The bacterial genetic determinants of Escherichia coli capacity to cause bloodstream infections in humans.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
16
06
2023
accepted:
23
06
2023
medline:
4
8
2023
pubmed:
2
8
2023
entrez:
2
8
2023
Statut:
epublish
Résumé
Escherichia coli is both a highly prevalent commensal and a major opportunistic pathogen causing bloodstream infections (BSI). A systematic analysis characterizing the genomic determinants of extra-intestinal pathogenic vs. commensal isolates in human populations, which could inform mechanisms of pathogenesis, diagnostic, prevention and treatment is still lacking. We used a collection of 912 BSI and 370 commensal E. coli isolates collected in France over a 17-year period (2000-2017). We compared their pangenomes, genetic backgrounds (phylogroups, STs, O groups), presence of virulence-associated genes (VAGs) and antimicrobial resistance genes, finding significant differences in all comparisons between commensal and BSI isolates. A machine learning linear model trained on all the genetic variants derived from the pangenome and controlling for population structure reveals similar differences in VAGs, discovers new variants associated with pathogenicity (capacity to cause BSI), and accurately classifies BSI vs. commensal strains. Pathogenicity is a highly heritable trait, with up to 69% of the variance explained by bacterial genetic variants. Lastly, complementing our commensal collection with an older collection from 1980, we predict that pathogenicity continuously increased through 1980, 2000, to 2010. Together our findings imply that E. coli exhibit substantial genetic variation contributing to the transition between commensalism and pathogenicity and that this species evolved towards higher pathogenicity.
Identifiants
pubmed: 37531401
doi: 10.1371/journal.pgen.1010842
pii: PGENETICS-D-23-00441
pmc: PMC10395866
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010842Informations de copyright
Copyright: © 2023 Burgaya et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Microb Genom. 2020 Mar;6(3):
pubmed: 32100713
Clin Microbiol Rev. 1991 Jan;4(1):80-128
pubmed: 1672263
ACS Chem Biol. 2014 Sep 19;9(9):2058-66
pubmed: 24988330
Kidney Int. 2007 Jul;72(1):19-25
pubmed: 17396114
J Hosp Infect. 2019 Feb;101(2):120-128
pubmed: 30403958
Infect Immun. 1981 Feb;31(2):564-70
pubmed: 7012012
Clin Microbiol Infect. 2015 Mar;21(3):251.e1-8
pubmed: 25698659
Genetics. 2017 May;206(1):363-376
pubmed: 28280056
PLoS Med. 2011 Oct;8(10):e1001104
pubmed: 22022233
Microb Genom. 2016 Jul 11;2(7):e000064
pubmed: 28348859
Epidemiol Infect. 2017 Apr;145(5):872-882
pubmed: 28029088
J Infect Dis. 1977 Sep;136(3):346-53
pubmed: 333035
J Clin Microbiol. 2012 Feb;50(2):449-56
pubmed: 22075599
Bioinformatics. 2009 Jun 1;25(11):1422-3
pubmed: 19304878
Int J Antimicrob Agents. 2010 Sep;36(3):284-7
pubmed: 20580534
Nucleic Acids Res. 2010 Mar;38(5):1723-37
pubmed: 20007596
Microbiol Spectr. 2022 Dec 21;10(6):e0255422
pubmed: 36409140
J Infect Dis. 1986 Oct;154(4):727-8
pubmed: 3528324
Clin Microbiol Infect. 2022 Jun;28(6):879.e1-879.e7
pubmed: 34922002
PLoS Genet. 2019 Apr 25;15(4):e1008059
pubmed: 31022167
Nat Commun. 2022 Aug 1;13(1):4459
pubmed: 35915063
Infect Immun. 2016 Mar 24;84(4):1112-1122
pubmed: 26831466
Elife. 2019 Feb 22;8:
pubmed: 30794157
Bioinformatics. 2018 Dec 15;34(24):4310-4312
pubmed: 30535304
Nat Commun. 2019 May 15;10(1):2176
pubmed: 31092817
J Bacteriol. 2010 Oct;192(19):4885-93
pubmed: 20656906
Genome Res. 2015 Jan;25(1):119-28
pubmed: 25373147
J Infect Dis. 1990 Apr;161(4):794-6
pubmed: 2181035
Microb Genom. 2021 Sep;7(9):
pubmed: 34559043
Mol Biol Evol. 2007 Nov;24(11):2373-84
pubmed: 17709333
Appl Environ Microbiol. 2004 Sep;70(9):5698-700
pubmed: 15345464
Bioinformatics. 2019 Feb 1;35(3):526-528
pubmed: 30016406
Nat Rev Genet. 2008 Apr;9(4):255-66
pubmed: 18319743
PLoS Genet. 2018 Nov 12;14(11):e1007758
pubmed: 30419019
Gut Pathog. 2019 Aug 01;11:42
pubmed: 31388358
Mol Microbiol. 2018 Sep;109(6):745-762
pubmed: 29884996
J Infect Dis. 2019 Jan 1;219(1):121-132
pubmed: 30085181
Infection. 2011 Oct;39(5):467-71
pubmed: 21826438
J Bacteriol. 2014 Dec;196(24):4276-84
pubmed: 25266386
Nat Commun. 2023 Jun 20;14(1):3667
pubmed: 37339949
Lancet Infect Dis. 2019 Jun;19(6):631-640
pubmed: 31079947
Lancet. 1981 Dec 19-26;2(8260-61):1369-72
pubmed: 6171697
Int J Med Microbiol. 2013 Dec;303(8):529-32
pubmed: 23927963
PLoS Pathog. 2022 Jun 14;18(6):e1010582
pubmed: 35700218
Nat Methods. 2020 Mar;17(3):261-272
pubmed: 32015543
J Clin Microbiol. 2008 Aug;46(8):2529-34
pubmed: 18495863
Genome Res. 2020 Jan;30(1):138-152
pubmed: 31809257
J Antimicrob Chemother. 2008 Feb;61(2):273-81
pubmed: 18077311
PLoS Genet. 2020 Oct 28;16(10):e1009065
pubmed: 33112851
PLoS Pathog. 2021 Oct 18;17(10):e1009992
pubmed: 34662348
Nat Commun. 2020 Nov 24;11(1):5968
pubmed: 33235212
Lancet Microbe. 2021 Jul;2(7):e331-e341
pubmed: 35544167
Genome Biol. 2020 Sep 17;21(1):249
pubmed: 32943081
mSphere. 2017 Nov 22;2(6):
pubmed: 29205229
J Clin Microbiol. 2004 Dec;42(12):5444-52
pubmed: 15583263
Lancet Infect Dis. 2017 May;17(5):528-537
pubmed: 28238601
Infect Immun. 1999 Aug;67(8):3703-13
pubmed: 10417127
Emerg Infect Dis. 2017 Nov;23(11):1815-1825
pubmed: 29047423
Sci Rep. 2018 Jul 18;8(1):10872
pubmed: 30022098
Mol Microbiol. 2008 Mar;67(5):996-1011
pubmed: 18208494
Antimicrob Agents Chemother. 2019 May 24;63(6):
pubmed: 30936104
Clin Infect Dis. 2021 Apr 8;72(7):1211-1219
pubmed: 32406495
Microorganisms. 2016 Feb 16;4(1):
pubmed: 27681908
Nat Rev Microbiol. 2010 Mar;8(3):207-17
pubmed: 20157339
J Antimicrob Chemother. 2019 Jun 1;74(6):1521-1530
pubmed: 30863849
Clin Microbiol Infect. 2008 Nov;14(11):1041-7
pubmed: 19040476
Genome Med. 2021 May 5;13(1):77
pubmed: 33952335
Mol Biol Evol. 2016 Apr;33(4):898-914
pubmed: 26613786
Microb Genom. 2021 Nov;7(11):
pubmed: 34812717
Mol Microbiol. 2013 Mar;87(6):1200-22
pubmed: 23347101
Nat Methods. 2018 Jul;15(7):475-476
pubmed: 29967506
J Bacteriol. 1994 Apr;176(8):2308-11
pubmed: 8157599
Appl Environ Microbiol. 2011 Apr;77(7):2303-8
pubmed: 21317254
Appl Environ Microbiol. 2022 Aug 9;88(15):e0066422
pubmed: 35862685
Proc Natl Acad Sci U S A. 2014 Apr 15;111(15):5694-9
pubmed: 24706808
mBio. 2020 Jul 7;11(4):
pubmed: 32636251
J Antimicrob Chemother. 2020 Aug 1;75(8):2334-2343
pubmed: 32417924
PLoS Genet. 2022 Mar 24;18(3):e1010112
pubmed: 35324915
Int J Antimicrob Agents. 2018 Sep;52(3):430-435
pubmed: 29966679
Microbiology (Reading). 2001 Jun;147(Pt 6):1671-1676
pubmed: 11390698
EcoSal Plus. 2006 Jan;2(1):
pubmed: 26443571
F1000Res. 2021 Jan 18;10:33
pubmed: 34035898
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Genome Res. 2023 Jan;33(1):129-140
pubmed: 36669850
Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10637-42
pubmed: 17563352
Infect Immun. 2000 Jan;68(1):424-5
pubmed: 10636718
Infect Immun. 1999 Feb;67(2):546-53
pubmed: 9916057
J Immunol. 1947 Sep;57(1):71-100
pubmed: 20264689
Int J Med Microbiol. 2010 Nov;300(7):435-9
pubmed: 20510652
Commun Biol. 2022 Jul 28;5(1):752
pubmed: 35902767
J Gen Microbiol. 1986 Jul;132(7):1853-8
pubmed: 3540189
Mol Microbiol. 2006 Jun;60(5):1136-51
pubmed: 16689791
Genome Biol. 2020 Jul 22;21(1):180
pubmed: 32698896
Elife. 2022 Jul 26;11:
pubmed: 35881438
Pediatr Res. 2003 Jul;54(1):8-14
pubmed: 12700366
Antimicrob Agents Chemother. 2013 Sep;57(9):4512-7
pubmed: 23836184
Front Cell Infect Microbiol. 2018 Jun 22;8:208
pubmed: 29988395
Microorganisms. 2022 Mar 21;10(3):
pubmed: 35336241
Proc Natl Acad Sci U S A. 1989 Jun;86(12):4357-61
pubmed: 2567514
Infect Immun. 2002 Mar;70(3):1225-9
pubmed: 11854204
FASEB J. 2010 Apr;24(4):1160-6
pubmed: 19917674
Genome Res. 2017 Jul 18;:
pubmed: 28720578
Nat Commun. 2023 Mar 18;14(1):1530
pubmed: 36934086
Microb Genom. 2016 Nov 30;2(11):e000093
pubmed: 28348833
Microbiology (Reading). 2016 Apr;162(4):642-650
pubmed: 26822436
Genetics. 2018 Mar;208(3):1247-1260
pubmed: 29330348
Infect Immun. 2021 May 17;89(6):
pubmed: 33753414
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Infect Immun. 2006 Feb;74(2):1387-93
pubmed: 16428790
J Bacteriol. 1986 Feb;165(2):570-8
pubmed: 2935523
J Clin Microbiol. 2011 Mar;49(3):777-83
pubmed: 21177892
Curr Microbiol. 2015 Aug;71(2):274-82
pubmed: 26037379