Non-pathogenic Escherichia coli acquires virulence by mutating a growth-essential LPS transporter.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
04 2020
Historique:
received: 10 07 2019
accepted: 09 03 2020
entrez: 24 4 2020
pubmed: 24 4 2020
medline: 5 8 2020
Statut: epublish

Résumé

The molecular mechanisms that allow pathogenic bacteria to infect animals have been intensively studied. On the other hand, the molecular mechanisms by which bacteria acquire virulence functions are not fully understood. In the present study, we experimentally evaluated the evolution of a non-pathogenic strain of Escherichia coli in a silkworm infection model and obtained pathogenic mutant strains. As one cause of the high virulence properties of E. coli mutants, we identified amino acid substitutions in LptD (G580S) and LptE (T95I) constituting the lipopolysaccharide (LPS) transporter, which translocates LPS from the inner to the outer membrane and is essential for E. coli growth. The growth of the LptD and LptE mutants obtained in this study was indistinguishable from that of the parent strain. The LptD and LptE mutants exhibited increased secretion of outer membrane vesicles containing LPS and resistance against various antibiotics, antimicrobial peptides, and host complement. In vivo cross-linking studies revealed that the conformation of the LptD-LptE complex was altered in the LptD and LptE mutants. Furthermore, several clinical isolates of E. coli carried amino acid substitutions of LptD and LptE that conferred resistance against antimicrobial substances. This study demonstrated an experimental evolution of bacterial virulence properties in an animal infection model and identified functional alterations of the growth-essential LPS transporter that led to high bacterial virulence by conferring resistance against antimicrobial substances. These findings suggest that non-pathogenic bacteria can gain virulence traits by changing the functions of essential genes, and provide new insight to bacterial evolution in a host environment.

Identifiants

pubmed: 32324807
doi: 10.1371/journal.ppat.1008469
pii: PPATHOGENS-D-19-01261
pmc: PMC7179839
doi:

Substances chimiques

Bacterial Outer Membrane Proteins 0
Escherichia coli Proteins 0
Lipopolysaccharides 0
LptD protein, E coli 0
LptE protein, E coli 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008469

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):E1904-E1912
pubmed: 28202733
Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11754-9
pubmed: 16861298
Infect Immun. 2011 Oct;79(10):4218-26
pubmed: 21825069
Curr Opin Microbiol. 2013 Dec;16(6):779-85
pubmed: 24148302
Methods Mol Biol. 2011;765:71-82
pubmed: 21815087
J Bacteriol. 2004 Nov;186(21):7112-22
pubmed: 15489422
Nat Rev Microbiol. 2015 Oct;13(10):605-19
pubmed: 26373371
Microbiol Mol Biol Rev. 2003 Dec;67(4):593-656
pubmed: 14665678
Heredity (Edinb). 2008 May;100(5):453-63
pubmed: 18212807
J Virol. 2014 Nov;88(21):12572-85
pubmed: 25142579
Proc Natl Acad Sci U S A. 2010 Mar 23;107(12):5363-8
pubmed: 20203010
J Bacteriol. 2013 Sep;195(18):4161-73
pubmed: 23852867
Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6742-6
pubmed: 11381128
Cell. 2005 Apr 22;121(2):307-17
pubmed: 15851036
Mol Microbiol. 2002 Sep;45(5):1289-302
pubmed: 12207697
Photosynth Res. 2007 May;92(2):245-59
pubmed: 17634749
FEMS Microbiol Lett. 2012 Aug;333(1):59-68
pubmed: 22612664
Genes Dev. 2005 Nov 15;19(22):2645-55
pubmed: 16291643
Proc Natl Acad Sci U S A. 2013 May 7;110(19):7642-7
pubmed: 23613592
Appl Environ Microbiol. 2005 Aug;71(8):4248-53
pubmed: 16085810
Microbiology. 2003 May;149(Pt 5):1265-1273
pubmed: 12724388
Can J Biochem Physiol. 1959 Aug;37(8):911-7
pubmed: 13671378
Nat Rev Microbiol. 2009 Sep;7(9):677-83
pubmed: 19633680
Microb Pathog. 2002 Apr;32(4):183-90
pubmed: 12079408
Proc Natl Acad Sci U S A. 2011 Feb 8;108(6):2486-91
pubmed: 21257904
Nat Commun. 2014 Jul 08;5:4352
pubmed: 25000950
Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12245-50
pubmed: 20566849
Mol Microbiol. 2005 May;56(4):934-44
pubmed: 15853881
Methods Mol Biol. 2008;416:195-204
pubmed: 18392969
BMC Microbiol. 2011 Dec 01;11:258
pubmed: 22133164
Plant J. 2005 Feb;41(3):478-92
pubmed: 15659105
J Biol Chem. 2014 May 16;289(20):14412-21
pubmed: 24706746
Nature. 2014 Jul 3;511(7507):108-11
pubmed: 24990751
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Science. 1999 Jul 16;285(5426):422-4
pubmed: 10411508
Infect Immun. 2010 Sep;78(9):3822-31
pubmed: 20605984
Cell Chem Biol. 2016 Feb 18;23(2):267-277
pubmed: 26853624
Nature. 2014 Jul 3;511(7507):52-6
pubmed: 24990744
Structure. 2016 Jun 7;24(6):965-976
pubmed: 27161977
PLoS Pathog. 2012;8(5):e1002731
pubmed: 22693450

Auteurs

Chikara Kaito (C)

Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama University, Kita-ku, Okayama, Japan.
Graduate School of Pharmaceutical Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Hirono Yoshikai (H)

Graduate School of Pharmaceutical Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Ai Wakamatsu (A)

Japan Biological Informatics Consortium (JBIC), Koto-ku, Tokyo, Japan.

Atsushi Miyashita (A)

Graduate School of Pharmaceutical Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.

Yasuhiko Matsumoto (Y)

Department of Microbiology, Meiji Pharmaceutical University, Kiyose, Tokyo, Japan.

Tomoko Fujiyuki (T)

The Institute of Medical Science, The University of Tokyo, Minato-ku, Tokyo, Japan.

Masaru Kato (M)

Devision of Bioanalytical Chemistry, School of Pharmacy, Showa University, Shinagawa-ku, Tokyo, Japan.

Yoshitoshi Ogura (Y)

Department of Bacteriology, Faculty of Medical Sciences, Kyushu University, Fukuoka, Japan.

Tetsuya Hayashi (T)

Department of Bacteriology, Faculty of Medical Sciences, Kyushu University, Fukuoka, Japan.

Takao Isogai (T)

Translational Research Center, Fukushima Medical University, Fukushima, Japan.

Kazuhisa Sekimizu (K)

Institute of Medical Mycology, Teikyo University, Hachioji, Tokyo, Japan.

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Classifications MeSH