RNA polymerase redistribution supports growth in E. coli strains with a minimal number of rRNA operons.
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
25 08 2023
25 08 2023
Historique:
accepted:
02
06
2023
revised:
24
05
2023
received:
02
02
2022
medline:
28
8
2023
pubmed:
23
6
2023
entrez:
23
6
2023
Statut:
ppublish
Résumé
Bacterial transcription by RNA polymerase (RNAP) is spatially organized. RNAPs transcribing highly expressed genes locate in the nucleoid periphery, and form clusters in rich medium, with several studies linking RNAP clustering and transcription of rRNA (rrn). However, the nature of RNAP clusters and their association with rrn transcription remains unclear. Here we address these questions by using single-molecule tracking to monitor the subcellular distribution of mobile and immobile RNAP in strains with a heavily reduced number of chromosomal rrn operons (Δrrn strains). Strikingly, we find that the fraction of chromosome-associated RNAP (which is mainly engaged in transcription) is robust to deleting five or six of the seven chromosomal rrn operons. Spatial analysis in Δrrn strains showed substantial RNAP redistribution during moderate growth, with clustering increasing at cell endcaps, where the remaining rrn operons reside. These results support a model where RNAPs in Δrrn strains relocate to copies of the remaining rrn operons. In rich medium, Δrrn strains redistribute RNAP to minimize growth defects due to rrn deletions, with very high RNAP densities on rrn genes leading to genomic instability. Our study links RNAP clusters and rrn transcription, and offers insight into how bacteria maintain growth in the presence of only 1-2 rrn operons.
Identifiants
pubmed: 37351576
pii: 7205755
doi: 10.1093/nar/gkad511
pmc: PMC10450203
doi:
Substances chimiques
DNA-Directed RNA Polymerases
EC 2.7.7.6
RNA, Ribosomal
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8085-8101Subventions
Organisme : Wellcome Trust
ID : 204684/Z/16/Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N018656/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 110164/Z/15/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 224212/Z/21/Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S008896/1
Pays : United Kingdom
Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Nucleic Acids Res. 2022 Dec 9;50(22):12601-12620
pubmed: 35552441
Proc Natl Acad Sci U S A. 2019 Oct 1;116(40):20115-20123
pubmed: 31527272
Trends Genet. 1990 Dec;6(12):390-5
pubmed: 2087780
J Bacteriol. 1995 Jul;177(14):4152-6
pubmed: 7608093
Cell. 2019 Jan 24;176(3):419-434
pubmed: 30682370
Nucleic Acids Res. 2014 Dec 16;42(22):13696-705
pubmed: 25416798
Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20245-50
pubmed: 19073937
Chem Rev. 2013 Nov 13;113(11):8662-82
pubmed: 23941620
J Mol Biol. 1992 May 20;225(2):239-50
pubmed: 1593619
Biophys J. 2013 Jul 2;105(1):172-81
pubmed: 23823236
FEMS Microbiol Rev. 2012 Mar;36(2):269-87
pubmed: 21569058
Proc Natl Acad Sci U S A. 2020 Aug 4;117(31):18540-18549
pubmed: 32675239
J Bacteriol. 2011 Oct;193(19):5138-46
pubmed: 21784927
Genes Dev. 2016 Oct 15;30(20):2272-2285
pubmed: 27898392
Science. 2018 Jul 27;361(6400):
pubmed: 29930091
Methods. 2017 May 1;120:103-114
pubmed: 28414097
Science. 2002 Jun 21;296(5576):2218-22
pubmed: 12077417
Annu Rev Genet. 2004;38:749-70
pubmed: 15568992
Nat Methods. 2012 Nov;9(11):1040-1
pubmed: 23132113
J Bacteriol. 2009 Jul;191(13):4180-5
pubmed: 19395497
EMBO J. 1993 Nov;12(11):4305-15
pubmed: 8223440
Elife. 2017 Mar 20;6:
pubmed: 28318486
J Mol Biol. 2018 Oct 26;430(22):4443-4455
pubmed: 29753778
Elife. 2016 May 03;5:
pubmed: 27138339
Science. 2018 Jul 27;361(6400):412-415
pubmed: 29930094
Mol Cell. 2018 Sep 20;71(6):1027-1039.e14
pubmed: 30197298
Nat Protoc. 2008;3(6):1101-8
pubmed: 18546601
J Bacteriol. 2006 Jun;188(11):4007-14
pubmed: 16707692
Mol Microbiol. 2003 Dec;50(5):1493-505
pubmed: 14651633
Front Microbiol. 2018 Jun 05;9:1115
pubmed: 29922250
Mol Cell. 2020 Jul 16;79(2):293-303.e4
pubmed: 32679076
Mol Cell. 2021 Apr 1;81(7):1499-1514.e6
pubmed: 33621478
G3 (Bethesda). 2015 Oct 04;5(12):2555-7
pubmed: 26438293
Science. 2018 Jul 27;361(6400):
pubmed: 29930090
Mol Microbiol. 2012 Jul;85(1):21-38
pubmed: 22624875
Nat Rev Microbiol. 2009 Nov;7(11):822-7
pubmed: 19806155
PLoS One. 2013 Oct 16;8(10):e76268
pubmed: 24146850
Science. 2003 Aug 8;301(5634):780-5
pubmed: 12907786
Sci Rep. 2018 Oct 8;8(1):14961
pubmed: 30297723
Microbiol Mol Biol Rev. 2004 Dec;68(4):639-68
pubmed: 15590778
Cell. 2019 May 30;177(6):1632-1648.e20
pubmed: 31150626
EMBO J. 2000 Feb 15;19(4):710-8
pubmed: 10675340
Microbiol Rev. 1990 Jun;54(2):89-100
pubmed: 1694554
Genes Dev. 2006 Aug 1;20(15):2121-34
pubmed: 16882985
EMBO J. 2009 Aug 5;28(15):2209-19
pubmed: 19574956
Proc Natl Acad Sci U S A. 2015 Aug 11;112(32):E4390-9
pubmed: 26224838
Front Microbiol. 2015 Jul 02;6:636
pubmed: 26191045
Nature. 2019 Sep;573(7772):144-148
pubmed: 31435012
J Mol Biol. 2010 Jan 8;395(1):1-10
pubmed: 19852969
EcoSal Plus. 2008 Sep;3(1):
pubmed: 26443740
Science. 1999 Jun 11;284(5421):1790-5
pubmed: 10364545
Science. 2013 Aug 9;341(6146):664-7
pubmed: 23828889
EMBO Rep. 2019 Jan;20(1):
pubmed: 30523075
Front Microbiol. 2018 Jun 08;9:1232
pubmed: 29937760
Crit Rev Biochem Mol Biol. 2017 Feb;52(1):96-106
pubmed: 28006965
Nature. 2011 Feb 24;470(7335):554-7
pubmed: 21350489
mBio. 2020 Mar 10;11(2):
pubmed: 32156825