Horizontal acquisition of a DNA ligase improves DNA damage tolerance in eukaryotes.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
22 Nov 2023
22 Nov 2023
Historique:
received:
20
09
2022
accepted:
30
10
2023
medline:
24
11
2023
pubmed:
23
11
2023
entrez:
22
11
2023
Statut:
epublish
Résumé
Bdelloid rotifers are part of the restricted circle of multicellular animals that can withstand a wide range of genotoxic stresses at any stage of their life cycle. In this study, bdelloid rotifer Adineta vaga is used as a model to decipher the molecular basis of their extreme tolerance. Proteomic analysis shows that a specific DNA ligase, different from those usually involved in DNA repair in eukaryotes, is strongly over-represented upon ionizing radiation. A phylogenetic analysis reveals its orthology to prokaryotic DNA ligase E, and its horizontal acquisition by bdelloid rotifers and plausibly other eukaryotes. The fungus Mortierella verticillata, having a single copy of this DNA Ligase E homolog, also exhibits an increased radiation tolerance with an over-expression of this DNA ligase E following X-ray exposure. We also provide evidence that A. vaga ligase E is a major contributor of DNA breaks ligation activity, which is a common step of all important DNA repair pathways. Consistently, its heterologous expression in human cell lines significantly improves their radio-tolerance. Overall, this study highlights the potential of horizontal gene transfers in eukaryotes, and their contribution to the adaptation to extreme conditions.
Identifiants
pubmed: 37993452
doi: 10.1038/s41467-023-43075-8
pii: 10.1038/s41467-023-43075-8
pmc: PMC10665377
doi:
Substances chimiques
DNA Ligases
EC 6.5.1.-
Ligases
EC 6.-
DNA Ligase ATP
EC 6.5.1.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7638Informations de copyright
© 2023. The Author(s).
Références
Trends Plant Sci. 2016 Jul;21(7):609-621
pubmed: 27021699
Elife. 2019 Oct 01;8:
pubmed: 31571581
BMC Evol Biol. 2018 Nov 28;18(1):177
pubmed: 30486781
Astrobiology. 2017 Feb;17(2):163-167
pubmed: 28206820
Eur J Biochem. 2000 Apr;267(8):2135-49
pubmed: 10759836
PLoS One. 2013 Sep 06;8(9):e72098
pubmed: 24039737
Nat Commun. 2019 Nov 15;10(1):5191
pubmed: 31729360
Nucleic Acids Res. 2022 Jan 7;50(D1):D543-D552
pubmed: 34723319
Proc Natl Acad Sci U S A. 2008 Apr 1;105(13):5139-44
pubmed: 18362355
Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2354-7
pubmed: 22308443
J Evol Biol. 2014 Jul;27(7):1334-45
pubmed: 25105197
J Biol Chem. 2007 Jul 6;282(27):19638-43
pubmed: 17507382
Comp Biochem Physiol A Mol Integr Physiol. 2016 Oct;200:64-78
pubmed: 26851497
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Science. 2008 May 30;320(5880):1210-3
pubmed: 18511688
New Phytol. 2016 Feb;209(3):1264-77
pubmed: 26436593
Nat Commun. 2022 Feb 28;13(1):1072
pubmed: 35228526
Curr Opin Plant Biol. 2010 Apr;13(2):153-9
pubmed: 20031477
Clin Oncol (R Coll Radiol). 2013 Oct;25(10):578-85
pubmed: 23849504
Traffic. 2009 Dec;10(12):1773-84
pubmed: 19843280
Annu Rev Biochem. 2017 Jun 20;86:715-748
pubmed: 28441057
PLoS One. 2016 Dec 20;11(12):e0168884
pubmed: 27997621
Carcinogenesis. 2001 Sep;22(9):1335-41
pubmed: 11532852
EMBO J. 2007 Apr 18;26(8):2094-103
pubmed: 17396150
Mol Microbiol. 2016 Jan;99(2):274-90
pubmed: 26412580
Curr Biol. 2016 Mar 21;26(6):723-32
pubmed: 26948882
Nucleic Acids Res. 2021 Jan 8;49(D1):D344-D354
pubmed: 33156333
Elife. 2014 Jan 01;3:e01322
pubmed: 24596148
Sci Adv. 2022 Dec 2;8(48):eadc8829
pubmed: 36449626
Trends Parasitol. 2020 Nov;36(11):927-941
pubmed: 32828660
Front Microbiol. 2020 Jul 31;11:1792
pubmed: 32849408
Nat Methods. 2021 Apr;18(4):366-368
pubmed: 33828273
DNA Repair (Amst). 2014 Apr;16:44-53
pubmed: 24674627
DNA Repair (Amst). 2012 Jan 2;11(1):12-21
pubmed: 22112864
Sci Adv. 2021 Oct 08;7(41):eabg4216
pubmed: 34613768
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296
pubmed: 33885785
Genome Biol. 2002 Jun 18;3(7):REVIEWS1019
pubmed: 12184812
Nat Protoc. 2006;1(5):2315-9
pubmed: 17406473
Mol Biol Evol. 2009 Feb;26(2):375-83
pubmed: 18996928
Nat Commun. 2016 Sep 20;7:12808
pubmed: 27649274
Nature. 2013 Aug 22;500(7463):453-7
pubmed: 23873043
Nucleic Acids Res. 2019 Jun 20;47(11):e61
pubmed: 30869144
PLoS Genet. 2012;8(11):e1003035
pubmed: 23166508
BMC Bioinformatics. 2009 Oct 27;10:356
pubmed: 19860910
PLoS Biol. 2018 Apr 24;16(4):e2004830
pubmed: 29689044
Nucleic Acids Res. 2008 Dec;36(22):6959-76
pubmed: 18981049
Cold Spring Harb Perspect Biol. 2013 Apr 01;5(4):a012583
pubmed: 23545420
Int J Radiat Biol. 2006 Dec;82(12):843-8
pubmed: 17178624
Mutat Res. 2011 Jun 3;711(1-2):134-41
pubmed: 21130102
Curr Biol. 2021 Jun 7;31(11):R712-R713
pubmed: 34102116
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Chem Rev. 2006 Feb;106(2):687-99
pubmed: 16464020
Life (Basel). 2017 Jun 15;7(2):
pubmed: 28617314
Nature. 2008 Jan 3;451(7174):81-5
pubmed: 18172500
Nucleic Acids Res. 2018 Sep 19;46(16):8616-8629
pubmed: 30007325
Nat Rev Microbiol. 2018 Feb;16(2):67-79
pubmed: 29176581
PLoS One. 2015 Apr 29;10(4):e0119248
pubmed: 25923521
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
Mol Cell. 2010 Oct 22;40(2):179-204
pubmed: 20965415
Nature. 2013 Oct 17;502(7471):333-339
pubmed: 24132290
Mol Biol Evol. 2014 May;31(5):1066-76
pubmed: 24577842
Heredity (Edinb). 2013 Feb;110(2):171-80
pubmed: 23169565
Oncotarget. 2018 Feb 12;9(18):14692-14722
pubmed: 29581875
Mol Cell Biol. 2008 Jul;28(14):4620-8
pubmed: 18474613
AMB Express. 2019 Sep 3;9(1):138
pubmed: 31482336
Nat Commun. 2012 May 08;3:815
pubmed: 22569363
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Integr Comp Biol. 2005 Nov;45(5):759-63
pubmed: 21676827
PLoS Genet. 2009 Mar;5(3):e1000401
pubmed: 19266019
Annu Rev Biochem. 2008;77:313-38
pubmed: 18518823
J Exp Biol. 2017 May 15;220(Pt 10):1749-1760
pubmed: 28515169