Pseudomonas sp. Strain 273 Incorporates Organofluorine into the Lipid Bilayer during Growth with Fluorinated Alkanes

Yongchao Xie; Amanda L. May; Gao Chen; Lindsay P. Brown; Joshua B. Powers; Eric D. Tague; Shawn R. Campagna; Frank E. Löffler

doi:10.1021/acs.est.2c01454

Pseudomonas sp. Strain 273 Incorporates Organofluorine into the Lipid Bilayer during Growth with Fluorinated Alkanes

Yongchao Xie
, Amanda L. May
, Gao Chen
, Lindsay P. Brown
, Joshua B. Powers
, Eric D. Tague
, Shawn R. Campagna
, Frank E. Löffler

Plant Systems Biology

Research output: Contribution to journal › Article › peer-review

23 Scopus citations

Abstract

Anthropogenic organofluorine compounds are recalcitrant, globally distributed, and a human health concern. Although rare, natural processes synthesize fluorinated compounds, and some bacteria have evolved mechanisms to metabolize organofluorine compounds. Pseudomonas sp. strain 273 grows with 1-fluorodecane (FD) and 1,10-difluorodecane (DFD) as carbon sources, but inorganic fluoride release was not stoichiometric. Metabolome studies revealed that this bacterium produces fluorinated anabolites and phospholipids. Mass spectrometric fatty acid profiling detected fluorinated long-chain (i.e., C₁₂-C₁₉) fatty acids in strain 273 cells grown with FD or DFD, and lipidomic profiling determined that 7.5 ± 0.2 and 82.0 ± 1.0% of the total phospholipids in strain 273 grown with FD or DFD, respectively, were fluorinated. The detection of the fluorinated metabolites and macromolecules represents a heretofore unrecognized sink for organofluorine, an observation with consequences for the environmental fate and transport of fluorinated aliphatic compounds.

Original language	English
Pages (from-to)	8155-8166
Number of pages	12
Journal	Environmental Science and Technology
Volume	56
Issue number	12
DOIs	https://doi.org/10.1021/acs.est.2c01454
State	Published - Jun 21 2022

Funding

This work was supported by The University Consortium for Field-Focused Groundwater Research. The authors acknowledge support from the China Scholarship Council to YX during his study at the University of Tennessee, Knoxville. Support for the analytical work was from NSF Award MCB-1615373 to JBP, NIH/NIAID Award R01AI116571 to EDF, and the University of Tennessee–Oak Ridge Innovation Institute (UT-ORII) for providing a fellowship to LPB. Some of the analyses used instrumentation provided by NSF Award DBI-1530975. The authors thank the Biological and Small Molecule Mass Spectrometry Core at the University of Tennessee (RRID: SCR_021368) for sample processing and data collection as well as H. Castro for assistance and helpful discussions.

Keywords

environmental fate
fluorinated alkanes
fluorinated lipids
lipid metabolism
lipidomics

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10.1021/acs.est.2c01454

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title = "Pseudomonas sp. Strain 273 Incorporates Organofluorine into the Lipid Bilayer during Growth with Fluorinated Alkanes",

abstract = "Anthropogenic organofluorine compounds are recalcitrant, globally distributed, and a human health concern. Although rare, natural processes synthesize fluorinated compounds, and some bacteria have evolved mechanisms to metabolize organofluorine compounds. Pseudomonas sp. strain 273 grows with 1-fluorodecane (FD) and 1,10-difluorodecane (DFD) as carbon sources, but inorganic fluoride release was not stoichiometric. Metabolome studies revealed that this bacterium produces fluorinated anabolites and phospholipids. Mass spectrometric fatty acid profiling detected fluorinated long-chain (i.e., C12-C19) fatty acids in strain 273 cells grown with FD or DFD, and lipidomic profiling determined that 7.5 ± 0.2 and 82.0 ± 1.0\% of the total phospholipids in strain 273 grown with FD or DFD, respectively, were fluorinated. The detection of the fluorinated metabolites and macromolecules represents a heretofore unrecognized sink for organofluorine, an observation with consequences for the environmental fate and transport of fluorinated aliphatic compounds.",

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author = "Yongchao Xie and May, \{Amanda L.\} and Gao Chen and Brown, \{Lindsay P.\} and Powers, \{Joshua B.\} and Tague, \{Eric D.\} and Campagna, \{Shawn R.\} and L{\"o}ffler, \{Frank E.\}",

year = "2022",

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doi = "10.1021/acs.est.2c01454",

language = "English",

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T1 - Pseudomonas sp. Strain 273 Incorporates Organofluorine into the Lipid Bilayer during Growth with Fluorinated Alkanes

AU - Xie, Yongchao

AU - May, Amanda L.

AU - Chen, Gao

AU - Brown, Lindsay P.

AU - Powers, Joshua B.

AU - Tague, Eric D.

AU - Campagna, Shawn R.

AU - Löffler, Frank E.

PY - 2022/6/21

Y1 - 2022/6/21

N2 - Anthropogenic organofluorine compounds are recalcitrant, globally distributed, and a human health concern. Although rare, natural processes synthesize fluorinated compounds, and some bacteria have evolved mechanisms to metabolize organofluorine compounds. Pseudomonas sp. strain 273 grows with 1-fluorodecane (FD) and 1,10-difluorodecane (DFD) as carbon sources, but inorganic fluoride release was not stoichiometric. Metabolome studies revealed that this bacterium produces fluorinated anabolites and phospholipids. Mass spectrometric fatty acid profiling detected fluorinated long-chain (i.e., C12-C19) fatty acids in strain 273 cells grown with FD or DFD, and lipidomic profiling determined that 7.5 ± 0.2 and 82.0 ± 1.0% of the total phospholipids in strain 273 grown with FD or DFD, respectively, were fluorinated. The detection of the fluorinated metabolites and macromolecules represents a heretofore unrecognized sink for organofluorine, an observation with consequences for the environmental fate and transport of fluorinated aliphatic compounds.

AB - Anthropogenic organofluorine compounds are recalcitrant, globally distributed, and a human health concern. Although rare, natural processes synthesize fluorinated compounds, and some bacteria have evolved mechanisms to metabolize organofluorine compounds. Pseudomonas sp. strain 273 grows with 1-fluorodecane (FD) and 1,10-difluorodecane (DFD) as carbon sources, but inorganic fluoride release was not stoichiometric. Metabolome studies revealed that this bacterium produces fluorinated anabolites and phospholipids. Mass spectrometric fatty acid profiling detected fluorinated long-chain (i.e., C12-C19) fatty acids in strain 273 cells grown with FD or DFD, and lipidomic profiling determined that 7.5 ± 0.2 and 82.0 ± 1.0% of the total phospholipids in strain 273 grown with FD or DFD, respectively, were fluorinated. The detection of the fluorinated metabolites and macromolecules represents a heretofore unrecognized sink for organofluorine, an observation with consequences for the environmental fate and transport of fluorinated aliphatic compounds.

KW - environmental fate

KW - fluorinated alkanes

KW - fluorinated lipids

KW - lipid metabolism

KW - lipidomics

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ER -

Pseudomonas sp. Strain 273 Incorporates Organofluorine into the Lipid Bilayer during Growth with Fluorinated Alkanes

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