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Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains

The increased availability of whole-genome-sequencing techniques generates a wealth of DNA data on numerous organisms, including foodborne pathogens such as Salmonella. However, how these data can be used to improve microbial risk assessment and understanding of Salmonella epidemiology remains a cha...

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Autores principales: Kuijpers, Angelina F. A., Bonacic Marinovic, Axel A., Wijnands, Lucas M., Delfgou-van Asch, Ellen H. M., van Hoek, Angela H. A. M., Franz, Eelco, Pielaat, Annemarie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6333659/
https://www.ncbi.nlm.nih.gov/pubmed/30687242
http://dx.doi.org/10.3389/fmicb.2018.03182
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author Kuijpers, Angelina F. A.
Bonacic Marinovic, Axel A.
Wijnands, Lucas M.
Delfgou-van Asch, Ellen H. M.
van Hoek, Angela H. A. M.
Franz, Eelco
Pielaat, Annemarie
author_facet Kuijpers, Angelina F. A.
Bonacic Marinovic, Axel A.
Wijnands, Lucas M.
Delfgou-van Asch, Ellen H. M.
van Hoek, Angela H. A. M.
Franz, Eelco
Pielaat, Annemarie
author_sort Kuijpers, Angelina F. A.
collection PubMed
description The increased availability of whole-genome-sequencing techniques generates a wealth of DNA data on numerous organisms, including foodborne pathogens such as Salmonella. However, how these data can be used to improve microbial risk assessment and understanding of Salmonella epidemiology remains a challenge. The aim of this study was to assess variability in in vitro virulence and genetic characteristics between and within different serovars. The phenotypic behavior of 59 strains of 32 different Salmonella enterica serovars from animal, human and food origin was assessed in an in vitro gastro-intestinal tract (GIT) system and they were analyzed for the presence of 233 putative virulence genes as markers for phenotypic prediction. The probability of in vitro infection, P(inf), defined as the fraction of infectious cells passing from inoculation to host cell invasion at the last stage of the GIT system, was interpreted as the in vitro virulence. Results showed that the (average) P(inf) of Salmonella serovars ranged from 5.3E-05 (S. Kedougou) to 5.2E-01 (S. Typhimurium). In general, a higher P(inf) on serovar level corresponded to higher reported human incidence from epidemiological reporting data. Of the 233 virulence genes investigated, only 101 showed variability in presence/absence among the strains. In vitro P(inf) was found to be positively associated with the presence of specific plasmid related virulence genes (mig-5, pef, rck, and spv). However, not all serovars with a relatively high P(inf), > 1E-02, could be linked with these specific genes. Moreover, some outbreak related strains (S. Heidelberg and S. Thompson) did not reveal this association with P(inf). No clear association with in vitro virulence P(inf) was identified when grouping serovars with the same virulence gene profile (virulence plasmid, Typhoid toxin, peg operon and stk operon). This study shows that the in vitro P(inf) variation among individual strains from the same serovar is larger than that found between serovars. Therefore, ranking P(inf) of S. enterica on serovar level alone, or in combination with a serovar specific virulence gene profile, cannot be recommended. The attribution of single biological phenomena to individual strains or serovars is not sufficient to improve the hazard characterization for S. enterica. Future microbial risk assessments, including virulence gene profiles, require a systematic approach linked to epidemiological studies rather than revealing differences in characteristics on serovar level alone.
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spelling pubmed-63336592019-01-25 Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains Kuijpers, Angelina F. A. Bonacic Marinovic, Axel A. Wijnands, Lucas M. Delfgou-van Asch, Ellen H. M. van Hoek, Angela H. A. M. Franz, Eelco Pielaat, Annemarie Front Microbiol Microbiology The increased availability of whole-genome-sequencing techniques generates a wealth of DNA data on numerous organisms, including foodborne pathogens such as Salmonella. However, how these data can be used to improve microbial risk assessment and understanding of Salmonella epidemiology remains a challenge. The aim of this study was to assess variability in in vitro virulence and genetic characteristics between and within different serovars. The phenotypic behavior of 59 strains of 32 different Salmonella enterica serovars from animal, human and food origin was assessed in an in vitro gastro-intestinal tract (GIT) system and they were analyzed for the presence of 233 putative virulence genes as markers for phenotypic prediction. The probability of in vitro infection, P(inf), defined as the fraction of infectious cells passing from inoculation to host cell invasion at the last stage of the GIT system, was interpreted as the in vitro virulence. Results showed that the (average) P(inf) of Salmonella serovars ranged from 5.3E-05 (S. Kedougou) to 5.2E-01 (S. Typhimurium). In general, a higher P(inf) on serovar level corresponded to higher reported human incidence from epidemiological reporting data. Of the 233 virulence genes investigated, only 101 showed variability in presence/absence among the strains. In vitro P(inf) was found to be positively associated with the presence of specific plasmid related virulence genes (mig-5, pef, rck, and spv). However, not all serovars with a relatively high P(inf), > 1E-02, could be linked with these specific genes. Moreover, some outbreak related strains (S. Heidelberg and S. Thompson) did not reveal this association with P(inf). No clear association with in vitro virulence P(inf) was identified when grouping serovars with the same virulence gene profile (virulence plasmid, Typhoid toxin, peg operon and stk operon). This study shows that the in vitro P(inf) variation among individual strains from the same serovar is larger than that found between serovars. Therefore, ranking P(inf) of S. enterica on serovar level alone, or in combination with a serovar specific virulence gene profile, cannot be recommended. The attribution of single biological phenomena to individual strains or serovars is not sufficient to improve the hazard characterization for S. enterica. Future microbial risk assessments, including virulence gene profiles, require a systematic approach linked to epidemiological studies rather than revealing differences in characteristics on serovar level alone. Frontiers Media S.A. 2019-01-09 /pmc/articles/PMC6333659/ /pubmed/30687242 http://dx.doi.org/10.3389/fmicb.2018.03182 Text en Copyright © 2019 Kuijpers, Bonacic Marinovic, Wijnands, Delfgou-van Asch, van Hoek, Franz and Pielaat. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Kuijpers, Angelina F. A.
Bonacic Marinovic, Axel A.
Wijnands, Lucas M.
Delfgou-van Asch, Ellen H. M.
van Hoek, Angela H. A. M.
Franz, Eelco
Pielaat, Annemarie
Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title_full Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title_fullStr Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title_full_unstemmed Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title_short Phenotypic Prediction: Linking in vitro Virulence to the Genomics of 59 Salmonella enterica Strains
title_sort phenotypic prediction: linking in vitro virulence to the genomics of 59 salmonella enterica strains
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6333659/
https://www.ncbi.nlm.nih.gov/pubmed/30687242
http://dx.doi.org/10.3389/fmicb.2018.03182
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