Insertion and deletion evolution reflects antibiotics selection pressure in a Mycobacterium tuberculosis outbreak.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
09 2020
Historique:
received: 22 01 2020
accepted: 18 08 2020
revised: 12 10 2020
pubmed: 1 10 2020
medline: 13 11 2020
entrez: 30 9 2020
Statut: epublish

Résumé

In genome evolution, genetic variants are the source of diversity, which natural selection acts upon. Treatment of human tuberculosis (TB) induces a strong selection pressure for the emergence of antibiotic resistance-conferring variants in the infecting Mycobacterium tuberculosis (MTB) strains. MTB evolution in response to treatment has been intensively studied and mainly attributed to point substitutions. However, the frequency and contribution of insertions and deletions (indels) to MTB genome evolution remains poorly understood. Here, we analyzed a multi-drug resistant MTB outbreak for the presence of high-quality indels and substitutions. We find that indels are significantly enriched in genes conferring antibiotic resistance. Furthermore, we show that indels are inherited during the outbreak and follow a molecular clock with an evolutionary rate of 5.37e-9 indels/site/year, which is 23 times lower than the substitution rate. Inherited indels may co-occur with substitutions in genes along related biological pathways; examples are iron storage and resistance to second-line antibiotics. This suggests that epistatic interactions between indels and substitutions affect antibiotic resistance and compensatory evolution in MTB.

Identifiants

pubmed: 32997707
doi: 10.1371/journal.ppat.1008357
pii: PPATHOGENS-D-20-00142
pmc: PMC7549793
doi:

Substances chimiques

Anti-Bacterial Agents 0
Antitubercular Agents 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008357

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

G3 (Bethesda). 2016 Aug 09;6(8):2583-91
pubmed: 27317782
Nat Ecol Evol. 2018 Dec;2(12):1982-1992
pubmed: 30397300
Nat Genet. 2006 Jul;38(7):819-23
pubmed: 16767103
Gene. 2007 Mar 1;389(1):87-95
pubmed: 17098378
Mol Microbiol. 2015 Jun;96(5):901-16
pubmed: 25727695
Bioinformatics. 2012 Sep 15;28(18):i333-i339
pubmed: 22962449
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
FEMS Microbiol Rev. 2017 May 1;41(3):354-373
pubmed: 28369307
Nat Methods. 2014 Oct;11(10):1033-6
pubmed: 25128977
Antimicrob Agents Chemother. 1997 Mar;41(3):540-3
pubmed: 9055989
Nat Rev Microbiol. 2010 Apr;8(4):260-71
pubmed: 20208551
Mol Ecol. 2016 Jan;25(1):42-66
pubmed: 26578204
mSystems. 2018 Jan 30;3(1):
pubmed: 29404424
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Genome Med. 2020 Mar 6;12(1):27
pubmed: 32143680
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
FEMS Microbiol Rev. 2003 Jun;27(2-3):145-63
pubmed: 12829265
Syst Biol. 2016 Jan;65(1):82-97
pubmed: 26424727
Trends Genet. 2000 Jun;16(6):276-7
pubmed: 10827456
Mol Microbiol. 2011 Dec;82(6):1375-91
pubmed: 22026918
Genome Biol. 2014 Nov 07;15(11):490
pubmed: 25418686
Bioinformatics. 2014 Dec 15;30(24):3451-7
pubmed: 25123898
PLoS Pathog. 2007 Aug 3;3(8):e105
pubmed: 17676952
Tuberculosis (Edinb). 2014 May;94(3):346-54
pubmed: 24637013
Genetics. 1977 Jul;86(3):607-21
pubmed: 892424
Tuberculosis (Edinb). 2007 Sep;87(5):393-404
pubmed: 17627889
Genome Biol Evol. 2018 Aug 1;10(8):1920-1926
pubmed: 30010866
Bioinformatics. 2012 Feb 15;28(4):593-4
pubmed: 22199392
J Mol Biol. 1970 Mar;48(3):443-53
pubmed: 5420325
Nat Genet. 2015 Mar;47(3):242-9
pubmed: 25599400
Clin Microbiol Rev. 2005 Jan;18(1):81-101
pubmed: 15653820
Antimicrob Agents Chemother. 2014 May;58(5):2979-81
pubmed: 24590481
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Lancet. 1993 Mar 13;341(8846):647-50
pubmed: 8095569
Nat Rev Microbiol. 2018 Apr;16(4):202-213
pubmed: 29456241
Genome Biol Evol. 2013;5(3):599-605
pubmed: 23475937
Antimicrob Agents Chemother. 2011 May;55(5):2032-41
pubmed: 21300839
Mol Ther Nucleic Acids. 2019 Jun 7;16:698-706
pubmed: 31128421
Genome Biol. 2017 Apr 19;18(1):71
pubmed: 28424085
Nature. 1998 Jun 11;393(6685):537-44
pubmed: 9634230
Elife. 2018 Oct 30;7:
pubmed: 30373719
Trends Genet. 2010 Aug;26(8):345-52
pubmed: 20594608
Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13881-13886
pubmed: 27872285
Genetics. 2000 Mar;154(3):985-97
pubmed: 10757748
BMC Genomics. 2018 May 16;19(1):365
pubmed: 29769016
Mol Biol Evol. 2015 Jul;32(7):1895-906
pubmed: 25771196
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
J Bacteriol. 2012 Feb;194(3):567-75
pubmed: 22101841
Nat Rev Microbiol. 2019 Sep;17(9):533-545
pubmed: 31209399
mBio. 2017 Jan 17;8(1):
pubmed: 28096490
Bioinformatics. 2009 Nov 1;25(21):2865-71
pubmed: 19561018
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
J Gen Virol. 2009 Jun;90(Pt 6):1539-1547
pubmed: 19264617
Nat Genet. 2018 Jun;50(6):849-856
pubmed: 29785015
Mol Biol Evol. 2020 Aug 1;37(8):2450-2460
pubmed: 32167543
Nat Rev Microbiol. 2016 Nov;14(11):677-691
pubmed: 27665717
PLoS Med. 2013;10(2):e1001387
pubmed: 23424287
Nature. 2006 Mar 2;440(7080):87-90
pubmed: 16511495
Antimicrob Agents Chemother. 2013 Feb;57(2):827-32
pubmed: 23208709
Nat Genet. 2013 Oct;45(10):1183-9
pubmed: 23995135
Nat Methods. 2015 Oct;12(10):966-8
pubmed: 26258291
Genome Res. 2018 Apr;28(4):581-591
pubmed: 29535149
Am J Respir Crit Care Med. 2016 Feb 1;193(3):337-40
pubmed: 26829425
Nat Commun. 2019 May 13;10(1):2128
pubmed: 31086182
Nature. 1992 Aug 13;358(6387):591-3
pubmed: 1501713
Antimicrob Agents Chemother. 2017 Nov 22;61(12):
pubmed: 28993337
Science. 1998 Sep 25;281(5385):1986-90
pubmed: 9748151
Microbiology (Reading). 2017 Dec;163(12):1740-1758
pubmed: 29171825
Proc Natl Acad Sci U S A. 2016 Aug 30;113(35):9876-81
pubmed: 27528665
Trends Microbiol. 2016 Aug;24(8):637-648
pubmed: 27068531
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
PLoS Pathog. 2019 Sep 12;15(9):e1008067
pubmed: 31513651

Auteurs

Maxime Godfroid (M)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Tal Dagan (T)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Matthias Merker (M)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Borstel, Germany.
German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Thomas A Kohl (TA)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Borstel, Germany.
German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Roland Diel (R)

German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.
Institute for Epidemiology, University Medical Hospital Schleswig-Holstein, Kiel, Germany.
Lungenclinic Grosshansdorf, Airway Research Center North (ARCN), Member of the German Center for Lung Research (DZL), Großhansdorf, Germany.

Florian P Maurer (FP)

National and WHO Supranational Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany.
Institute of Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Stefan Niemann (S)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Borstel, Germany.
German Center for Infection Research, Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Anne Kupczok (A)

Institute of General Microbiology, Kiel University, Kiel, Germany.

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Classifications MeSH