Evolutionary Dynamics of the Accessory Genome of Listeria monocytogenes

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  den Bakker, Henk C ^a   Desjardins, Christopher A ^b   Griggs, Allison D ^b   Peters, Joseph E ^a   Zeng, Qiandong ^b   Young, Sarah K ^b   Kodira, Chinnappa D ^b   Yandava, Chandri ^b   Hepburn, Theresa A ^b   Haas, Brian J ^b   Birren, Bruce W ^b   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; O ANTIGEN; PHOSPHOTRANSFERASE; REGULATOR PROTEIN;

ACCESSORY GENE; ARTICLE; BACILLUS CEREUS; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL STRAIN; CELL SURFACE; DNA REPLICATION ORIGIN; GENE CLUSTER; GENE MAPPING; GENE SEQUENCE; GENETIC VARIABILITY; HORIZONTAL GENE TRANSFER; LISTERIA MONOCYTOGENES; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PHYLOGENY; PREDICTION; SEQUENCE ANALYSIS; SEROTYPE; STAPHYLOCOCCUS AUREUS;

CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; GENOMICS; LISTERIA MONOCYTOGENES; O ANTIGENS; PHOSPHOTRANSFERASES; PHYLOGENY; PROPHAGES;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; STAPHYLOCOCCUS AUREUS;

EID: 84879370410     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067511     Document Type: Article

References (75)

1. Gray MJ, Freitag NE, Boor KJ, (2006) How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr. Jekyll to pathogenic Mr. Hyde. Infect Immun 74: 2505-2512 doi:10.1128/IAI.74.5.2505-2512.2006.
2. Orsi RH, Bakker den HC, Wiedmann M, (2011) Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 301: 79-96 doi:10.1016/j.ijmm.2010.05.002.
3. Roberts AJ, Nightingale KK, Jeffers G, Fortes ED, Kongo JM, et al. (2006) Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology (Reading, Engl) 152: 685-693 doi:10.1099/mic.0.28503-0.
4. Bille J, Rocourt J, (1996) WHO International Multicenter Listeria monocytogenes Subtyping Study-rationale and set-up of the study. Int J Food Microbiol 32: 251-262.
5. Seeliger HPR, Höhne K (1979) Chapter II Serotyping of Listeria monocytogenes and Related Species. In: Norris TBAJR, editor. Methods in Microbiology. Methods in Microbiology. Academic Press, Vol. Volume 13. 31-49T2-. doi: 10.1016/S0580-9517(08)70372-6.
6. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, et al. (2008) A New Perspective on Listeria monocytogenes Evolution. PLoS Pathog 4: e1000146 doi:10.1371/journal.ppat.1000146.
7. Fiedler F, (1988) Biochemistry of the cell surface of Listeria strains: a locating general view. Infection 16Suppl 2: S92-S97.
8. Uchikawa K, Sekikawa I, Azuma I, (1986) Structural studies on lipoteichoic acids from four Listeria strains. J Bacteriol 168: 115-122.
9. Kamisango K, Fujii H, Okumura H, Saiki I, Araki Y, et al. (1983) Structural and immunochemical studies of teichoic acid of Listeria monocytogenes. J Biochem 93: 1401-1409.
10. Uchikawa K, Sekikawa I, Azuma I, (1986) Structural studies on teichoic acids in cell walls of several serotypes of Listeria monocytogenes. J Biochem 99: 315-327.
11. Zhang C, Zhang M, Ju J, Nietfeldt J, Wise J, et al. (2003) Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes: identification of segments unique to lineage II populations. J Bacteriol 185: 5573-5584.
12. Grimont PAD, Weill F (2007) Antigenic formulae of the Salmonella serovars. WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur, Paris, France.
13. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, BockemUhl J, et al. (2010) Supplement 2003-2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Research in Microbiology 161: 26-29 doi:10.1016/j.resmic.2009.10.002.
14. Deng X, Phillippy AM, Li Z, Salzberg SL, Zhang W, (2010) Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification. BMC Genomics 11: 500 doi:10.1186/1471-2164-11-500.
15. Orsi RH, Sun Q, Wiedmann M, (2008) Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes. BMC Evol Biol 8: 233 doi:10.1186/1471-2148-8-233.
16. Dunn KA, Bielawski JP, Ward TJ, Urquhart C, Gu H, (2009) Reconciling ecological and genomic divergence among lineages of Listeria under an "extended mosaic genome concept.". Mol Biol Evol 26: 2605-2615 doi:10.1093/molbev/msp176.
17. Tettelin H, Riley D, Cattuto C, Medini D, (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11: 472-477.
18. Coleman ML, Chisholm SW, (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 107: 18634-18639 doi:10.1073/pnas.1009480107.
19. Steele CL, Donaldson JR, Paul D, Banes MM, Arick T, et al. (2011) Genome sequence of lineage III Listeria monocytogenes strain HCC23. J Bacteriol 193: 3679-3680 doi:10.1128/JB.05236-11.
20. Nelson KE, Fouts DE, Mongodin EF, Ravel J, DeBoy RT, et al. (2004) Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res 32: 2386-2395 doi:10.1093/nar/gkh562.
21. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 849-852 doi:10.1126/science.1063447.
22. Hain T, Steinweg C, Kuenne CT, Billion A, Ghai R, et al. (2006) Whole-genome sequence of Listeria welshimeri reveals common steps in genome reduction with Listeria innocua as compared to Listeria monocytogenes. J Bacteriol 188: 7405-7415 doi:10.1128/JB.00758-06.
23. Steinweg C, Kuenne CT, Billion A, Mraheil MA, Domann E, et al. (2010) Complete genome sequence of Listeria seeligeri, a nonpathogenic member of the genus Listeria. J Bacteriol 192: 1473-1474 doi:10.1128/JB.01415-09.
24. Bakker den HC, Bowen BM, Rodriguez-Rivera LD, Wiedmann M (2012) FSL J1-208: a virulent uncommon phylogenetic lineage IV Listeria monocytogenes strain with a small chromosome size and a putative virulence plasmid carrying internalin-like genes. Appl Environ Microbiol. doi:10.1128/AEM.06969-11.
25. Gilmour MW, Graham M, van Domselaar G, Tyler S, Kent H, et al. (2010) High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11: 120 doi:10.1186/1471-2164-11-120.
26. Kämper J, Kahmann R, Bölker M, Ma L-J, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101 doi:10.1038/nature05248.
27. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380 doi:10.1038/nature03959.
28. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59 doi:10.1038/nature07517.
29. Jaffe DB, Butler J, Gnerre S, Mauceli E, Lindblad-Toh K, et al. (2003) Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res 13: 91-96 doi:10.1101/gr.828403.
30. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL, (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27: 4636-4641.
31. Noguchi H, Park J, Takagi T, (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34: 5623-5630 doi:10.1093/nar/gkl723.
32. Borodovsky M, McIninch J, (1993) Recognition of genes in DNA sequence with ambiguities. BioSystems 30: 161-171.
33. Holder JW, Ulrich JC, DeBono AC, Godfrey PA, Desjardins CA, et al. (2011) Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. PLoS Genet 7: e1002219 doi:10.1371/journal.pgen.1002219.
34. Delcher AL, Kasif S, Fleischmann RD, Peterson J, White O, et al. (1999) Alignment of whole genomes. Nucleic Acids Res 27: 2369-2376.
35. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, et al. (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13: 721-731 doi:10.1101/gr.926603.
36. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T, et al. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100-3108 doi:10.1093/nar/gkm160.
37. Lowe TM, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
38. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, et al. (2005) Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33: D121-D124 doi:10.1093/nar/gki081.
39. Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435 doi:10.1093/nar/gkn176.
40. Li L, Stoeckert CJ, Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189 doi:10.1101/gr.1224503.
41. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797 doi:10.1093/nar/gkh340.
42. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T, (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973 doi:10.1093/bioinformatics/btp348.
43. Price MN, Dehal PS, Arkin AP, (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641-1650 doi:10.1093/molbev/msp077.
44. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591 doi:10.1093/molbev/msm088.
45. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690 doi:10.1093/bioinformatics/btl446.
46. Britton T, Anderson CL, Jacquet D, Lundqvist S, Bremer K, (2007) Estimating divergence times in large phylogenetic trees. Systematic Biology 56: 741-752 doi:10.1080/10635150701613783.
47. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344 doi:10.1371/journal.pgen.1000344.
48. Janssen PJ, Audit B, Ouzounis CA, (2001) Strain-specific genes of Helicobacter pylori: distribution, function and dynamics. Nucleic Acids Res 29: 4395-4404.
49. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J, et al. (2012) Comparative Genomics of Enterococci: Variation in Enterococcus faecalis, Clade Structure in E. faecium, and Defining Characteristics of E. gallinarum and E. casseliflavus. mBio 3. doi:10.1128/mBio.00318-11.
50. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645 doi:10.1101/gr.092759.109.
51. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
52. Bakker den HC, Bundrant BN, Fortes ED, Orsi RH, Wiedmann M, (2010) A population genetics-based and phylogenetic approach to understanding the evolution of virulence in the genus Listeria. Appl Environ Microbiol 76: 6085-6100 doi:10.1128/AEM.00447-10.
53. David LA, Alm EJ, (2011) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469: 93-96 doi:10.1038/nature09649.
54. Doyon J-P, Ranwez V, Daubin V, Berry V, (2011) Models, algorithms and programs for phylogeny reconciliation. Brief Bioinformatics 12: 392-400 doi:10.1093/bib/bbr045.
55. Etherington GJ, Dicks J, Roberts IN, (2005) Recombination Analysis Tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics 21: 278-281 doi:10.1093/bioinformatics/bth500.
56. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, et al. (2008) Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9: 539 doi:10.1186/1471-2164-9-539.
57. Ward TJ, Ducey TF, Usgaard T, Dunn KA, Bielawski JP, (2008) Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl Environ Microbiol 74: 7629-7642 doi:10.1128/AEM.01127-08.
58. Kuenne C, Billion A, Mraheil MA, Strittmatter A, Daniel R, et al. (2013) Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics 14: 47 doi:10.1186/1471-2164-14-47.
59. Webb AJ, Karatsa-Dodgson M, Gründling A, (2009) Two-enzyme systems for glycolipid and polyglycerolphosphate lipoteichoic acid synthesis in Listeria monocytogenes. Mol Microbiol 74: 299-314 doi:10.1111/j.1365-2958.2009.06829.x.
60. Promadej N, Fiedler F, Cossart P, Dramsi S, Kathariou S, (1999) Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene. J Bacteriol 181: 418-425.
61. Lei XH, Fiedler F, Lan Z, Kathariou S, (2001) A novel serotype-specific gene cassette (gltA-gltB) is required for expression of teichoic acid-associated surface antigens in Listeria monocytogenes of serotype 4b. J Bacteriol 183: 1133-1139 doi:10.1128/JB.183.4.1133-1139.2001.
62. Cheng Y, Promadej N, Kim J-W, Kathariou S, (2008) Teichoic acid glycosylation mediated by gtcA is required for phage adsorption and susceptibility of Listeria monocytogenes serotype 4b. Appl Environ Microbiol 74: 1653-1655 doi:10.1128/AEM.01773-07.
63. Denapaite D, Brückner R, Hakenbeck R, Vollmer W, (2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb Drug Resist 18: 344-358 doi:10.1089/mdr.2012.0026.
64. Lazarevic V, Abellan F-X, Möller SB, Karamata D, Mauël C, (2002) Comparison of ribitol and glycerol teichoic acid genes in Bacillus subtilis W23 and 168: identical function, similar divergent organization, but different regulation. Microbiology (Reading, Engl) 148: 815-824.
65. Faith N, Kathariou S, Cheng Y, Promadej N, Neudeck BL, et al. (2009) The role of L. monocytogenes serotype 4b gtcA in gastrointestinal listeriosis in A/J mice. Foodborne Pathog Dis 6: 39-48 doi:10.1089/fpd.2008.0154.
66. Lan Z, Fiedler F, Kathariou S, (2000) A sheep in wolf's clothing: Listeria innocua strains with teichoic acid-associated surface antigens and genes characteristic of Listeria monocytogenes serogroup 4. J Bacteriol 182: 6161-6168.
67. Hain T, Steinweg C, Chakraborty T, (2006) Comparative and functional genomics of Listeria spp. J Biotechnol 126: 37-51 doi:10.1016/j.jbiotec.2006.03.047.
68. Mira A, Ochman H, Moran NA, (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589-596.
69. Mercier R, Petit MA, Schbath S, Robin S, Karoui El M, et al. (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135: 475-485 doi:10.1016/j.cell.2008.08.031.
70. Thiel A, Valens M, Vallet-Gely I, Espeli O, Boccard F, (2012) Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain. PLoS Genet 8: e1002672 doi:10.1371/journal.pgen.1002672.
71. Martincorena I, Seshasayee ASN, Luscombe NM (2012) Evidence of non-random mutation rates suggests an evolutionary risk management strategy. Nature. doi:10.1038/nature10995.
72. Doumith M, Cazalet C, Simoes N, Frangeul L, Jacquet C, et al. (2004) New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infect Immun 72: 1072-1083.
73. Bierne H, Sabet C, Personnic N, Cossart P, (2007) Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 9: 1156-1166 doi:10.1016/j.micinf.2007.05.003.
74. Stoll R, Goebel W, (2010) The major PEP-phosphotransferase systems (PTSs) for glucose, mannose and cellobiose of Listeria monocytogenes, and their significance for extra- and intracellular growth. Microbiology (Reading, Engl) 156: 1069-1083 doi:10.1099/mic.0.034934-0.
75. Kjos M, Salehian Z, Nes IF, Diep DB, (2010) An Extracellular Loop of the Mannose Phosphotransferase System Component IIC Is Responsible for Specific Targeting by Class IIa Bacteriocins. J Bacteriol 192: 5906-5913 doi:10.1128/JB.00777-10.