Exogenous polyunsaturated fatty acids (PUFAs) promote changes in growth, phospholipid composition, membrane permeability

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RESEARCH ARTICLE

Open Access

Exogenous polyunsaturated fatty acids (PUFAs) promote changes in growth, phospholipid composition, membrane permeability and virulence phenotypes in Escherichia coli Joshua L. Herndon1, Rachel E. Peters1, Rachel N. Hofer2, Timothy B. Simmons1, Steven J. Symes2 and David K. Giles1*

Abstract Background: The utilization of exogenous fatty acids by Gram-negative bacteria has been linked to many cellular processes, including fatty acid oxidation for metabolic gain, assimilation into membrane phospholipids, and control of phenotypes associated with virulence. The expanded fatty acid handling capabilities have been demonstrated in several bacteria of medical importance; however, a survey of the polyunsaturated fatty acid responses in the model organism Escherichia coli has not been performed. The current study examined the impacts of exogenous fatty acids on E. coli. Results: All PUFAs elicited higher overall growth, with several fatty acids supporting growth as sole carbon sources. Most PUFAs were incorporated into membrane phospholipids as determined by Ultra performance liquid chromatography-mass spectrometry, whereas membrane permeability was variably affected as measured by two separate dye uptake assays. Biofilm formation, swimming motility and antimicrobial peptide resistance were altered in the presence of PUFAs, with arachidonic and docosahexaenoic acids eliciting strong alteration to these phenotypes. Conclusions: The findings herein add E. coli to the growing list of Gram-negative bacteria with broader capabilities for utilizing and responding to exogenous fatty acids. Understanding bacterial responses to PUFAs may lead to microbial behavioral control regimens for disease prevention. Keywords: Escherichia coli, Polyunsaturated fatty acids (PUFAs), Phospholipids, Antimicrobial peptides, Biofilm, Motility

Background An emerging body of evidence has highlighted the expanded fatty acid handling characteristics of Gram-negative bacteria. The impacts of fatty acids acquired from growth media include phospholipid remodeling and phenotypes * Correspondence: [email protected] 1 Department of Biology, Geology, and Environmental Science, The University of Tennessee at Chattanooga, Chattanooga, TN, USA Full list of author information is available at the end of the article

affecting growth and virulence [1–4]. The expanded utility of fatty acids magnifies the relevance of environmental adaptation for bacteria, especially those that oscillate between host and aquatic niches. While the membrane phospholipid modifications and behavioral responses (biofilm formation, motility) of several gammaproteobacteria have been demonstrated, an examination of Escherichia coli has not been performed. E. coli, regarded as the Gramnegative model organism for bacteria due to its historical

© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as