Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.

Multiple Listeria monocytogenes strains can be present in the same food sample; moreover, infection with more than one L. monocytogenes strain can also occur. In this study we investigated the impact of strain competition on the growth and in vitro virulence potential of L. monocytogenes. We identif...

Full description

Bibliographic Details
Main Authors: Evangelia A Zilelidou, Kathrin Rychli, Evanthia Manthou, Luminita Ciolacu, Martin Wagner, Panagiotis N Skandamis
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0141617
id doaj-dc6abed8f24a4fd887b17ef3f1614f08
record_format Article
spelling doaj-dc6abed8f24a4fd887b17ef3f1614f082021-03-03T19:58:02ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011011e014161710.1371/journal.pone.0141617Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.Evangelia A ZilelidouKathrin RychliEvanthia ManthouLuminita CiolacuMartin WagnerPanagiotis N SkandamisMultiple Listeria monocytogenes strains can be present in the same food sample; moreover, infection with more than one L. monocytogenes strain can also occur. In this study we investigated the impact of strain competition on the growth and in vitro virulence potential of L. monocytogenes. We identified two strong competitor strains, whose growth was not (or only slightly) influenced by the presence of other strains and two weak competitor strains, which were outcompeted by other strains. Cell contact was essential for growth inhibition. In vitro virulence assays using human intestinal epithelial Caco2 cells showed a correlation between the invasion efficiency and growth inhibition: the strong growth competitor strains showed high invasiveness. Moreover, invasion efficiency of the highly invasive strain was further increased in certain combinations by the presence of a low invasive strain. In all tested combinations, the less invasive strain was outcompeted by the higher invasive strain. Studying the effect of cell contact on in vitro virulence competition revealed a complex pattern in which the observed effects depended only partially on cell-contact suggesting that competition occurs at two different levels: i) during co-cultivation prior to infection, which might influence the expression of virulence factors, and ii) during infection, when bacterial cells compete for the host cell. In conclusion, we show that growth of L. monocytogenes can be inhibited by strains of the same species leading potentially to biased recovery during enrichment procedures. Furthermore, the presence of more than one L. monocytogenes strain in food can lead to increased infection rates due to synergistic effects on the virulence potential.https://doi.org/10.1371/journal.pone.0141617
collection DOAJ
language English
format Article
sources DOAJ
author Evangelia A Zilelidou
Kathrin Rychli
Evanthia Manthou
Luminita Ciolacu
Martin Wagner
Panagiotis N Skandamis
spellingShingle Evangelia A Zilelidou
Kathrin Rychli
Evanthia Manthou
Luminita Ciolacu
Martin Wagner
Panagiotis N Skandamis
Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
PLoS ONE
author_facet Evangelia A Zilelidou
Kathrin Rychli
Evanthia Manthou
Luminita Ciolacu
Martin Wagner
Panagiotis N Skandamis
author_sort Evangelia A Zilelidou
title Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
title_short Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
title_full Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
title_fullStr Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
title_full_unstemmed Highly Invasive Listeria monocytogenes Strains Have Growth and Invasion Advantages in Strain Competition.
title_sort highly invasive listeria monocytogenes strains have growth and invasion advantages in strain competition.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Multiple Listeria monocytogenes strains can be present in the same food sample; moreover, infection with more than one L. monocytogenes strain can also occur. In this study we investigated the impact of strain competition on the growth and in vitro virulence potential of L. monocytogenes. We identified two strong competitor strains, whose growth was not (or only slightly) influenced by the presence of other strains and two weak competitor strains, which were outcompeted by other strains. Cell contact was essential for growth inhibition. In vitro virulence assays using human intestinal epithelial Caco2 cells showed a correlation between the invasion efficiency and growth inhibition: the strong growth competitor strains showed high invasiveness. Moreover, invasion efficiency of the highly invasive strain was further increased in certain combinations by the presence of a low invasive strain. In all tested combinations, the less invasive strain was outcompeted by the higher invasive strain. Studying the effect of cell contact on in vitro virulence competition revealed a complex pattern in which the observed effects depended only partially on cell-contact suggesting that competition occurs at two different levels: i) during co-cultivation prior to infection, which might influence the expression of virulence factors, and ii) during infection, when bacterial cells compete for the host cell. In conclusion, we show that growth of L. monocytogenes can be inhibited by strains of the same species leading potentially to biased recovery during enrichment procedures. Furthermore, the presence of more than one L. monocytogenes strain in food can lead to increased infection rates due to synergistic effects on the virulence potential.
url https://doi.org/10.1371/journal.pone.0141617
work_keys_str_mv AT evangeliaazilelidou highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
AT kathrinrychli highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
AT evanthiamanthou highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
AT luminitaciolacu highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
AT martinwagner highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
AT panagiotisnskandamis highlyinvasivelisteriamonocytogenesstrainshavegrowthandinvasionadvantagesinstraincompetition
_version_ 1714824868436901888