Xenosiderophore Utilization Promotes Bacteroides thetaiotaomicron Resilience during Colitis.
bacteroidetes
gut inflammation
gut microbiota resilience
iron metabolism
siderophore
Journal
Cell host & microbe
ISSN: 1934-6069
Titre abrégé: Cell Host Microbe
Pays: United States
ID NLM: 101302316
Informations de publication
Date de publication:
11 03 2020
11 03 2020
Historique:
received:
02
08
2019
revised:
02
12
2019
accepted:
16
01
2020
pubmed:
23
2
2020
medline:
24
3
2020
entrez:
21
2
2020
Statut:
ppublish
Résumé
During short-lived perturbations, such as inflammation, the gut microbiota exhibits resilience and reverts to its original configuration. Although microbial access to the micronutrient iron is decreased during colitis, pathogens can scavenge iron by using siderophores. How commensal bacteria acquire iron during gut inflammation is incompletely understood. Curiously, the human commensal Bacteroides thetaiotaomicron does not produce siderophores but grows under iron-limiting conditions using enterobacterial siderophores. Using RNA-seq, we identify B. thetaiotaomicron genes that were upregulated during Salmonella-induced gut inflammation and were predicted to be involved in iron uptake. Mutants in the xusABC locus (BT2063-2065) were defective for xenosiderophore-mediated iron uptake in vitro. In the normal mouse gut, the XusABC system was dispensable, while a xusA mutant colonized poorly during colitis. This work identifies xenosiderophore utilization as a critical mechanism for B. thetaiotaomicron to sustain colonization during inflammation and suggests a mechanism of how interphylum iron metabolism contributes to gut microbiota resilience.
Identifiants
pubmed: 32075741
pii: S1931-3128(20)30049-4
doi: 10.1016/j.chom.2020.01.010
pmc: PMC7439322
mid: NIHMS1568769
pii:
doi:
Substances chimiques
Siderophores
0
Iron
E1UOL152H7
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
376-388.e8Subventions
Organisme : NIAID NIH HHS
ID : R01 AI118807
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK070855
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI128151
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Informations de copyright
Copyright © 2020 Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of Interests The corresponding author (S.E.W.) is listed as an inventor on patent application WO2014200929A1, which describes a treatment to prevent the inflammation-associated expansion of Enterobacteriaceae. The other authors declare no competing interests.
Références
Nat Rev Microbiol. 2012 Jul 16;10(8):525-37
pubmed: 22796883
Science. 2015 Jan 9;347(6218):170-5
pubmed: 25574022
Cell Host Microbe. 2018 Aug 8;24(2):296-307.e7
pubmed: 30057174
Infect Immun. 2008 Mar;76(3):907-15
pubmed: 18160481
Cell Host Microbe. 2009 May 8;5(5):476-86
pubmed: 19454351
J Bacteriol. 1999 Jun;181(11):3610-2
pubmed: 10348879
Cell Host Microbe. 2009 Sep 17;6(3):279-89
pubmed: 19748469
Structure. 2008 Jul;16(7):1105-15
pubmed: 18611383
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Science. 2013 Jul 5;341(6141):1237439
pubmed: 23828941
Nat Rev Gastroenterol Hepatol. 2018 Aug;15(8):457-458
pubmed: 29752457
Gastroenterology. 2017 Dec;153(6):1621-1633.e6
pubmed: 28823860
Cell Microbiol. 2008 Apr;10(4):876-90
pubmed: 18034866
Sci Rep. 2018 Sep 26;8(1):14430
pubmed: 30258117
J Mol Biol. 2014 Nov 25;426(23):3851-65
pubmed: 25026064
Cell Host Microbe. 2014 Dec 10;16(6):759-69
pubmed: 25498343
J Bacteriol. 1978 Jun;134(3):1141-56
pubmed: 149110
Cell Host Microbe. 2013 Jul 17;14(1):26-37
pubmed: 23870311
Bioinformatics. 2019 Feb 1;35(3):421-432
pubmed: 30020410
Infect Immun. 2015 Jan;83(1):300-10
pubmed: 25368114
Gut Microbes. 2014 Jan-Feb;5(1):71-3
pubmed: 24637596
Mol Microbiol. 2014 Sep;93(6):1314-26
pubmed: 25081030
Mol Gen Genet. 1972;119(1):75-88
pubmed: 4564719
J Bacteriol. 1971 Apr;106(1):51-7
pubmed: 4928016
Infect Immun. 2019 Mar 25;87(4):
pubmed: 30617205
Appl Environ Microbiol. 1997 Jul;63(7):2593-9
pubmed: 9212409
J Bacteriol. 2004 Aug;186(16):5432-41
pubmed: 15292145
Biometals. 2009 Aug;22(4):691-5
pubmed: 19214756
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):3677-82
pubmed: 12655053
FEMS Microbiol Lett. 1991 Nov 1;68(1):45-50
pubmed: 1769555
Int J Hyperthermia. 2018 Jun;34(4):373-381
pubmed: 28758530
Infect Immun. 2003 Dec;71(12):6953-61
pubmed: 14638784
J Bacteriol. 1976 Jun;126(3):1052-62
pubmed: 7543
Science. 2003 Mar 28;299(5615):2074-6
pubmed: 12663928
Genome Biol. 2014;15(12):550
pubmed: 25516281
J Biomol Tech. 2003 Mar;14(1):33-43
pubmed: 12901609
Nat Rev Microbiol. 2017 Oct;15(10):630-638
pubmed: 28626231
J Biol Chem. 1993 Aug 5;268(22):16302-8
pubmed: 8344918
Cell Host Microbe. 2018 Jun 13;23(6):737-748
pubmed: 29902439
Microbiologyopen. 2017 Aug;6(4):
pubmed: 28397401
Cell Host Microbe. 2010 Sep 16;8(3):292-300
pubmed: 20833380
Proc Natl Acad Sci U S A. 2016 Nov 22;113(47):13462-13467
pubmed: 27821741
mBio. 2017 May 23;8(3):
pubmed: 28536292
J Bacteriol. 1982 Mar;149(3):880-8
pubmed: 6174499
Curr Opin Microbiol. 2014 Feb;17:67-74
pubmed: 24581695
Lancet. 1999 Aug 21;354(9179):635-9
pubmed: 10466665
Cell Host Microbe. 2012 Mar 15;11(3):227-39
pubmed: 22423963
Cell. 2017 Apr 20;169(3):547-558.e15
pubmed: 28431252
Nature. 2013 Dec 19;504(7480):451-5
pubmed: 24226773
Cell Host Microbe. 2017 Feb 8;21(2):208-219
pubmed: 28182951
Cell Host Microbe. 2007 Aug 16;2(2):119-29
pubmed: 18005726
Biochem Biophys Res Commun. 1970 Mar 12;38(5):989-92
pubmed: 4908541
PLoS Biol. 2007 Oct;5(10):2177-89
pubmed: 17760501
Gut. 2004 Jan;53(1):1-4
pubmed: 14684564
J Exp Med. 2019 Oct 7;216(10):2378-2393
pubmed: 31358565
J Bacteriol. 1995 Aug;177(16):4628-37
pubmed: 7642488
J Exp Med. 2019 Jan 7;216(1):84-98
pubmed: 30563917
Elife. 2018 Sep 18;7:
pubmed: 30226189
Infect Immun. 1990 Dec;58(12):3954-8
pubmed: 2254022
Nat Prod Rep. 2010 May;27(5):637-57
pubmed: 20376388
Environ Microbiol. 2003 Dec;5(12):1294-308
pubmed: 14641575
Cell Host Microbe. 2019 Sep 11;26(3):426-434.e6
pubmed: 31447308
Nature. 2013 Sep 19;501(7467):426-9
pubmed: 23955152
Nature. 1981 May 21;291(5812):238-9
pubmed: 7015147
J Microbiol Methods. 2011 Sep;86(3):351-6
pubmed: 21704084
Front Immunol. 2012 Oct 09;3:310
pubmed: 23087688
Science. 2013 Feb 8;339(6120):708-11
pubmed: 23393266
mBio. 2016 Oct 25;7(5):
pubmed: 27795390
Infect Immun. 2013 Nov;81(11):4063-70
pubmed: 23959718
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Front Cell Infect Microbiol. 2013 Nov 19;3:80
pubmed: 24312900
Gene. 1991 Apr;100:195-9
pubmed: 2055470
J Bacteriol. 1971 Aug;107(2):557-62
pubmed: 4939766
Nature. 2012 Sep 13;489(7415):220-30
pubmed: 22972295
Microbiology. 2004 Jul;150(Pt 7):2125-2134
pubmed: 15256555
J Bacteriol. 1975 Nov;124(2):704-12
pubmed: 126991
Cell Host Microbe. 2008 Nov 13;4(5):447-57
pubmed: 18996345
Cell. 2016 Nov 17;167(5):1339-1353.e21
pubmed: 27863247
Nature. 2018 Jan 11;553(7687):208-211
pubmed: 29323293
J Bacteriol. 1978 Feb;133(2):661-6
pubmed: 146699
J Bacteriol. 1998 Mar;180(6):1446-53
pubmed: 9515912
Biometals. 2019 Jun;32(3):369-384
pubmed: 30788645
Cell Host Microbe. 2016 Jun 8;19(6):814-25
pubmed: 27281571
Int J Med Microbiol. 2016 Dec;306(8):604-610
pubmed: 27760693
Gut. 2004 Nov;53(11):1617-23
pubmed: 15479682
Cell Host Microbe. 2014 Jan 15;15(1):47-57
pubmed: 24439897
Infect Immun. 2008 May;76(5):2008-17
pubmed: 18347048
mBio. 2014 Feb 25;5(2):e01089-13
pubmed: 24570372
J Bacteriol. 2005 Nov;187(21):7167-75
pubmed: 16237000
J Bacteriol. 1995 Mar;177(5):1357-66
pubmed: 7868611
FEMS Microbiol Lett. 2016 Oct;363(19):
pubmed: 27619890
Cell Host Microbe. 2011 Oct 20;10(4):336-47
pubmed: 22018234
Cell Host Microbe. 2017 Sep 13;22(3):291-301.e6
pubmed: 28844888
PLoS Pathog. 2010 Sep 09;6(9):e1001097
pubmed: 20844578
Aliment Pharmacol Ther. 1997 Oct;11(5):853-8
pubmed: 9354192
Zentralbl Bakteriol Orig A. 1973 Mar;223(2):333-42
pubmed: 4145840
Science. 2012 Oct 5;338(6103):120-3
pubmed: 22903521
Pediatrics. 2006 Aug;118(2):511-21
pubmed: 16882802
Mol Microbiol. 2008 Mar;67(5):971-83
pubmed: 18194158
Inflamm Bowel Dis. 2005 Dec;11(12):1060-9
pubmed: 16306768