Multiple Losses of MSH1, Gain of mtMutS, and Other Changes in the MutS Family of DNA Repair Proteins in Animals.
DNA repair
MutS
cnidarians
mitochondria
octocorals
Journal
Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707
Informations de publication
Date de publication:
01 09 2021
01 09 2021
Historique:
accepted:
11
08
2021
pubmed:
18
8
2021
medline:
1
4
2022
entrez:
17
8
2021
Statut:
ppublish
Résumé
MutS is a key component of the mismatch repair (MMR) pathway. Members of the MutS protein family are present in prokaryotes, eukaryotes, and viruses. Six MutS homologs (MSH1-6) have been identified in yeast, of which three function in nuclear MMR, while MSH1 functions in mitochondrial DNA repair. MSH proteins are believed to be well conserved in animals, except for MSH1-which is thought to be lost. Two intriguing exceptions to this general picture have been found, both in the class Anthozoa within the phylum Cnidaria. First, an ortholog of the yeast-MSH1 was reported in one hexacoral species. Second, a MutS homolog (mtMutS) has been found in the mitochondrial genome of all octocorals. To understand the origin and potential functional implications of these exceptions, we investigated the evolution of the MutS family both in Cnidaria and in animals in general. Our study confirmed the acquisition of octocoral mtMutS by horizontal gene transfer from a giant virus. Surprisingly, we identified MSH1 in all hexacorals and several sponges and placozoans. By contrast, MSH1 orthologs were lacking in other cnidarians, ctenophores, and bilaterian animals. Furthermore, while we identified MSH2 and MSH6 in nearly all animals, MSH4, MSH5, and, especially, MSH3 were missing in multiple species. Overall, our analysis revealed a dynamic evolution of the MutS family in animals, with multiple losses of MSH1, MSH3, some losses of MSH4 and MSH5, and a gain of the octocoral mtMutS. We propose that octocoral mtMutS functionally replaced MSH1 that was present in the common ancestor of Anthozoa.
Identifiants
pubmed: 34402879
pii: 6353608
doi: 10.1093/gbe/evab191
pmc: PMC8438181
pii:
doi:
Substances chimiques
DNA-Binding Proteins
0
Fungal Proteins
0
MSH4 protein, S cerevisiae
0
MSH5 protein, S cerevisiae
0
MSH6 protein, S cerevisiae
0
Saccharomyces cerevisiae Proteins
0
MutS DNA Mismatch-Binding Protein
EC 3.6.1.3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
J Cell Biol. 2000 Jul 24;150(2):F31-6
pubmed: 10908583
Genome Biol Evol. 2016 Sep 26;8(9):2896-2913
pubmed: 27557826
Mol Phylogenet Evol. 2013 Nov;69(2):313-9
pubmed: 22982435
Nature. 2000 Oct 12;407(6805):711-7
pubmed: 11048711
J Mol Evol. 1998 Dec;47(6):697-708
pubmed: 9847412
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
J Nucleic Acids. 2010 Jul 27;2010:
pubmed: 20725617
PLoS Comput Biol. 2011 Oct;7(10):e1002195
pubmed: 22039361
J Biol Chem. 1994 Nov 25;269(47):29984-92
pubmed: 7961998
Genes Dev. 1999 Mar 1;13(5):523-31
pubmed: 10072381
Genetics. 2009 Jul;182(3):699-709
pubmed: 19398768
Environ Mol Mutagen. 2017 Jun;58(5):235-263
pubmed: 28485537
Microbiome. 2018 Apr 2;6(1):64
pubmed: 29609655
Proc Natl Acad Sci U S A. 1973 Dec;70(12):3541-5
pubmed: 4148702
Genetics. 1992 Dec;132(4):975-85
pubmed: 1334021
Nat Ecol Evol. 2020 Apr;4(4):519-523
pubmed: 32094540
BMC Evol Biol. 2011 Jul 29;11:228
pubmed: 21801381
J Mol Evol. 2006 Aug;63(2):165-73
pubmed: 16830098
Genetics. 2017 Feb;205(2):471-490
pubmed: 28154196
Mech Ageing Dev. 2008 Jul-Aug;129(7-8):391-407
pubmed: 18406444
Bioinformatics. 2020 Jan 1;36(1):56-64
pubmed: 31218353
Nat Protoc. 2007;2(4):953-71
pubmed: 17446895
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
DNA Repair (Amst). 2009 Jun 4;8(6):704-19
pubmed: 19272840
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Mutat Res Rev Mutat Res. 2017 Jul;773:174-187
pubmed: 28927527
Mol Cell Proteomics. 2015 Apr;14(4):1113-26
pubmed: 25670805
Proc Natl Acad Sci U S A. 2017 Apr 4;114(14):3552-3554
pubmed: 28356513
Nat Struct Mol Biol. 2011 Dec 18;19(1):72-8
pubmed: 22179786
Science. 1994 Mar 18;263(5153):1625-9
pubmed: 8128251
Nucleic Acids Res. 2003 Feb 1;31(3):1052-8
pubmed: 12560503
Nature. 2000 Oct 12;407(6805):703-10
pubmed: 11048710
DNA Repair (Amst). 2017 Mar;51:2-13
pubmed: 28189416
Trends Genet. 2006 Feb;22(2):90-5
pubmed: 16364493
IUBMB Life. 2018 Dec;70(12):1289-1301
pubmed: 30419142
Proc Natl Acad Sci U S A. 2020 Jul 14;117(28):16448-16455
pubmed: 32601224
Nucleic Acids Res. 2007;35(22):7591-603
pubmed: 17965091
PLoS Genet. 2013 Oct;9(10):e1003920
pubmed: 24204320
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
Nat Genet. 1996 Jul;13(3):336-42
pubmed: 8673133
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
DNA Repair (Amst). 2009 Mar 1;8(3):318-29
pubmed: 19056520
Nucleic Acids Res. 2015 Jan;43(Database issue):D204-12
pubmed: 25348405
Coral Reefs. 2012;31(2):487-491
pubmed: 32214633
J Cell Physiol. 2002 Apr;191(1):28-41
pubmed: 11920679
Mol Ecol. 2018 Apr;27(7):1651-1666
pubmed: 29575260
Nucleic Acids Res. 1998 Sep 15;26(18):4291-300
pubmed: 9722651
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
ISME J. 2011 Jul;5(7):1143-51
pubmed: 21248859
Curr Biol. 2002 Oct 15;12(20):1773-8
pubmed: 12401173
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W320-4
pubmed: 24753421