Assessment of plasmids for relating the 2020 Salmonella enterica serovar Newport onion outbreak to farms implicated by the outbreak investigation.
Mobilome
Molecular epidemiology
Pangenome
Plasmid
Salmonella enterica
Salmonella enterica Newport
Source tracking
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
04 Apr 2023
04 Apr 2023
Historique:
received:
14
10
2022
accepted:
13
03
2023
medline:
6
4
2023
entrez:
4
4
2023
pubmed:
5
4
2023
Statut:
epublish
Résumé
The Salmonella enterica serovar Newport red onion outbreak of 2020 was the largest foodborne outbreak of Salmonella in over a decade. The epidemiological investigation suggested two farms as the likely source of contamination. However, single nucleotide polymorphism (SNP) analysis of the whole genome sequencing data showed that none of the Salmonella isolates collected from the farm regions were linked to the clinical isolates-preventing the use of phylogenetics in source identification. Here, we explored an alternative method for analyzing the whole genome sequencing data driven by the hypothesis that if the outbreak strain had come from the farm regions, then the clinical isolates would disproportionately contain plasmids found in isolates from the farm regions due to horizontal transfer. SNP analysis confirmed that the clinical isolates formed a single, nearly-clonal clade with evidence for ancestry in California going back a decade. The clinical clade had a large core genome (4,399 genes) and a large and sparsely distributed accessory genome (2,577 genes, at least 64% on plasmids). At least 20 plasmid types occurred in the clinical clade, more than were found in the literature for Salmonella Newport. A small number of plasmids, 14 from 13 clinical isolates and 17 from 8 farm isolates, were found to be highly similar (> 95% identical)-indicating they might be related by horizontal transfer. Phylogenetic analysis was unable to determine the geographic origin, isolation source, or time of transfer of the plasmids, likely due to their promiscuous and transient nature. However, our resampling analysis suggested that observing a similar number and combination of highly similar plasmids in random samples of environmental Salmonella enterica within the NCBI Pathogen Detection database was unlikely, supporting a connection between the outbreak strain and the farms implicated by the epidemiological investigation. Horizontally transferred plasmids provided evidence for a connection between clinical isolates and the farms implicated as the source of the outbreak. Our case study suggests that such analyses might add a new dimension to source tracking investigations, but highlights the need for detailed and accurate metadata, more extensive environmental sampling, and a better understanding of plasmid molecular evolution.
Sections du résumé
BACKGROUND
BACKGROUND
The Salmonella enterica serovar Newport red onion outbreak of 2020 was the largest foodborne outbreak of Salmonella in over a decade. The epidemiological investigation suggested two farms as the likely source of contamination. However, single nucleotide polymorphism (SNP) analysis of the whole genome sequencing data showed that none of the Salmonella isolates collected from the farm regions were linked to the clinical isolates-preventing the use of phylogenetics in source identification. Here, we explored an alternative method for analyzing the whole genome sequencing data driven by the hypothesis that if the outbreak strain had come from the farm regions, then the clinical isolates would disproportionately contain plasmids found in isolates from the farm regions due to horizontal transfer.
RESULTS
RESULTS
SNP analysis confirmed that the clinical isolates formed a single, nearly-clonal clade with evidence for ancestry in California going back a decade. The clinical clade had a large core genome (4,399 genes) and a large and sparsely distributed accessory genome (2,577 genes, at least 64% on plasmids). At least 20 plasmid types occurred in the clinical clade, more than were found in the literature for Salmonella Newport. A small number of plasmids, 14 from 13 clinical isolates and 17 from 8 farm isolates, were found to be highly similar (> 95% identical)-indicating they might be related by horizontal transfer. Phylogenetic analysis was unable to determine the geographic origin, isolation source, or time of transfer of the plasmids, likely due to their promiscuous and transient nature. However, our resampling analysis suggested that observing a similar number and combination of highly similar plasmids in random samples of environmental Salmonella enterica within the NCBI Pathogen Detection database was unlikely, supporting a connection between the outbreak strain and the farms implicated by the epidemiological investigation.
CONCLUSION
CONCLUSIONS
Horizontally transferred plasmids provided evidence for a connection between clinical isolates and the farms implicated as the source of the outbreak. Our case study suggests that such analyses might add a new dimension to source tracking investigations, but highlights the need for detailed and accurate metadata, more extensive environmental sampling, and a better understanding of plasmid molecular evolution.
Identifiants
pubmed: 37016310
doi: 10.1186/s12864-023-09245-0
pii: 10.1186/s12864-023-09245-0
pmc: PMC10074901
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
165Subventions
Organisme : Joint Institute for Food Safety and Applied Nutrition, University of Maryland
ID : 5U01-FD001418
Informations de copyright
© 2023. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.
Références
BMC Genomics. 2020 Nov 25;21(1):829
pubmed: 33238876
Nat Rev Genet. 2018 Sep;19(9):549-565
pubmed: 29973680
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Bioinformatics. 2018 Jan 15;34(2):292-293
pubmed: 29028899
Front Microbiol. 2020 Jul 22;11:1729
pubmed: 32793169
Appl Environ Microbiol. 2006 Sep;72(9):5777-83
pubmed: 16957193
PLoS Comput Biol. 2017 Jun 8;13(6):e1005595
pubmed: 28594827
Nat Rev Microbiol. 2022 Apr;20(4):206-218
pubmed: 34773098
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
PLoS One. 2013;8(2):e55687
pubmed: 23409020
Cell Mol Life Sci. 2002 Dec;59(12):2071-82
pubmed: 12568333
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Mol Biol Evol. 2017 Aug 1;34(8):2115-2122
pubmed: 28460117
Plasmid. 2018 Sep;99:56-67
pubmed: 30086339
Front Microbiol. 2018 Jan 23;9:23
pubmed: 29410657
Nat Biotechnol. 2017 Nov;35(11):1026-1028
pubmed: 29035372
PLoS One. 2018 Aug 31;13(8):e0202286
pubmed: 30169497
PLoS One. 2016 Nov 10;11(11):e0166162
pubmed: 27832109
Bioinformatics. 2015 Nov 15;31(22):3691-3
pubmed: 26198102
Foodborne Pathog Dis. 2018 Jun;15(6):361-371
pubmed: 29620958
Nat Commun. 2019 Nov 26;10(1):5376
pubmed: 31772262
Proc Natl Acad Sci U S A. 2020 Jun 9;117(23):12518-12519
pubmed: 32381733
mBio. 2012 Jul 03;3(4):e00077-12
pubmed: 22761390
J Glob Antimicrob Resist. 2017 Dec;11:123-132
pubmed: 28801276
Trends Microbiol. 2018 Dec;26(12):986-998
pubmed: 29954653
Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13950-5
pubmed: 16172379
Mol Microbiol. 1999 Aug;33(3):612-22
pubmed: 10417651
Mol Biol Evol. 2022 Jun 2;39(6):
pubmed: 35639760
Mol Ecol. 2017 Apr;26(7):1832-1847
pubmed: 28206693
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296
pubmed: 33885785
Front Microbiol. 2018 May 18;9:877
pubmed: 29867794
BMC Bioinformatics. 2021 Jul 31;22(1):390
pubmed: 34332528
Antimicrob Agents Chemother. 2018 Jun 26;62(7):
pubmed: 29760131
Plasmid. 2020 Mar;108:102477
pubmed: 31870701
Front Microbiol. 2020 Oct 08;11:562181
pubmed: 33133037
Clin Infect Dis. 2010 Mar 15;50(6):882-9
pubmed: 20158401
Mol Biol Evol. 2020 May 1;37(5):1530-1534
pubmed: 32011700
Genetics. 2010 Apr;184(4):1133-9
pubmed: 20124027
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
Plasmid. 2017 May;91:90-95
pubmed: 28461121
Syst Biol. 2014 Sep;63(5):812-8
pubmed: 24789072
Ann N Y Acad Sci. 2015 Sep;1354:12-31
pubmed: 26190223
Philos Trans R Soc Lond B Biol Sci. 2022 Oct 10;377(1861):20210234
pubmed: 35989606
BMC Genomics. 2020 Mar 5;21(Suppl 1):106
pubmed: 32138652
Microb Genom. 2020 Oct;6(10):
pubmed: 32579097
Plasmid. 2006 Nov;56(3):228-32
pubmed: 16828160
Nat Commun. 2020 May 15;11(1):2452
pubmed: 32415210
Nat Commun. 2020 Jul 17;11(1):3602
pubmed: 32681114
Emerg Microbes Infect. 2020 Dec;9(1):535-538
pubmed: 32122270
PLoS One. 2018 Mar 07;13(3):e0193435
pubmed: 29513730
Wellcome Open Res. 2018 Sep 24;3:124
pubmed: 30345391
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
mBio. 2016 Sep 06;7(5):
pubmed: 27601577
Nature. 2000 May 18;405(6784):299-304
pubmed: 10830951
Genome Biol Evol. 2017 Apr 1;9(4):1047-1050
pubmed: 28379364
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Microbiol Mol Biol Rev. 2021 Apr 28;85(2):
pubmed: 33910982