Promotion of plasmid maintenance by heterogeneous partitioning of microbial communities.
antibiotic resistance
heterogeneous community partitioning
horizontal gene transfer
microbial communities
plasmid
Journal
Cell systems
ISSN: 2405-4720
Titre abrégé: Cell Syst
Pays: United States
ID NLM: 101656080
Informations de publication
Date de publication:
18 Oct 2023
18 Oct 2023
Historique:
received:
17
10
2022
revised:
09
05
2023
accepted:
19
09
2023
pmc-release:
18
10
2024
medline:
23
10
2023
pubmed:
12
10
2023
entrez:
11
10
2023
Statut:
ppublish
Résumé
Transferable plasmids play a critical role in shaping the functions of microbial communities. Previous studies suggested multiple mechanisms underlying plasmid persistence and abundance. Here, we focus on the interplay between heterogeneous community partitioning and plasmid fates. Natural microbiomes often experience partitioning that creates heterogeneous local communities with reduced population sizes and biodiversity. Little is known about how population partitioning affects the plasmid fate through the modulation of community structure. By modeling and experiments, we show that heterogeneous community partitioning can paradoxically promote the persistence of a plasmid that would otherwise not persist in a global community. Among the local communities created by partitioning, a minority will primarily consist of members able to transfer the plasmid fast enough to support its maintenance by serving as a local plasmid haven. Our results provide insights into plasmid maintenance and suggest a generalizable approach to modulate plasmid persistence for engineering and medical applications.
Identifiants
pubmed: 37820728
pii: S2405-4712(23)00267-3
doi: 10.1016/j.cels.2023.09.002
pmc: PMC10591896
mid: NIHMS1934348
pii:
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
895-905.e5Subventions
Organisme : NIAID NIH HHS
ID : R01 AI125604
Pays : United States
Organisme : NIBIB NIH HHS
ID : R01 EB031869
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM098642
Pays : United States
Informations de copyright
Copyright © 2023 Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
Front Microbiol. 2018 Jul 27;9:1583
pubmed: 30108552
Nat Commun. 2020 Sep 1;11(1):4379
pubmed: 32873785
PLoS Pathog. 2015 Oct 29;11(10):e1005156
pubmed: 26513155
Nat Chem Biol. 2019 Oct;15(10):1017-1024
pubmed: 31527836
Gut Microbes. 2013 Jul-Aug;4(4):271-80
pubmed: 23651955
FEMS Microbiol Rev. 2012 Nov;36(6):1083-104
pubmed: 22393901
Proc Natl Acad Sci U S A. 2018 Sep 25;115(39):9791-9796
pubmed: 30209211
Nat Rev Genet. 2015 Aug;16(8):472-82
pubmed: 26184597
Front Microbiol. 2014 Jan 17;4:420
pubmed: 24478761
Environ Pollut. 2018 Jun;237:253-261
pubmed: 29494919
Nat Commun. 2014 Oct 10;5:5208
pubmed: 25302567
Trends Microbiol. 2022 Jun;30(6):534-543
pubmed: 34848115
Proc Natl Acad Sci U S A. 2018 Oct 16;115(42):E9842-E9848
pubmed: 30266791
Nat Rev Microbiol. 2019 Dec;17(12):725-741
pubmed: 31548653
Nat Rev Microbiol. 2010 Aug;8(8):552-63
pubmed: 20601965
mBio. 2016 Apr 05;7(2):e02234-15
pubmed: 27048805
Trends Biotechnol. 2002 Mar;20(3):103-5
pubmed: 11841860
Proc Natl Acad Sci U S A. 2012 Jan 24;109(4):1269-74
pubmed: 22232693
mBio. 2015 Oct 27;6(6):e01163-15
pubmed: 26507229
Mol Syst Biol. 2006;2:2006.0008
pubmed: 16738554
Genetics. 2002 Dec;162(4):1525-32
pubmed: 12524329
FEMS Microbiol Lett. 2012 Jan;326(1):76-82
pubmed: 22092700
mBio. 2017 Apr 4;8(2):
pubmed: 28377533
Cell. 2021 Apr 15;184(8):2053-2067.e18
pubmed: 33794144
Curr Biol. 2015 Aug 3;25(15):2034-9
pubmed: 26190075
Gut Microbes. 2022 Jan-Dec;14(1):2022442
pubmed: 35030982
Crit Rev Microbiol. 2015 Feb;41(1):101-8
pubmed: 23862575
Nat Chem Biol. 2022 Nov;18(11):1245-1252
pubmed: 36050493
Heredity (Edinb). 2011 Jan;106(1):1-10
pubmed: 20332804
Nat Commun. 2019 Feb 27;10(1):968
pubmed: 30814504
Microbiol Spectr. 2017 Sep;5(5):
pubmed: 28944751
Nature. 2016 Jul 21;535(7612):435-439
pubmed: 27409808
ISME J. 2022 Feb;16(2):521-532
pubmed: 34455424
Annu Rev Microbiol. 2017 Sep 8;71:579-596
pubmed: 28697667
Nat Chem Biol. 2022 Apr;18(4):394-402
pubmed: 35145274
Microbiome. 2020 Nov 18;8(1):161
pubmed: 33208178
Proc Natl Acad Sci U S A. 2018 Mar 6;115(10):2526-2531
pubmed: 29463749
Front Microbiol. 2013 Mar 07;4:44
pubmed: 23471189
Nat Commun. 2019 Jun 13;10(1):2595
pubmed: 31197163
Elife. 2020 Jun 17;9:
pubmed: 32553109
PLoS Genet. 2009 Mar;5(3):e1000402
pubmed: 19266023
Mol Microbiol. 2020 Mar;113(3):672-681
pubmed: 32185830
PLoS Pathog. 2014 Dec 18;10(12):e1004557
pubmed: 25522364
Sci Adv. 2020 Jan 24;6(4):eaax3173
pubmed: 32042895
Nat Commun. 2022 Feb 11;13(1):836
pubmed: 35149704
ILAR J. 2015;56(2):169-78
pubmed: 26323627
Nat Rev Microbiol. 2005 Sep;3(9):722-32
pubmed: 16138100
Nat Methods. 2019 Feb;16(2):167-170
pubmed: 30643213
Nat Commun. 2017 Nov 22;8(1):1689
pubmed: 29162798
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Trends Microbiol. 2021 Feb;29(2):107-116
pubmed: 32800610
Genome Biol Evol. 2020 Nov 3;12(11):2002-2014
pubmed: 32687170
Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):E9105-E9114
pubmed: 29073107
Nat Commun. 2021 May 11;12(1):2653
pubmed: 33976161
Nat Rev Microbiol. 2019 Sep;17(9):569-586
pubmed: 31213707
G3 (Bethesda). 2011 Aug 1;1(3):183-186
pubmed: 22207905
Microbiol Mol Biol Rev. 2010 Sep;74(3):434-52
pubmed: 20805406
Comput Struct Biotechnol J. 2020 Dec 29;19:586-599
pubmed: 33510864
Front Microbiol. 2020 Nov 27;11:590776
pubmed: 33329469
Proc Natl Acad Sci U S A. 2016 Jul 19;113(29):8260-5
pubmed: 27385827
mSphere. 2020 Jan 29;5(1):
pubmed: 31996415
Sci Rep. 2022 Jul 15;12(1):12102
pubmed: 35840779
Front Microbiol. 2021 Nov 04;12:606396
pubmed: 34803935
BMC Bioinformatics. 2010 Mar 08;11:119
pubmed: 20211023
Curr Biol. 2015 Aug 31;25(17):R764-7
pubmed: 26325139
Bioessays. 2021 Sep;43(9):e2100084
pubmed: 34278591
PLoS Pathog. 2019 Feb 21;15(2):e1007563
pubmed: 30789972
Nat Commun. 2020 Nov 4;11(1):5589
pubmed: 33149119
FEMS Microbiol Ecol. 2002 Nov 1;42(2):199-208
pubmed: 19709279
Proc Natl Acad Sci U S A. 2015 Feb 24;112(8):E911-20
pubmed: 25605935
Nat Commun. 2020 Jan 8;11(1):116
pubmed: 31913270
Microbiology (Reading). 2021 Sep;167(9):
pubmed: 34494951
Nat Rev Microbiol. 2016 Mar;14(3):150-62
pubmed: 26806595
Science. 2010 Oct 1;330(6000):50
pubmed: 20929803
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
PLoS Pathog. 2015 Jun 11;11(6):e1004823
pubmed: 26066486