The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures

<i>Listeria monocytogenes</i> is a foodborne pathogen capable of secreting listeriolysin O (LLO), a pore-forming toxin encoded by the <i>hly</i> gene. While the functions of LLO have been studied extensively, how the production of LLO is modulated by the intestinal environmen...

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Main Authors: Erica Rinehart, Julia Chapman, Yvonne Sun
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Toxins
Subjects:
LLO
Online Access:https://www.mdpi.com/2072-6651/12/4/218
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spelling doaj-14c0fcbb81dc4815a82395a5f15ec2cd2020-11-25T02:04:01ZengMDPI AGToxins2072-66512020-03-011221821810.3390/toxins12040218The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid MixturesErica Rinehart0Julia Chapman1Yvonne Sun2Department of Biology, Integrative Science and Engineering Center, University of Dayton, Dayton, OH 45469, USADepartment of Biology, Integrative Science and Engineering Center, University of Dayton, Dayton, OH 45469, USADepartment of Biology, Integrative Science and Engineering Center, University of Dayton, Dayton, OH 45469, USA<i>Listeria monocytogenes</i> is a foodborne pathogen capable of secreting listeriolysin O (LLO), a pore-forming toxin encoded by the <i>hly</i> gene. While the functions of LLO have been studied extensively, how the production of LLO is modulated by the intestinal environment, devoid of oxygen and enriched in short chain fatty acids (SCFAs), is not completely understood. Using <i>L. monocytogenes</i> strain 10403s, we found that <i>hly</i> transcription was moderately decreased by aerobic SCFA exposures but significantly increased by anaerobic SCFA exposures. Moreover, aerobic, but not anaerobic, exposure to low levels of SCFAs resulted in a significantly higher LLO activity. These results demonstrated that transcriptional and post-transcriptional regulations of LLO production were separately modulated by SCFAs and were responsive to oxygen levels. Examining isogenic mutants revealed that PrfA and SigB play a role in regulating LLO production in response to SCFAs. Effects of SCFAs were also present in the cardiotropic strain 07PF0776 but distinctly different from those in strain 10403s. For both strains, prior exposures to SCFAs altered intracellular infections in Caco-2 and RAW264.7 cells and the plaque sizes in L fibroblasts, a result confirming the ability of <i>L. monocytogenes</i> to adapt to SCFAs in ways that impact its subsequent infection outcomes.https://www.mdpi.com/2072-6651/12/4/218<i>Listeria monocytogenes</i>LLOshort chain fatty acids<i>hly</i>aerobicanaerobic
collection DOAJ
language English
format Article
sources DOAJ
author Erica Rinehart
Julia Chapman
Yvonne Sun
spellingShingle Erica Rinehart
Julia Chapman
Yvonne Sun
The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
Toxins
<i>Listeria monocytogenes</i>
LLO
short chain fatty acids
<i>hly</i>
aerobic
anaerobic
author_facet Erica Rinehart
Julia Chapman
Yvonne Sun
author_sort Erica Rinehart
title The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
title_short The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
title_full The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
title_fullStr The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
title_full_unstemmed The Production of Listeriolysin O and Subsequent Intracellular Infections by <i>Listeria monocytogenes</i> Are Regulated by Exogenous Short Chain Fatty Acid Mixtures
title_sort production of listeriolysin o and subsequent intracellular infections by <i>listeria monocytogenes</i> are regulated by exogenous short chain fatty acid mixtures
publisher MDPI AG
series Toxins
issn 2072-6651
publishDate 2020-03-01
description <i>Listeria monocytogenes</i> is a foodborne pathogen capable of secreting listeriolysin O (LLO), a pore-forming toxin encoded by the <i>hly</i> gene. While the functions of LLO have been studied extensively, how the production of LLO is modulated by the intestinal environment, devoid of oxygen and enriched in short chain fatty acids (SCFAs), is not completely understood. Using <i>L. monocytogenes</i> strain 10403s, we found that <i>hly</i> transcription was moderately decreased by aerobic SCFA exposures but significantly increased by anaerobic SCFA exposures. Moreover, aerobic, but not anaerobic, exposure to low levels of SCFAs resulted in a significantly higher LLO activity. These results demonstrated that transcriptional and post-transcriptional regulations of LLO production were separately modulated by SCFAs and were responsive to oxygen levels. Examining isogenic mutants revealed that PrfA and SigB play a role in regulating LLO production in response to SCFAs. Effects of SCFAs were also present in the cardiotropic strain 07PF0776 but distinctly different from those in strain 10403s. For both strains, prior exposures to SCFAs altered intracellular infections in Caco-2 and RAW264.7 cells and the plaque sizes in L fibroblasts, a result confirming the ability of <i>L. monocytogenes</i> to adapt to SCFAs in ways that impact its subsequent infection outcomes.
topic <i>Listeria monocytogenes</i>
LLO
short chain fatty acids
<i>hly</i>
aerobic
anaerobic
url https://www.mdpi.com/2072-6651/12/4/218
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