full_unstemmed Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title_short Bridging the membrane lipid divide: bacteria of the FCB group superphylum have the potential to synthesize archaeal ether lipids
title_sort bridging the membrane lipid divide: bacteria of the fcb group superphylum have the potential to synthesize archaeal ether lipids
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7852524/
https://www.ncbi.nlm.nih.gov/pubmed/32929208
http://dx.doi.org/10.1038/s41396-020-00772-2
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