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...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2020-03-01
|
Series: | Toxins |
Subjects: | |
Online Access: | https://www.mdpi.com/2072-6651/12/4/218 |
id |
doaj-14c0fcbb81dc4815a82395a5f15ec2cd |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT ericarinehart theproductionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures AT juliachapman theproductionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures AT yvonnesun theproductionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures AT ericarinehart productionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures AT juliachapman productionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures AT yvonnesun productionoflisteriolysinoandsubsequentintracellularinfectionsbyilisteriamonocytogenesiareregulatedbyexogenousshortchainfattyacidmixtures |
_version_ |
1724945102771585024 |