Metabolic adaptation to consume butyrate under prolonged resource exhaustion.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
08
03
2023
accepted:
02
06
2023
revised:
05
07
2023
medline:
7
7
2023
pubmed:
22
6
2023
entrez:
22
6
2023
Statut:
epublish
Résumé
Bacteria must often survive following the exhaustion of their external growth resources. Fitting with this need, many bacterial species that cannot sporulate, can enter a state known as long term stationary phase (LTSP) in which they can persist for years within spent media. Several recent studies have revealed the dynamics of genetic adaptation of Escherichia coli under LTSP. Yet, the metabolic consequences of such genetic adaptation were not addressed. Here, we characterized the metabolic changes LTSP populations experience, over the first 32 days under LTSP. This allowed us to link genetic adaptations observed in a convergent manner across LTSP populations back to their metabolic adaptive effect. Specifically, we demonstrate that through the acquisition of mutations combinations in specific sets of metabolic genes, E. coli acquires the ability to consume the short chain fatty acid butyrate. Intriguingly, this fatty acid is not initially present within the rich media we used in this study. Instead, it is E. coli itself that produces butyrate during its initial growth within fresh rich media. The mutations that enable butyrate consumption allow E. coli to grow on butyrate. However, the clones carrying these mutations rapidly decrease in frequency, once the butyrate is consumed, likely reflecting an associated cost to fitness. Yet despite this, E. coli populations show a remarkable capability of maintaining these genotypes at low frequency, as standing variation. This in turn allows them to more rapidly re-adapt to consume butyrate, once it again becomes available to them.
Identifiants
pubmed: 37347785
doi: 10.1371/journal.pgen.1010812
pii: PGENETICS-D-23-00263
pmc: PMC10321620
doi:
Substances chimiques
Butyrates
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1010812Informations de copyright
Copyright: © 2023 Katz 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
PLoS One. 2016 Jul 28;11(7):e0160035
pubmed: 27466817
Mol Ecol. 2020 Jan;29(1):138-148
pubmed: 31725941
Genome Biol Evol. 2020 Dec 6;12(12):2292-2301
pubmed: 33283867
PLoS Biol. 2012;10(5):e1001325
pubmed: 22589700
Genetics. 1976 Sep;84(1):145-57
pubmed: 992363
Methods Enzymol. 2015;561:171-96
pubmed: 26358905
Nat Commun. 2019 Feb 21;10(1):890
pubmed: 30792386
Nat Commun. 2020 Jan 14;11(1):279
pubmed: 31937786
Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):5881-6
pubmed: 20231463
Genomics. 2014 Dec;104(6 Pt A):399-405
pubmed: 25281774
Science. 1993 Mar 19;259(5102):1757-60
pubmed: 7681219
Cancer Metab. 2016 Sep 02;4(1):17
pubmed: 27594997
Sci Adv. 2016 Oct 28;2(10):e1601273
pubmed: 27819051
Evol Appl. 2018 Jan 02;11(1):60-75
pubmed: 29302272
Microbiology (Reading). 2009 Feb;155(Pt 2):521-530
pubmed: 19202100
Mol Biol Evol. 2021 Jun 25;38(7):2778-2790
pubmed: 33734381
mSphere. 2020 Aug 12;5(4):
pubmed: 32817448
Appl Environ Microbiol. 2013 Feb;79(3):1008-17
pubmed: 23204426
mBio. 2014 Apr 22;5(2):e00889
pubmed: 24757212
Appl Environ Microbiol. 2014 May;80(9):2901-9
pubmed: 24584250
Nat Rev Genet. 2013 Dec;14(12):827-39
pubmed: 24166031
Mol Biol Evol. 2017 Jul 1;34(7):1758-1769
pubmed: 28369614
Sci Rep. 2018 Jan 12;8(1):609
pubmed: 29330542
EMBO J. 2000 Oct 2;19(19):5167-77
pubmed: 11013219
PLoS One. 2015 May 22;10(5):e0128036
pubmed: 26000737
Biochem Biophys Res Commun. 1967 Oct 11;29(1):28-33
pubmed: 4861587
Nat Commun. 2019 Jul 26;10(1):3354
pubmed: 31350417
J Bacteriol. 1943 Jun;45(6):555-64
pubmed: 16560666
Biotechnol J. 2013 Sep;8(9):1105-14
pubmed: 23744758
Microb Cell Fact. 2004 Jun 16;3(1):8
pubmed: 15200682
J Inflamm Res. 2021 Nov 18;14:6025-6041
pubmed: 34819742
mSphere. 2017 May 24;2(3):
pubmed: 28567442
Anal Biochem. 2000 Aug 1;283(2):192-9
pubmed: 10906239
Mol Microbiol. 2002 Dec;46(5):1451-64
pubmed: 12453229
Curr Microbiol. 2009 Dec;59(6):656-63
pubmed: 19727942
Nat Commun. 2020 Feb 3;11(1):670
pubmed: 32015341
Transl Cancer Res. 2016 Sep;5(Suppl 3):S526-S528
pubmed: 30568890
Genetics. 2005 Apr;169(4):1807-14
pubmed: 15687275
Nature. 2017 Nov 2;551(7678):45-50
pubmed: 29045390
Nat Rev Microbiol. 2006 Feb;4(2):113-20
pubmed: 16415927
mBio. 2021 Jan 26;12(1):
pubmed: 33500336
Biomed Pharmacother. 2022 Jan;145:112352
pubmed: 34840032
Methods Mol Biol. 2014;1151:165-88
pubmed: 24838886