A new perspective on Listeria monocytogenes evolution.
Listeria monocytogenes is a model organism for cellular microbiology and host-pathogen interaction studies and an important food-borne pathogen widespread in the environment, thus representing an attractive model to study the evolution of virulence. The phylogenetic structure of L. monocytogenes was determined by sequencing internal portions of seven housekeeping genes (3,288 nucleotides) in 360 representative isolates. Fifty-eight of the 126 disclosed sequence types were grouped into seven well-demarcated clonal complexes (clones) that comprised almost 75% of clinical isolates. Each clone had a unique or dominant serotype (4b for clones 1, 2 and 4, 1/2b for clones 3 and 5, 1/2a for clone 7, and 1/2c for clone 9), with no association of clones with clinical forms of human listeriosis. Homologous recombination was extremely limited (r/m<1 for nucleotides), implying long-term genetic stability of multilocus genotypes over time. Bayesian analysis based on 438 SNPs recovered the three previously defined lineages, plus one unclassified isolate of mixed ancestry. The phylogenetic distribution of serotypes indicated that serotype 4b evolved once from 1/2b, the likely ancestral serotype of lineage I. Serotype 1/2c derived once from 1/2a, with reference strain EGDe (1/2a) likely representing an intermediate evolutionary state. In contrast to housekeeping genes, the virulence factor internalin (InlA) evolved by localized recombination resulting in a mosaic pattern, with convergent evolution indicative of natural selection towards a truncation of InlA protein. This work provides a reference evolutionary framework for future studies on L. monocytogenes epidemiology, ecology, and virulence.
Ragon
Marie
M
Institut Pasteur, Laboratoire des Listeria, Paris, France.
Wirth
Thierry
T
Hollandt
Florian
F
Lavenir
Rachel
R
Lecuit
Marc
M
Le Monnier
Alban
A
Brisse
Sylvain
S
D005075:Biological Evolution; D019143:Evolution, Molecular; D005798:Genes, Bacterial; D014644:Genetic Variation; D016680:Genome, Bacterial; D008089:Listeria monocytogenes / Q000235:genetics*; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide; D011995:Recombination, Genetic; D017422:Sequence Analysis, DNA
Appl Environ Microbiol. 1994 Jul;60(7):2584-92
8074531
J Bacteriol. 2004 Aug;186(15):4994-5002
15262937
Appl Environ Microbiol. 2004 Apr;70(4):2193-203
15066813
Infect Immun. 1997 Jul;65(7):2707-16
9199440
J Clin Microbiol. 2006 Oct;44(10):3742-51
17021104
Bioinformatics. 2005 Jan 15;21(2):260-2
15377507
Microbiology (Reading). 2001 May;147(Pt 5):1095-1104
11320113
J Clin Microbiol. 2004 Nov;42(11):5270-6
15528725
Infect Immun. 1991 Nov;59(11):3945-51
1937753
Science. 1994 Nov 25;266(5189):1380-3
7973728
J Bacteriol. 2005 Aug;187(16):5537-51
16077098
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3140-5
9501229
Int J Food Microbiol. 2001 Apr 11;65(1-2):55-62
11322701
J Clin Microbiol. 2008 Apr;46(4):1478-84
18256228
J Clin Microbiol. 1994 Dec;32(12):2936-43
7883880
Eur J Clin Microbiol. 1986 Apr;5(2):169-71
3087749
Genetics. 2006 Mar;172(3):1411-25
16387887
Infect Immun. 1998 Jul;66(7):3420-2
9632615
J Bacteriol. 2004 Aug;186(16):5496-505
15292152
Science. 2001 Jun 1;292(5522):1722-5
11387478
Nat Rev Microbiol. 2004 Jun;2(6):483-95
15152204
Appl Environ Microbiol. 2004 Apr;70(4):2180-5
15066811
Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12619-24
9770535
Proc Natl Acad Sci U S A. 1989 May;86(10):3818-22
2498876
Cell. 1991 Jun 28;65(7):1127-41
1905979
J Med Microbiol. 2006 Jun;55(Pt 6):645-659
16687581
Science. 2001 Oct 26;294(5543):849-52
11679669
Int J Food Microbiol. 1998 Aug 18;43(1-2):61-71
9761339
N Engl J Med. 1983 Jan 27;308(4):203-6
6401354
Nucleic Acids Res. 2007;35(3):962-74
17259222
Genetics. 2003 Jul;164(3):1229-36
12871927
Genetics. 2007 Mar;175(3):1251-66
17151252
Annu Rev Microbiol. 2001;55:561-90
11544367
J Clin Microbiol. 2003 Feb;41(2):757-62
12574278
Infect Immun. 2004 Feb;72(2):1072-83
14742555
Infect Genet Evol. 2006 Mar;6(2):97-112
16503511
Microbiol Rev. 1991 Sep;55(3):476-511
1943998
Mol Biol Evol. 2006 Feb;23(2):254-67
16221896
Clin Microbiol Rev. 2001 Jul;14(3):584-640
11432815
Genetics. 2002 Mar;160(3):1231-41
11901136
Cell. 2002 Dec 13;111(6):825-36
12526809
Appl Environ Microbiol. 2005 Dec;71(12):8764-72
16332872
Am J Vet Res. 2006 Apr;67(4):616-26
16579754
Int J Syst Bacteriol. 1997 Oct;47(4):1145-56
9336922
Nat Rev Microbiol. 2006 Jun;4(6):423-34
16710323
J Clin Microbiol. 2004 Jan;42(1):276-85
14715765
Bioinformatics. 1999 Feb;15(2):174-5
10089204
Appl Environ Microbiol. 2007 Jan;73(1):133-47
17085705
J Bacteriol. 1991 Nov;173(22):7257-68
1938920
Microbiology (Reading). 1995 Sep;141 ( Pt 9):2053-61
7496516
Infect Immun. 2003 Mar;71(3):1217-24
12595435
J Clin Microbiol. 2007 Mar;45(3):835-46
17215339
Pol J Microbiol. 2006;55(1):31-5
16878601
J Infect Dis. 2004 Jun 1;189(11):2094-100
15143478
Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):2045-53
17062419
J Clin Microbiol. 2004 Aug;42(8):3819-22
15297538
J Bacteriol. 2003 Jun;185(11):3307-16
12754228
Microbiology (Reading). 2007 Aug;153(Pt 8):2666-2678
17660431
Appl Environ Microbiol. 2004 Feb;70(2):913-20
14766571
J Gen Microbiol. 1988 Sep;134(9):2593-8
3151210
Mol Microbiol. 2006 Jun;60(5):1136-51
16689791
Appl Environ Microbiol. 2005 Feb;71(2):961-7
15691954
J Food Prot. 1993 Apr;56(4):297-301
31091625
Int J Antimicrob Agents. 2007 Feb;29(2):129-35
17204401
J Clin Microbiol. 2003 Apr;41(4):1623-36
12682154
Mol Biol Evol. 1999 Nov;16(11):1496-502
10555280
Genetics. 2000 Jun;155(2):945-59
10835412
Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384-8
8506277
Syst Appl Microbiol. 2000 Apr;23(1):132-6
10879987
Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):1917-27
17062411
Int J Food Microbiol. 2007 Mar 10;114(2):187-94
17188773
Cell. 1996 Mar 22;84(6):923-32
8601315
Bioinformatics. 2001 Dec;17(12):1244-5
11751241
Nat Rev Microbiol. 2005 Sep;3(9):733-9
16138101
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):182-7
11136255
Genetics. 2003 Aug;164(4):1567-87
12930761