Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment.
MutS proteins are ubiquitous in cellular organisms and have important roles in DNA mismatch repair or recombination. In the virus world, the amoeba-infecting Mimivirus, as well as the recently sequenced Cafeteria roenbergensis virus are known to encode a MutS related to the homologs found in octocorals and ɛ-proteobacteria. To explore the presence of MutS proteins in other viral genomes, we performed a genomic survey of four giant viruses ('giruses') (Pyramimonas orientalis virus (PoV), Phaeocystis pouchetii virus (PpV), Chrysochromulina ericina virus (CeV) and Heterocapsa circularisquama DNA virus (HcDNAV)) that infect unicellular marine algae. Our analysis revealed the presence of a close homolog of Mimivirus MutS in all the analyzed giruses. These viral homologs possess a specific domain structure, including a C-terminal HNH-endonuclease domain, defining the new MutS7 subfamily. We confirmed the presence of conserved mismatch recognition residues in all members of the MutS7 subfamily, suggesting their role in DNA mismatch repair rather than DNA recombination. PoV and PpV were found to contain an additional type of MutS, which we propose to call MutS8. The MutS8 proteins in PoV and PpV were found to be closely related to homologs from 'Candidatus Amoebophilus asiaticus', an obligate intracellular amoeba-symbiont belonging to the Bacteroidetes. Furthermore, our analysis revealed that MutS7 and MutS8 are abundant in marine microbial metagenomes and that a vast majority of these environmental sequences are likely of girus origin. Giruses thus seem to represent a major source of the underexplored diversity of the MutS family in the microbial world.
Information Génomique et Structurale, CNRS-UPR2589, Institut de Microbiologie de la Méditerranée, Parc Scientifique de Luminy, Aix-Marseille Université, Marseille Cedex 9, France. Hiroyuki.Ogata@igs.cnrs-mrs.fr
Hiroyuki
H
Ogata
Jessica
J
Ray
Kensuke
K
Toyoda
Ruth-Anne
RA
Sandaa
Keizo
K
Nagasaki
Gunnar
G
Bratbak
Jean-Michel
JM
Claverie
D019295:Computational Biology; D053843:DNA Mismatch Repair; D004279:DNA, Viral / Q000235:genetics; D054892:Metagenome; D051719:MutS DNA Mismatch-Binding Protein / Q000235:genetics*; D017862:Phycodnaviridae / Q000235:genetics*; D010802:Phylogeny; D012623:Seawater / Q000821:virology*; D017422:Sequence Analysis, DNA; D014764:Viral Proteins / Q000235:genetics*
D004279:DNA, Viral; D014764:Viral Proteins; D051719:MutS DNA Mismatch-Binding Protein
J Mol Evol. 2006 Aug;63(2):165-73
16830098
Annu Rev Microbiol. 2003;57:579-608
14527292
Nucleic Acids Res. 2000 Jan 15;28(2):463-71
10606644
Appl Environ Microbiol. 2008 May;74(10):3048-57
18359826
J Mol Biol. 2000 Sep 8;302(1):205-17
10964570
Science. 2009 Jan 16;323(5912):379-82
19150844
Virol J. 2009 Oct 27;6:178
19860921
Nucleic Acids Res. 2010 Jan;38(Database issue):D142-8
19843607
Nat Rev Microbiol. 2009 Aug;7(8):615; author reply 615
19561626
Chem Rev. 2006 Feb;106(2):302-23
16464007
J Virol. 2010 Oct;84(19):9733-48
20660197
Vet Microbiol. 2005 Jul 1;108(3-4):215-23
15936904
Trends Microbiol. 2005 Nov;13(11):510-3
16157484
Appl Environ Microbiol. 1997 Apr;63(4):1551-6
9097450
Nucleic Acids Res. 2003 Oct 15;31(20):6027-34
14530450
Bioinformatics. 2007 Nov 1;23(21):2947-8
17846036
PLoS Biol. 2007 Mar;5(3):e77
17355176
Appl Environ Microbiol. 2008 Feb;74(4):1145-56
18065616
Annu Rev Microbiol. 2010;64:83-99
20690825
J Biol Chem. 2010 Sep 3;285(36):27664-72
20601642
Mol Biol Evol. 2008 Jul;25(7):1307-20
18367465
Science. 2004 Nov 19;306(5700):1344-50
15486256
Virology. 2009 Jul 20;390(1):102-9
19464038
BMC Genomics. 2007 Dec 10;8:456
18070355
Trends Genet. 2010 Oct;26(10):431-7
20696492
Mol Cell. 2005 Jan 7;17(1):113-20
15629722
J Invertebr Pathol. 2009 Jul;101(3):172-80
19457438
Virology. 2001 Nov 25;290(2):272-80
11883191
Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19508-13
20974979
Bioinformatics. 2005 May 1;21(9):2104-5
15647292
Mol Phylogenet Evol. 2006 Dec;41(3):513-27
16876445
Trends Biochem Sci. 2000 Sep;25(9):414-8
10973051
Genome Res. 2007 Sep;17(9):1353-61
17652424
Syst Biol. 2003 Oct;52(5):696-704
14530136
BMC Bioinformatics. 2009 Oct 27;10:356
19860910
Nucleic Acids Res. 2007;35(22):7591-603
17965091
PLoS Genet. 2006 May;2(5):e76
16703114
Virus Res. 2006 Apr;117(1):133-44
16469402
Curr Opin Struct Biol. 1996 Jun;6(3):361-5
8804822
Nature. 2008 Sep 4;455(7209):100-4
18690211
Intervirology. 2010;53(5):344-53
20551686
Trends Biochem Sci. 1999 Aug;24(8):298-300
10431172
Virol J. 2008 Jan 23;5:12
18215256
J Mol Evol. 2008 Aug;67(2):125-36
18506498
PLoS One. 2007 Dec 26;2(12):e1358
18159241
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
9254694
Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12146-50
17615243
Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160-4
1831267
Trends Ecol Evol. 2000 Aug;15(8):321-326
10884696
Genome Res. 2010 May;20(5):664-74
20360389
Nucleic Acids Res. 2003 Aug 15;31(16):4814-21
12907723
J Biol Chem. 2008 Nov 28;283(48):33417-27
18838375
Nature. 1995 May 11;375(6527):109-11
7753165
Nucleic Acids Res. 1998 Sep 15;26(18):4291-300
9722651
Brief Bioinform. 2008 Jul;9(4):299-306
18417537
Virol J. 2009 Dec 17;6:223
20017929