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Title: Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties

Abstract

Bacterial membranes are complex mixtures of lipids and proteins, the combination of which confers biophysical properties that allows cells to respond to environmental conditions. Carotenoids are sterol analogs that are important for regulating membrane dynamics. The membrane of Pantoea sp. YR343 is characterized by the presence of the carotenoid zeaxanthin, and a carotenoid-deficient mutant, ΔcrtB, displays defects in root colonization, reduced secretion of indole-3-acetic acid, and defects in biofilm formation. Here we demonstrate that the loss of carotenoids results in changes to the membrane lipid composition in Pantoea sp. YR343, including increased amounts of unsaturated fatty acids in the ΔcrtB mutant membranes. These mutant cells displayed less fluid membranes in comparison to wild type cells as measured by fluorescence anisotropy of whole cells. Studies with artificial systems, however, have shown that carotenoids impart membrane rigidifying properties. Thus, we examined membrane fluidity using spheroplasts and vesicles composed of lipids extracted from either wild type or mutant cells. Interestingly, with the removal of the cell wall and membrane proteins, ΔcrtB vesicles were more fluid than vesicles made from lipids extracted from wild type cells. In addition, carotenoids appeared to stabilize membrane fluidity during rapidly changing temperatures. Taken together, these results suggest thatmore » Pantoea sp. YR343 compensates for the loss of carotenoids by changing lipid composition, which together with membrane proteins, results in reduced membrane fluidity. Here these changes may influence the abundance or function of membrane proteins that are responsible for the physiological changes observed in the ΔcrtB mutant cells.« less

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1635710
Alternate Identifier(s):
OSTI ID: 1515682; OSTI ID: 1547211
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Biochimica et Biophysica Acta. Biomembranes
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta. Biomembranes Journal Volume: 1861 Journal Issue: 7; Journal ID: ISSN 0005-2736
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Zeaxanthin; Pantoea; Membrane fluidity; Atomic force microscopy; Fluorescence anisotropy

Citation Formats

Kumar, Sushmitha Vijaya, Taylor, Graham, Hasim, Sahar, Collier, C. Patrick, Farmer, Abigail T., Campagna, Shawn R., Bible, Amber N., Doktycz, Mitchel J., and Morrell-Falvey, Jennifer. Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties. Netherlands: N. p., 2019. Web. doi:10.1016/j.bbamem.2019.05.009.
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Kumar, Sushmitha Vijaya, Taylor, Graham, Hasim, Sahar, Collier, C. Patrick, Farmer, Abigail T., Campagna, Shawn R., Bible, Amber N., Doktycz, Mitchel J., & Morrell-Falvey, Jennifer. Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties. Netherlands. https://doi.org/10.1016/j.bbamem.2019.05.009
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Kumar, Sushmitha Vijaya, Taylor, Graham, Hasim, Sahar, Collier, C. Patrick, Farmer, Abigail T., Campagna, Shawn R., Bible, Amber N., Doktycz, Mitchel J., and Morrell-Falvey, Jennifer. Mon . "Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties". Netherlands. https://doi.org/10.1016/j.bbamem.2019.05.009.
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@article{osti_1635710,
title = {Loss of carotenoids from membranes of Pantoea sp. YR343 results in altered lipid composition and changes in membrane biophysical properties},
author = {Kumar, Sushmitha Vijaya and Taylor, Graham and Hasim, Sahar and Collier, C. Patrick and Farmer, Abigail T. and Campagna, Shawn R. and Bible, Amber N. and Doktycz, Mitchel J. and Morrell-Falvey, Jennifer},
abstractNote = {Bacterial membranes are complex mixtures of lipids and proteins, the combination of which confers biophysical properties that allows cells to respond to environmental conditions. Carotenoids are sterol analogs that are important for regulating membrane dynamics. The membrane of Pantoea sp. YR343 is characterized by the presence of the carotenoid zeaxanthin, and a carotenoid-deficient mutant, ΔcrtB, displays defects in root colonization, reduced secretion of indole-3-acetic acid, and defects in biofilm formation. Here we demonstrate that the loss of carotenoids results in changes to the membrane lipid composition in Pantoea sp. YR343, including increased amounts of unsaturated fatty acids in the ΔcrtB mutant membranes. These mutant cells displayed less fluid membranes in comparison to wild type cells as measured by fluorescence anisotropy of whole cells. Studies with artificial systems, however, have shown that carotenoids impart membrane rigidifying properties. Thus, we examined membrane fluidity using spheroplasts and vesicles composed of lipids extracted from either wild type or mutant cells. Interestingly, with the removal of the cell wall and membrane proteins, ΔcrtB vesicles were more fluid than vesicles made from lipids extracted from wild type cells. In addition, carotenoids appeared to stabilize membrane fluidity during rapidly changing temperatures. Taken together, these results suggest that Pantoea sp. YR343 compensates for the loss of carotenoids by changing lipid composition, which together with membrane proteins, results in reduced membrane fluidity. Here these changes may influence the abundance or function of membrane proteins that are responsible for the physiological changes observed in the ΔcrtB mutant cells.},
doi = {10.1016/j.bbamem.2019.05.009},
journal = {Biochimica et Biophysica Acta. Biomembranes},
number = 7,
volume = 1861,
place = {Netherlands},
year = {Mon Jul 01 00:00:00 EDT 2019},
month = {Mon Jul 01 00:00:00 EDT 2019}
}
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https://doi.org/10.1016/j.bbamem.2019.05.009
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