Atlas of mRNA translation and decay for bacteria.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
16
06
2022
accepted:
19
04
2023
medline:
5
6
2023
pubmed:
23
5
2023
entrez:
22
5
2023
Statut:
ppublish
Résumé
Regulation of messenger RNA stability is pivotal for programmed gene expression in bacteria and is achieved by a myriad of molecular mechanisms. By bulk sequencing of 5' monophosphorylated mRNA decay intermediates (5'P), we show that cotranslational mRNA degradation is conserved among both Gram-positive and -negative bacteria. We demonstrate that, in species with 5'-3' exonucleases, the exoribonuclease RNase J tracks the trailing ribosome to produce an in vivo single-nucleotide toeprint of the 5' position of the ribosome. In other species lacking 5'-3' exonucleases, ribosome positioning alters endonucleolytic cleavage sites. Using our metadegradome (5'P degradome) sequencing approach, we characterize 5'P mRNA decay intermediates in 96 species including Bacillus subtilis, Escherichia coli, Synechocystis spp. and Prevotella copri and identify codon- and gene-level ribosome stalling responses to stress and drug treatment. We also apply 5'P sequencing to complex clinical and environmental microbiomes and demonstrate that metadegradome sequencing provides fast, species-specific posttranscriptional characterization of responses to drug or environmental perturbations. Finally we produce a degradome atlas for 96 species to enable analysis of mechanisms of RNA degradation in bacteria. Our work paves the way for the application of metadegradome sequencing to investigation of posttranscriptional regulation in unculturable species and complex microbial communities.
Identifiants
pubmed: 37217719
doi: 10.1038/s41564-023-01393-z
pii: 10.1038/s41564-023-01393-z
pmc: PMC10234816
doi:
Substances chimiques
RNA, Bacterial
0
Endoribonucleases
EC 3.1.-
Exonucleases
EC 3.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1123-1136Informations de copyright
© 2023. The Author(s).
Références
Cell. 2015 Jun 4;161(6):1400-12
pubmed: 26046441
Cell. 2007 May 18;129(4):681-92
pubmed: 17512403
Bioinformatics. 2017 Nov 15;33(22):3645-3647
pubmed: 29036507
Genome Biol. 2014;15(12):550
pubmed: 25516281
Mol Cell. 2019 Jun 20;74(6):1227-1238.e3
pubmed: 31003868
EMBO J. 2021 Jan 15;40(2):e106696
pubmed: 33346941
Front Cell Infect Microbiol. 2019 Mar 20;9:59
pubmed: 30949454
Trends Biochem Sci. 2020 Jan;45(1):42-57
pubmed: 31679841
Genome Res. 2017 Mar;27(3):491-499
pubmed: 28100584
Cell. 2014 Apr 24;157(3):624-35
pubmed: 24766808
Curr Opin Microbiol. 2011 Apr;14(2):148-54
pubmed: 21334965
Cell Rep Methods. 2021 Apr 02;1(1):100001
pubmed: 35474692
Proc Natl Acad Sci U S A. 2014 Oct 28;111(43):15379-84
pubmed: 25313041
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Nature. 2019 May;569(7758):641-648
pubmed: 31142853
Nucleic Acids Res. 2006 Feb 01;34(2):659-66
pubmed: 16452296
Elife. 2019 Feb 06;8:
pubmed: 30724162
BMC Genomics. 2018 Mar 27;19(1):223
pubmed: 29587634
Elife. 2013 Dec 17;2:e01501
pubmed: 24347549
PLoS Genet. 2020 Mar 16;16(3):e1008275
pubmed: 32176689
Nucleic Acids Res. 2019 Jul 2;47(W1):W199-W205
pubmed: 31114916
J Biol Chem. 1996 Apr 26;271(17):10060-5
pubmed: 8626562
EMBO J. 2009 Nov 18;28(22):3523-33
pubmed: 19779461
STAR Protoc. 2021 Mar 31;2(2):100447
pubmed: 33870233
Wiley Interdiscip Rev RNA. 2021 Nov;12(6):e1658
pubmed: 33949788
J Bacteriol. 2013 May;195(10):2340-8
pubmed: 23504012
J Mol Biol. 1991 Sep 5;221(1):81-95
pubmed: 1920421
Wiley Interdiscip Rev RNA. 2014 Nov-Dec;5(6):747-63
pubmed: 24944158
Science. 2009 Apr 10;324(5924):218-23
pubmed: 19213877
Cell. 2015 Mar 12;160(6):1111-24
pubmed: 25768907
Elife. 2014 May 09;3:e01257
pubmed: 24842990
Cell Rep. 2018 Oct 9;25(2):478-486.e8
pubmed: 30304686
Nat Chem Biol. 2020 Mar;16(3):310-317
pubmed: 31844301
Cell Syst. 2020 Aug 26;11(2):121-130.e6
pubmed: 32726597
Nat Commun. 2020 Jun 29;11(1):3268
pubmed: 32601270
Mol Microbiol. 2011 Sep;81(6):1459-73
pubmed: 21815947
Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):15958-63
pubmed: 25349425
Cold Spring Harb Perspect Med. 2016 Sep 01;6(9):
pubmed: 27481773
NAR Genom Bioinform. 2020 Nov 24;2(4):lqaa099
pubmed: 33575643
Nature. 2022 Mar;603(7901):503-508
pubmed: 35264790
Mol Cell Biol. 1993 Sep;13(9):5141-8
pubmed: 8355674
Microb Genom. 2021 Feb;7(2):
pubmed: 33539279
Nucleic Acids Res. 2019 Jan 8;47(D1):D212-D220
pubmed: 30395280
PLoS Genet. 2015 Oct 16;11(10):e1005577
pubmed: 26473962
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Nucleic Acids Res. 2019 May 7;47(8):e47
pubmed: 30783653
Antimicrob Agents Chemother. 2007 Nov;51(11):4111-7
pubmed: 17724150
Nat Protoc. 2016 Feb;11(2):359-76
pubmed: 26820793
Nat Commun. 2020 Mar 27;11(1):1587
pubmed: 32221293
J Oral Biosci. 2016 Nov;58(4):142-149
pubmed: 28392745
Nat Microbiol. 2022 Mar;7(3):434-450
pubmed: 35241796
Nature. 2016 Jan 21;529(7586):358-363
pubmed: 26760206
Cell. 2013 Jan 17;152(1-2):17-24
pubmed: 23332744
J Biomed Sci. 2011 Mar 22;18:23
pubmed: 21418661
Antimicrob Resist Infect Control. 2020 Aug 10;9(1):130
pubmed: 32778149
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Sci Rep. 2016 May 05;6:25477
pubmed: 27146487
Nucleic Acids Res. 2003 Aug 15;31(16):4710-6
pubmed: 12907711
Nucleic Acids Res. 2019 Jan 8;47(D1):D309-D314
pubmed: 30418610
Cell Host Microbe. 2014 Sep 10;16(3):276-89
pubmed: 25211071
Nat Struct Mol Biol. 2019 Apr;26(4):275-280
pubmed: 30911188
Nat Commun. 2021 May 14;12(1):2803
pubmed: 33990576
Front Microbiol. 2020 Jun 03;11:1055
pubmed: 32582060
J Bacteriol. 2013 Feb;195(3):510-22
pubmed: 23175650