O antigen biogenesis sensitises Escherichia coli K-12 to bile salts, providing a plausible explanation for its evolutionary loss.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
23
05
2023
accepted:
25
09
2023
revised:
16
10
2023
medline:
23
10
2023
pubmed:
4
10
2023
entrez:
4
10
2023
Statut:
epublish
Résumé
Escherichia coli K-12 is a model organism for bacteriology and has served as a workhorse for molecular biology and biochemistry for over a century since its first isolation in 1922. However, Escherichia coli K-12 strains are phenotypically devoid of an O antigen (OAg) since early reports in the scientific literature. Recent studies have reported the presence of independent mutations that abolish OAg repeating-unit (RU) biogenesis in E. coli K-12 strains from the same original source, suggesting unknown evolutionary forces have selected for inactivation of OAg biogenesis during the early propagation of K-12. Here, we show for the first time that restoration of OAg in E. coli K-12 strain MG1655 synergistically sensitises bacteria to vancomycin with bile salts (VBS). Suppressor mutants surviving lethal doses of VBS primarily contained disruptions in OAg biogenesis. We present data supporting a model where the transient presence and accumulation of lipid-linked OAg intermediates in the periplasmic leaflet of the inner membrane interfere with peptidoglycan sacculus biosynthesis, causing growth defects that are synergistically enhanced by bile salts. Lastly, we demonstrate that continuous bile salt exposure of OAg-producing MG1655 in the laboratory, can recreate a scenario where OAg disruption is selected for as an evolutionary fitness benefit. Our work thus provides a plausible explanation for the long-held mystery of the selective pressure that may have led to the loss of OAg biogenesis in E. coli K-12; this opens new avenues for exploring long-standing questions on the intricate network coordinating the synthesis of different cell envelope components in Gram-negative bacteria.
Identifiants
pubmed: 37792901
doi: 10.1371/journal.pgen.1010996
pii: PGENETICS-D-23-00575
pmc: PMC10578602
doi:
Substances chimiques
O Antigens
0
Escherichia coli Proteins
0
Bile Acids and Salts
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010996Informations de copyright
Copyright: © 2023 Qin 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 declare no competing interest exists.
Références
J Med Microbiol. 2009 Dec;58(Pt 12):1533-1541
pubmed: 19762477
Eur J Gastroenterol Hepatol. 1997 Jul;9(7):703-9
pubmed: 9262981
Microb Pathog. 1993 Jun;14(6):433-40
pubmed: 7692209
Mol Microbiol. 2009 Aug;73(4):571-85
pubmed: 19650773
Sci Rep. 2022 Jul 8;12(1):11629
pubmed: 35804085
Microbiol Mol Biol Rev. 2003 Mar;67(1):86-156, table of contents
pubmed: 12626685
Microb Genom. 2023 Feb;9(2):
pubmed: 36745549
J Gen Microbiol. 1973 Jul;77(1):151-60
pubmed: 4579437
EcoSal Plus. 2023 Jan 9;:eesp00202022
pubmed: 36622162
Acta Pathol Microbiol Scand. 1961;51:280-90
pubmed: 13731304
J Med Microbiol. 2021 Mar;70(3):
pubmed: 33448923
Res Microbiol. 2001 Jan-Feb;152(1):17-26
pubmed: 11281321
Cold Spring Harb Symp Quant Biol. 1981;45 Pt 1:135-40
pubmed: 6271456
FEMS Microbiol Lett. 2020 May 1;367(10):
pubmed: 32407499
J Bacteriol. 1988 Jan;170(1):228-33
pubmed: 3275612
Science. 1997 Sep 5;277(5331):1453-62
pubmed: 9278503
Infect Immun. 2007 Apr;75(4):1661-6
pubmed: 17158899
Eur J Biochem. 1976 Nov 1;70(1):171-7
pubmed: 795647
Mol Microbiol. 1995 Oct;18(2):209-23
pubmed: 8709841
Microbiol Spectr. 2022 Aug 31;10(4):e0173422
pubmed: 35758683
PLoS One. 2013 Aug 08;8(8):e71097
pubmed: 23951089
Proc Natl Acad Sci U S A. 2014 Apr 22;111(16):E1610-9
pubmed: 24706920
J Bacteriol. 2022 Apr 19;204(4):e0054621
pubmed: 35293778
J Bacteriol. 1996 Apr;178(7):2102-7
pubmed: 8606190
J Bacteriol. 2014 May;196(9):1713-22
pubmed: 24532778
Appl Environ Microbiol. 2008 Aug;74(16):5015-22
pubmed: 18552194
FEMS Microbiol Lett. 2006 Oct;263(2):252-7
pubmed: 16978365
Anal Biochem. 1982 Jan 1;119(1):115-9
pubmed: 6176137
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
mBio. 2018 Aug 7;9(4):
pubmed: 30087168
Microbiology (Reading). 2014 Mar;160(Pt 3):589-601
pubmed: 24425769
J Hyg (Lond). 1905 Jul;5(3):333-79
pubmed: 20474229
Virology. 1955 Jul;1(2):190-206
pubmed: 13267987
J Bacteriol. 2003 Sep;185(17):5328-32
pubmed: 12923112
PLoS Biol. 2021 Nov 16;19(11):e3001424
pubmed: 34784345
Proc Natl Acad Sci U S A. 2010 Mar 23;107(12):5363-8
pubmed: 20203010
Microbiology (Reading). 2001 Apr;147(Pt 4):851-860
pubmed: 11283281
J Bacteriol. 1997 Apr;179(8):2512-8
pubmed: 9098046
J Mol Biol. 2009 Dec 11;394(4):644-52
pubmed: 19786035
J Bacteriol. 1994 Jul;176(13):4144-56
pubmed: 7517391
Antimicrob Agents Chemother. 2016 Nov 21;60(12):7372-7381
pubmed: 27697764
Proc Natl Acad Sci U S A. 1944 Dec 15;30(12):404-10
pubmed: 16588675
J Bacteriol. 1972 Feb;109(2):520-5
pubmed: 4333606
FEMS Microbiol Lett. 1991 Oct 1;67(2):213-8
pubmed: 1778433
Nature. 1975 Jun 5;255(5508):500-2
pubmed: 1094297
J Hyg (Lond). 1908 Jun;8(3):322-34
pubmed: 20474363
Microbiology (Reading). 1994 Jan;140 ( Pt 1):49-57
pubmed: 7512872
J Bacteriol. 1947 Jun;53(6):673-84
pubmed: 16561324
J Mol Biol. 2009 Dec 11;394(4):634-43
pubmed: 19765591
J Gen Microbiol. 1977 Oct;102(2):319-26
pubmed: 336846
mBio. 2021 Jan 26;12(1):
pubmed: 33500336
Biochem J. 1969 Jan;111(2):195-205
pubmed: 5763787
J Bacteriol. 1946 Jan;51:126
pubmed: 21065836
BMC Genomics. 2013 Jul 03;14:441
pubmed: 23822838
J Bacteriol. 2020 Dec 23;:
pubmed: 33361196
Virus Genes. 1995;11(2-3):285-97
pubmed: 8828153