Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane

Antonella Caforio, Melvin F. Siliakus, Marten Exterkate, Samta Jain, Varsha R. Jumde, Ruben L.H. Andringa, Servé W.M. Kengen, Adriaan J. Minnaard, Arnold J.M. Driessen*, John van der Oost

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

13 Citations (Scopus)

Abstract

One of the main differences between bacteria and archaea concerns their membrane composition. Whereas bacterial membranes are made up of glycerol-3-phosphate ester lipids, archaeal membranes are composed of glycerol-1-phosphate ether lipids. Here, we report the construction of a stable hybrid heterochiral membrane through lipid engineering of the bacterium Escherichia coli. By boosting isoprenoid biosynthesis and heterologous expression of archaeal ether lipid biosynthesis genes, we obtained a viable E. coli strain of which the membranes contain archaeal lipids with the expected stereochemistry. It has been found that the archaeal lipid biosynthesis enzymes are relatively promiscuous with respect to their glycerol phosphate backbone and that E. coli has the unexpected potential to generate glycerol-1-phosphate. The unprecedented level of 20–30% archaeal lipids in a bacterial cell has allowed for analyzing the effect on the mixed-membrane cell’s phenotype. Interestingly, growth rates are unchanged, whereas the robustness of cells with a hybrid heterochiral membrane appeared slightly increased. The implications of these findings for evolutionary scenarios are discussed.
Original languageEnglish
Pages (from-to)3704-3709
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number14
DOIs
Publication statusPublished - 3 Apr 2018

Fingerprint

Archaea
Escherichia coli
Lipids
Membranes
Membrane Lipids
Phospholipid Ethers
Bacteria
Terpenes
Ether
Glycerol
Esters
Phosphates
Cell Membrane
Phenotype
Enzymes
Growth
Genes
alpha-glycerophosphoric acid

Keywords

  • Archaea
  • Bacteria
  • Ether lipids
  • Hybrid membranes
  • Lipid biosynthesis

Cite this

Caforio, Antonella ; Siliakus, Melvin F. ; Exterkate, Marten ; Jain, Samta ; Jumde, Varsha R. ; Andringa, Ruben L.H. ; Kengen, Servé W.M. ; Minnaard, Adriaan J. ; Driessen, Arnold J.M. ; van der Oost, John. / Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 14. pp. 3704-3709.
@article{f20669f7c13a418d911c23d67a18c0f3,
title = "Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane",
abstract = "One of the main differences between bacteria and archaea concerns their membrane composition. Whereas bacterial membranes are made up of glycerol-3-phosphate ester lipids, archaeal membranes are composed of glycerol-1-phosphate ether lipids. Here, we report the construction of a stable hybrid heterochiral membrane through lipid engineering of the bacterium Escherichia coli. By boosting isoprenoid biosynthesis and heterologous expression of archaeal ether lipid biosynthesis genes, we obtained a viable E. coli strain of which the membranes contain archaeal lipids with the expected stereochemistry. It has been found that the archaeal lipid biosynthesis enzymes are relatively promiscuous with respect to their glycerol phosphate backbone and that E. coli has the unexpected potential to generate glycerol-1-phosphate. The unprecedented level of 20–30{\%} archaeal lipids in a bacterial cell has allowed for analyzing the effect on the mixed-membrane cell’s phenotype. Interestingly, growth rates are unchanged, whereas the robustness of cells with a hybrid heterochiral membrane appeared slightly increased. The implications of these findings for evolutionary scenarios are discussed.",
keywords = "Archaea, Bacteria, Ether lipids, Hybrid membranes, Lipid biosynthesis",
author = "Antonella Caforio and Siliakus, {Melvin F.} and Marten Exterkate and Samta Jain and Jumde, {Varsha R.} and Andringa, {Ruben L.H.} and Kengen, {Serv{\'e} W.M.} and Minnaard, {Adriaan J.} and Driessen, {Arnold J.M.} and {van der Oost}, John",
year = "2018",
month = "4",
day = "3",
doi = "10.1073/pnas.1721604115",
language = "English",
volume = "115",
pages = "3704--3709",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "14",

}

Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane. / Caforio, Antonella; Siliakus, Melvin F.; Exterkate, Marten; Jain, Samta; Jumde, Varsha R.; Andringa, Ruben L.H.; Kengen, Servé W.M.; Minnaard, Adriaan J.; Driessen, Arnold J.M.; van der Oost, John.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 14, 03.04.2018, p. 3704-3709.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Converting Escherichia coli into an archaebacterium with a hybrid heterochiral membrane

AU - Caforio, Antonella

AU - Siliakus, Melvin F.

AU - Exterkate, Marten

AU - Jain, Samta

AU - Jumde, Varsha R.

AU - Andringa, Ruben L.H.

AU - Kengen, Servé W.M.

AU - Minnaard, Adriaan J.

AU - Driessen, Arnold J.M.

AU - van der Oost, John

PY - 2018/4/3

Y1 - 2018/4/3

N2 - One of the main differences between bacteria and archaea concerns their membrane composition. Whereas bacterial membranes are made up of glycerol-3-phosphate ester lipids, archaeal membranes are composed of glycerol-1-phosphate ether lipids. Here, we report the construction of a stable hybrid heterochiral membrane through lipid engineering of the bacterium Escherichia coli. By boosting isoprenoid biosynthesis and heterologous expression of archaeal ether lipid biosynthesis genes, we obtained a viable E. coli strain of which the membranes contain archaeal lipids with the expected stereochemistry. It has been found that the archaeal lipid biosynthesis enzymes are relatively promiscuous with respect to their glycerol phosphate backbone and that E. coli has the unexpected potential to generate glycerol-1-phosphate. The unprecedented level of 20–30% archaeal lipids in a bacterial cell has allowed for analyzing the effect on the mixed-membrane cell’s phenotype. Interestingly, growth rates are unchanged, whereas the robustness of cells with a hybrid heterochiral membrane appeared slightly increased. The implications of these findings for evolutionary scenarios are discussed.

AB - One of the main differences between bacteria and archaea concerns their membrane composition. Whereas bacterial membranes are made up of glycerol-3-phosphate ester lipids, archaeal membranes are composed of glycerol-1-phosphate ether lipids. Here, we report the construction of a stable hybrid heterochiral membrane through lipid engineering of the bacterium Escherichia coli. By boosting isoprenoid biosynthesis and heterologous expression of archaeal ether lipid biosynthesis genes, we obtained a viable E. coli strain of which the membranes contain archaeal lipids with the expected stereochemistry. It has been found that the archaeal lipid biosynthesis enzymes are relatively promiscuous with respect to their glycerol phosphate backbone and that E. coli has the unexpected potential to generate glycerol-1-phosphate. The unprecedented level of 20–30% archaeal lipids in a bacterial cell has allowed for analyzing the effect on the mixed-membrane cell’s phenotype. Interestingly, growth rates are unchanged, whereas the robustness of cells with a hybrid heterochiral membrane appeared slightly increased. The implications of these findings for evolutionary scenarios are discussed.

KW - Archaea

KW - Bacteria

KW - Ether lipids

KW - Hybrid membranes

KW - Lipid biosynthesis

U2 - 10.1073/pnas.1721604115

DO - 10.1073/pnas.1721604115

M3 - Article

VL - 115

SP - 3704

EP - 3709

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 14

ER -