Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion

Abstract Background Lignin is a recalcitrant aromatic polymer that is a potential feedstock for renewable fuel and chemical production. Rhodococcus opacus PD630 is a promising strain for the biological upgrading of lignin due to its ability to tolerate and utilize lignin-derived aromatic compounds....

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Main Authors: William R. Henson, Fong-Fu Hsu, Gautam Dantas, Tae Seok Moon, Marcus Foston
Format: Article
Language:English
Published: BMC 2018-12-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-018-1337-z
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author William R. Henson
Fong-Fu Hsu
Gautam Dantas
Tae Seok Moon
Marcus Foston
author_facet William R. Henson
Fong-Fu Hsu
Gautam Dantas
Tae Seok Moon
Marcus Foston
author_sort William R. Henson
collection DOAJ
description Abstract Background Lignin is a recalcitrant aromatic polymer that is a potential feedstock for renewable fuel and chemical production. Rhodococcus opacus PD630 is a promising strain for the biological upgrading of lignin due to its ability to tolerate and utilize lignin-derived aromatic compounds. To enhance its aromatic tolerance, we recently applied adaptive evolution using phenol as a sole carbon source and characterized a phenol-adapted R. opacus strain (evol40) and the wild-type (WT) strain by whole genome and RNA sequencing. While this effort increased our understanding of the aromatic tolerance, the tolerance mechanisms were not completely elucidated. Results We hypothesize that the composition of lipids plays an important role in phenol tolerance. To test this hypothesis, we applied high-resolution mass spectrometry analysis to lipid samples obtained from the WT and evol40 strains grown in 1 g/L glucose (glucose), 0.75 g/L phenol (low phenol), or 1.5 g/L phenol (high phenol, evol40 only) as a sole carbon source. This analysis identified > 100 lipid species of mycolic acids, phosphatidylethanolamines (PEs), phosphatidylinositols (PIs), and triacylglycerols. In both strains, mycolic acids had fewer double bond numbers in phenol conditions than the glucose condition, and evol40 had significantly shorter mycolic acid chain lengths than the WT strain in phenol conditions. These results indicate that phenol adaptation affected mycolic acid membrane composition. In addition, the percentage of unsaturated phospholipids decreased for both strains in phenol conditions compared to the glucose condition. Moreover, the PI content increased for both strains in the low phenol condition compared to the glucose condition, and the PI content increased further for evol40 in the high phenol condition relative to the low phenol condition. Conclusions This work represents the first comprehensive lipidomic study on the membrane of R. opacus grown using phenol as a sole carbon source. Our results suggest that the alteration of the mycolic acid and phospholipid membrane composition may be a strategy of R. opacus for phenol tolerance.
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spelling doaj.art-0cfccb70b2bf457a955e77305d430cd92022-12-22T00:26:28ZengBMCBiotechnology for Biofuels1754-68342018-12-0111111510.1186/s13068-018-1337-zLipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversionWilliam R. Henson0Fong-Fu Hsu1Gautam Dantas2Tae Seok Moon3Marcus Foston4Department of Energy, Environmental and Chemical Engineering, Washington University in St. LouisMass Spectrometry Resource, Division of Endocrinology, Diabetes, Metabolism, and Lipid Research, Department of Internal Medicine, Washington University School of MedicineDepartment of Pathology and Immunology, Washington University in St. Louis School of MedicineDepartment of Energy, Environmental and Chemical Engineering, Washington University in St. LouisDepartment of Energy, Environmental and Chemical Engineering, Washington University in St. LouisAbstract Background Lignin is a recalcitrant aromatic polymer that is a potential feedstock for renewable fuel and chemical production. Rhodococcus opacus PD630 is a promising strain for the biological upgrading of lignin due to its ability to tolerate and utilize lignin-derived aromatic compounds. To enhance its aromatic tolerance, we recently applied adaptive evolution using phenol as a sole carbon source and characterized a phenol-adapted R. opacus strain (evol40) and the wild-type (WT) strain by whole genome and RNA sequencing. While this effort increased our understanding of the aromatic tolerance, the tolerance mechanisms were not completely elucidated. Results We hypothesize that the composition of lipids plays an important role in phenol tolerance. To test this hypothesis, we applied high-resolution mass spectrometry analysis to lipid samples obtained from the WT and evol40 strains grown in 1 g/L glucose (glucose), 0.75 g/L phenol (low phenol), or 1.5 g/L phenol (high phenol, evol40 only) as a sole carbon source. This analysis identified > 100 lipid species of mycolic acids, phosphatidylethanolamines (PEs), phosphatidylinositols (PIs), and triacylglycerols. In both strains, mycolic acids had fewer double bond numbers in phenol conditions than the glucose condition, and evol40 had significantly shorter mycolic acid chain lengths than the WT strain in phenol conditions. These results indicate that phenol adaptation affected mycolic acid membrane composition. In addition, the percentage of unsaturated phospholipids decreased for both strains in phenol conditions compared to the glucose condition. Moreover, the PI content increased for both strains in the low phenol condition compared to the glucose condition, and the PI content increased further for evol40 in the high phenol condition relative to the low phenol condition. Conclusions This work represents the first comprehensive lipidomic study on the membrane of R. opacus grown using phenol as a sole carbon source. Our results suggest that the alteration of the mycolic acid and phospholipid membrane composition may be a strategy of R. opacus for phenol tolerance.http://link.springer.com/article/10.1186/s13068-018-1337-zRhodococcus opacusPhenolTriacylglycerolMycolic acidPhospholipidMass spectrometry
spellingShingle William R. Henson
Fong-Fu Hsu
Gautam Dantas
Tae Seok Moon
Marcus Foston
Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
Biotechnology for Biofuels
Rhodococcus opacus
Phenol
Triacylglycerol
Mycolic acid
Phospholipid
Mass spectrometry
title Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
title_full Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
title_fullStr Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
title_full_unstemmed Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
title_short Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion
title_sort lipid metabolism of phenol tolerant rhodococcus opacus strains for lignin bioconversion
topic Rhodococcus opacus
Phenol
Triacylglycerol
Mycolic acid
Phospholipid
Mass spectrometry
url http://link.springer.com/article/10.1186/s13068-018-1337-z
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