Helicobacter pylori evolution: lineage- specific adaptations in homologs of eukaryotic Sel1-like genes.
Geographic partitioning is postulated to foster divergence of Helicobacter pylori populations as an adaptive response to local differences in predominant host physiology. H. pylori's ability to establish persistent infection despite host inflammatory responses likely involves active management of host defenses using bacterial proteins that may themselves be targets for adaptive evolution. Sequenced H. pylori genomes encode a family of eight or nine secreted proteins containing repeat motifs that are characteristic of the eukaryotic Sel1 regulatory protein, whereas the related Campylobacter and Wolinella genomes each contain only one or two such "Sel1-like repeat" (SLR) genes ("slr genes"). Signatures of positive selection (ratio of nonsynonymous to synonymous mutations, dN/dS = omega > 1) were evident in the evolutionary history of H. pylori slr gene family expansion. Sequence analysis of six of these slr genes (hp0160, hp0211, hp0235, hp0519, hp0628, and hp1117) from representative East Asian, European, and African H. pylori strains revealed that all but hp0628 had undergone positive selection, with different amino acids often selected in different regions. Most striking was a divergence of Japanese and Korean alleles of hp0519, with Japanese alleles having undergone particularly strong positive selection (omegaJ > 25), whereas alleles of other genes from these populations were intermingled. Homology-based structural modeling localized most residues under positive selection to SLR protein surfaces. Rapid evolution of certain slr genes in specific H. pylori lineages suggests a model of adaptive change driven by selection for fine-tuning of host responses, and facilitated by geographic isolation. Characterization of such local adaptations should help elucidate how H. pylori manages persistent infection, and potentially lead to interventions tailored to diverse human populations.
Ogura
Masako
M
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri, United States of America.
Perez
J Christian
JC
Mittl
Peer R E
PR
Lee
Hae-Kyung
HK
Dailide
Geidrius
G
Tan
Shumin
S
Ito
Yoshiyuki
Y
Secka
Ousman
O
Dailidiene
Daiva
D
Putty
Kalyani
K
Berg
Douglas E
DE
Kalia
Awdhesh
A
D000222:Adaptation, Physiological / Q000502:physiology*; D000595:Amino Acid Sequence; D005075:Biological Evolution; D002352:Carrier Proteins / Q000235:genetics*; D002874:Chromosome Mapping / Q000379:methods; D019143:Evolution, Molecular; D016680:Genome, Bacterial / Q000235:genetics*; D016480:Helicobacter pylori / Q000235:genetics*; D008969:Molecular Sequence Data; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics*; D020539:Sequence Analysis, Protein / Q000379:methods*; D017386:Sequence Homology, Amino Acid
D002352:Carrier Proteins; D029701:Saccharomyces cerevisiae Proteins; C507001:UBX2 protein, S cerevisiae
Mol Biol Evol. 1998 May;15(5):568-73
9580986
Genetics. 2003 Jul;164(3):1229-36
12871927
Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12619-24
9770535
Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13108-13
9789049
Nature. 1999 Jan 14;397(6715):176-80
9923682
Mol Microbiol. 1999 Jan;31(1):31-43
9987107
Mol Microbiol. 1999 May;32(3):459-70
10320570
Science. 1999 May 21;284(5418):1328-33
10334982
J Biol Chem. 2000 Jun 9;275(23):17693-9
10748053
Science. 2000 Nov 10;290(5494):1151-5
11073452
Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15056-61
11742075
J Bacteriol. 2002 Feb;184(4):992-1002
11807059
J Biol Chem. 2002 Mar 22;277(12):10187-93
11777911
Mol Biol Evol. 2002 Jun;19(6):908-17
12032247
Science. 2002 Jul 26;297(5581):573-8
12142529
Mol Biol Evol. 2002 Oct;19(10):1686-94
12270895
Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14428-33
12391297
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14878-83
12403824
Curr Opin Genet Dev. 2002 Dec;12(6):688-94
12433583
Nat Genet. 2002 Dec;32(4):569-77
12457190
Science. 2003 Mar 7;299(5612):1582-5
12624269
Gastric Cancer. 2002;5 Suppl 1:5-11
12772880
J Clin Microbiol. 1999 Jul;37(7):2274-9
10364597
J Bacteriol. 1999 Aug;181(16):5107-10
10438788
Infect Immun. 1999 Sep;67(9):4713-9
10456921
Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11690-5
14500908
J Bacteriol. 2004 Jan;186(2):356-65
14702304
Gene. 2004 Feb 4;326:149-56
14729273
J Clin Invest. 2004 Feb;113(3):321-33
14755326
J Mol Biol. 2004 Jul 16;340(4):829-41
15223324
Science. 2004 Jul 23;305(5683):519-22
15273394
Nucleic Acids Res. 1992 Oct 11;20(19):5137-42
1408828
Trends Microbiol. 1993 Oct;1(7):255-60
8162405
Mol Biol Evol. 1996 Jul;13(6):735-48
8754210
Genetics. 1996 May;143(1):237-47
8722778
J Clin Microbiol. 1997 Jul;35(7):1710-4
9196179
Nature. 1997 Aug 7;388(6642):539-47
9252185
Nat Med. 1997 Oct;3(10):1076-8
9334711
Natl Med J India. 1998 Jan-Feb;11(1):5-8
9557510
J Bacteriol. 2004 Nov;186(22):7508-20
15516562
PLoS Biol. 2005 Jan;3(1):e15
15660156
Helicobacter. 2005 Apr;10(2):107-13
15810940
Cancer Epidemiol Biomarkers Prev. 2005 Jun;14(6):1464-9
15941957
Infect Immun. 2005 Aug;73(8):4732-42
16040986
Genetics. 2005 Jul;170(3):1323-32
15879511
J Bacteriol. 2005 Nov;187(22):7687-95
16267293
Curr Opin Gastroenterol. 2006 Jan;22(1):3-7
16319669
Microbes Infect. 2006 Jan;8(1):52-60
16260169
Nat Rev Genet. 2006 May;7(5):337-48
16619049
J Cell Physiol. 2006 Jul;208(1):23-38
16331677
Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9999-10004
16788065
Clin Microbiol Rev. 2006 Jul;19(3):449-90
16847081
PLoS Genet. 2006 Jul;2(7):e120
16789826
Clin Microbiol Rev. 2006 Oct;19(4):597-613
17041136
Nat Rev Microbiol. 2006 Nov;4(11):826-36
17041630
Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17319-24
17082307
Cell Signal. 2007 Jan;19(1):20-31
16870393
Annu Rev Pathol. 2006;1:63-96
18039108
Nature. 2000 Feb 10;403(6770):665-8
10688204
Genetics. 2000 May;155(1):431-49
10790415
Clin Diagn Lab Immunol. 2003 Jul;10(4):542-5
12853383
Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7901-6
12810954
J Bacteriol. 2000 Jun;182(11):3210-8
10809702
J Infect Dis. 1998 Jul;178(1):220-6
9652444