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Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome

Developing cultivation methods that yield chemically and isotopically defined fatty acid (FA) compositions within bacterial cytoplasmic membranes establishes an in vivo experimental platform to study membrane biophysics and cell membrane regulation using novel approaches. Yet before fully realizing...

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Autores principales: Nickels, Jonathan D., Poudel, Suresh, Chatterjee, Sneha, Farmer, Abigail, Cordner, Destini, Campagna, Shawn R., Giannone, Richard J., Hettich, Robert L., Myles, Dean A. A., Standaert, Robert F., Katsaras, John, Elkins, James G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243436/
https://www.ncbi.nlm.nih.gov/pubmed/32499768
http://dx.doi.org/10.3389/fmicb.2020.00914
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author Nickels, Jonathan D.
Poudel, Suresh
Chatterjee, Sneha
Farmer, Abigail
Cordner, Destini
Campagna, Shawn R.
Giannone, Richard J.
Hettich, Robert L.
Myles, Dean A. A.
Standaert, Robert F.
Katsaras, John
Elkins, James G.
author_facet Nickels, Jonathan D.
Poudel, Suresh
Chatterjee, Sneha
Farmer, Abigail
Cordner, Destini
Campagna, Shawn R.
Giannone, Richard J.
Hettich, Robert L.
Myles, Dean A. A.
Standaert, Robert F.
Katsaras, John
Elkins, James G.
author_sort Nickels, Jonathan D.
collection PubMed
description Developing cultivation methods that yield chemically and isotopically defined fatty acid (FA) compositions within bacterial cytoplasmic membranes establishes an in vivo experimental platform to study membrane biophysics and cell membrane regulation using novel approaches. Yet before fully realizing the potential of this method, it is prudent to understand the systemic changes in cells induced by the labeling procedure itself. In this work, analysis of cellular membrane compositions was paired with proteomics to assess how the proteome changes in response to the directed incorporation of exogenous FAs into the membrane of Bacillus subtilis. Key findings from this analysis include an alteration in lipid headgroup distribution, with an increase in phosphatidylglycerol lipids and decrease in phosphatidylethanolamine lipids, possibly providing a fluidizing effect on the cell membrane in response to the induced change in membrane composition. Changes in the abundance of enzymes involved in FA biosynthesis and degradation are observed; along with changes in abundance of cell wall enzymes and isoprenoid lipid production. The observed changes may influence membrane organization, and indeed the well-known lipid raft-associated protein flotillin was found to be substantially down-regulated in the labeled cells – as was the actin-like protein MreB. Taken as a whole, this study provides a greater depth of understanding for this important cell membrane experimental platform and presents a number of new connections to be explored in regard to modulating cell membrane FA composition and its effects on lipid headgroup and raft/cytoskeletal associated proteins.
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spelling pubmed-72434362020-06-03 Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome Nickels, Jonathan D. Poudel, Suresh Chatterjee, Sneha Farmer, Abigail Cordner, Destini Campagna, Shawn R. Giannone, Richard J. Hettich, Robert L. Myles, Dean A. A. Standaert, Robert F. Katsaras, John Elkins, James G. Front Microbiol Microbiology Developing cultivation methods that yield chemically and isotopically defined fatty acid (FA) compositions within bacterial cytoplasmic membranes establishes an in vivo experimental platform to study membrane biophysics and cell membrane regulation using novel approaches. Yet before fully realizing the potential of this method, it is prudent to understand the systemic changes in cells induced by the labeling procedure itself. In this work, analysis of cellular membrane compositions was paired with proteomics to assess how the proteome changes in response to the directed incorporation of exogenous FAs into the membrane of Bacillus subtilis. Key findings from this analysis include an alteration in lipid headgroup distribution, with an increase in phosphatidylglycerol lipids and decrease in phosphatidylethanolamine lipids, possibly providing a fluidizing effect on the cell membrane in response to the induced change in membrane composition. Changes in the abundance of enzymes involved in FA biosynthesis and degradation are observed; along with changes in abundance of cell wall enzymes and isoprenoid lipid production. The observed changes may influence membrane organization, and indeed the well-known lipid raft-associated protein flotillin was found to be substantially down-regulated in the labeled cells – as was the actin-like protein MreB. Taken as a whole, this study provides a greater depth of understanding for this important cell membrane experimental platform and presents a number of new connections to be explored in regard to modulating cell membrane FA composition and its effects on lipid headgroup and raft/cytoskeletal associated proteins. Frontiers Media S.A. 2020-05-15 /pmc/articles/PMC7243436/ /pubmed/32499768 http://dx.doi.org/10.3389/fmicb.2020.00914 Text en Copyright © 2020 Nickels, Poudel, Chatterjee, Farmer, Cordner, Campagna, Giannone, Hettich, Myles, Standaert, Katsaras and Elkins. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Nickels, Jonathan D.
Poudel, Suresh
Chatterjee, Sneha
Farmer, Abigail
Cordner, Destini
Campagna, Shawn R.
Giannone, Richard J.
Hettich, Robert L.
Myles, Dean A. A.
Standaert, Robert F.
Katsaras, John
Elkins, James G.
Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title_full Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title_fullStr Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title_full_unstemmed Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title_short Impact of Fatty-Acid Labeling of Bacillus subtilis Membranes on the Cellular Lipidome and Proteome
title_sort impact of fatty-acid labeling of bacillus subtilis membranes on the cellular lipidome and proteome
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7243436/
https://www.ncbi.nlm.nih.gov/pubmed/32499768
http://dx.doi.org/10.3389/fmicb.2020.00914
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