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

Zilelidou EA, Rychli K, Manthou E, Ciolacu L, Wagner M, Skandamis PN - PLoS ONE (2015)

Bottom Line: Cell contact was essential for growth inhibition.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Food Quality Control and Hygiene, Department of Food Science and Human Nutrition, Agricultural University of Athens, Athens, Greece.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

Effect of strain competition on the invasion efficiency of L. monocytogenes strains.Invasion efficiency (%) of L. monocytogenes strains (A) PL25-RifR, (B) C5-StrR, (C) ScottA-StrR/RifR and (D) 6179-RifR grown alone (single) or in the presence of a second L. monocytogenes strain (1 day, 10°C, TSB-Y) was determined using Caco2 cells. Cells were infected for 1h with bacteria (multiplicity of infection of 25), and incubated for 45min (invasion) with gentamycin. Data, represented as % of invasion, are mean values ± standard deviation of three biological replicates performed in triplicate. *indicates significant difference of the mixed culture compared to the corresponding single culture (P<0.05). p-values are shown in S3 Table.
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pone.0141617.g003: Effect of strain competition on the invasion efficiency of L. monocytogenes strains.Invasion efficiency (%) of L. monocytogenes strains (A) PL25-RifR, (B) C5-StrR, (C) ScottA-StrR/RifR and (D) 6179-RifR grown alone (single) or in the presence of a second L. monocytogenes strain (1 day, 10°C, TSB-Y) was determined using Caco2 cells. Cells were infected for 1h with bacteria (multiplicity of infection of 25), and incubated for 45min (invasion) with gentamycin. Data, represented as % of invasion, are mean values ± standard deviation of three biological replicates performed in triplicate. *indicates significant difference of the mixed culture compared to the corresponding single culture (P<0.05). p-values are shown in S3 Table.

Mentions: Invasion efficiency of the high invasive strains C5 and PL25 increased slightly, but significantly when co-cultured with the moderate invasive strain ScottA (Fig 3A and 3B). Strain PL25, the strongest growth competitor, also showed increased invasion efficiency in the presence of C5 (Fig 3A). However, these effects were only mosdest. Strain ScottA demonstrated attenuated invasion efficiency, when co-cultured with C5 or PL25 (Fig 3C), whereas its ability to invade into Caco2 cells increased in the presence of the low invasive strain 6179 up to 10-fold. Furthermore, the invasion efficiency of strain 6179 was significantly decreased when co-cultured with C5 (Fig 3D). These results show an invasion advantage for the higher invasive strain in several strain combinations, which can also be disadvantageous for the low invasive strains.


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

Zilelidou EA, Rychli K, Manthou E, Ciolacu L, Wagner M, Skandamis PN - PLoS ONE (2015)

Effect of strain competition on the invasion efficiency of L. monocytogenes strains.Invasion efficiency (%) of L. monocytogenes strains (A) PL25-RifR, (B) C5-StrR, (C) ScottA-StrR/RifR and (D) 6179-RifR grown alone (single) or in the presence of a second L. monocytogenes strain (1 day, 10°C, TSB-Y) was determined using Caco2 cells. Cells were infected for 1h with bacteria (multiplicity of infection of 25), and incubated for 45min (invasion) with gentamycin. Data, represented as % of invasion, are mean values ± standard deviation of three biological replicates performed in triplicate. *indicates significant difference of the mixed culture compared to the corresponding single culture (P<0.05). p-values are shown in S3 Table.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4631365&req=5

pone.0141617.g003: Effect of strain competition on the invasion efficiency of L. monocytogenes strains.Invasion efficiency (%) of L. monocytogenes strains (A) PL25-RifR, (B) C5-StrR, (C) ScottA-StrR/RifR and (D) 6179-RifR grown alone (single) or in the presence of a second L. monocytogenes strain (1 day, 10°C, TSB-Y) was determined using Caco2 cells. Cells were infected for 1h with bacteria (multiplicity of infection of 25), and incubated for 45min (invasion) with gentamycin. Data, represented as % of invasion, are mean values ± standard deviation of three biological replicates performed in triplicate. *indicates significant difference of the mixed culture compared to the corresponding single culture (P<0.05). p-values are shown in S3 Table.
Mentions: Invasion efficiency of the high invasive strains C5 and PL25 increased slightly, but significantly when co-cultured with the moderate invasive strain ScottA (Fig 3A and 3B). Strain PL25, the strongest growth competitor, also showed increased invasion efficiency in the presence of C5 (Fig 3A). However, these effects were only mosdest. Strain ScottA demonstrated attenuated invasion efficiency, when co-cultured with C5 or PL25 (Fig 3C), whereas its ability to invade into Caco2 cells increased in the presence of the low invasive strain 6179 up to 10-fold. Furthermore, the invasion efficiency of strain 6179 was significantly decreased when co-cultured with C5 (Fig 3D). These results show an invasion advantage for the higher invasive strain in several strain combinations, which can also be disadvantageous for the low invasive strains.

Bottom Line: Cell contact was essential for growth inhibition.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Food Quality Control and Hygiene, Department of Food Science and Human Nutrition, Agricultural University of Athens, Athens, Greece.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus