Comparative genomics analysis of Streptococcus isolates from the human small intestine reveals their adaptation to a highly dynamic ecosystem

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Van Den Bogert, Bartholomeus ^a,b   Boekhorst, Jos ^c,d   Herrmann, Ruth ^a,b   Smid, Eddy J ^a,b   Zoetendal, Erwin G ^a,b   Kleerebezem, Michiel ^a,b,d  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d NIZO FOOD RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; CARBOHYDRATE METABOLISM; CARBON; GENE-ENVIRONMENT INTERACTION; GENOME, BACTERIAL; HUMANS; INTESTINE, SMALL; METAGENOMICS; PHYLOGENY; PYRUVIC ACID; SEQUENCE ANALYSIS, DNA; STREPTOCOCCUS; VITAMINS;

EID: 84893619555     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083418     Document Type: Article

References (77)

1. De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, et al. (2009) Bergey's Manual of Systematic Bacteriology. New York: Springer.
2. Luca-Harari B, Darenberg J, Neal S, Siljander T, Strakova L, et al. (2009) Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 47: 115521165.
3. Kadioglu A, Weiser JN, Paton JC, Andrew PW (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 2882301.
4. Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, et al. (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dent Res 87: 101621020.
5. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43: 572125732.
6. Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, et al. (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 3: e2836.
7. Pei Z, Bini EJ, Yang L, Zhou M, Francois F, et al. (2004) Bacterial biota in the human distal esophagus. Proc Natl Acad Sci U S A 101: 425024255.
8. Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA, et al. (2006) Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci U S A 103: 7322737.
9. Booijink CC, El-Aidy S, Rajilić-Stojanović M, Heilig HG, Troost FJ, et al. (2010) High temporal and inter-individual variation detected in the human ileal microbiota. Environ Microbiol 12: 321323227.
10. van den Bogert B, de Vos WM, Zoetendal EG, Kleerebezem M (2011) Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl Environ Microbiol 77: 207122080.
11. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, et al. (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. Isme J 6: 141521426.
12. van den Bogert B, Erkus O, Boekhorst J, de Goffau M, Smid EJ, et al. (2013) Diversity of human small intestinal Streptococcus and Veillonella populations. FEMS Microbiol Ecol 85: 3762388.
13. Van den Bogert B, Leimena MM, De Vos WM, Zoetendal EG, Kleerebezem M (2011) Functional Intestinal Metagenomics. In: De Bruin FJ, editor. Handbook of Molecular Microbial Ecology. Hoboken, NJ: Wiley-Blackwell. pp. 1702190.
14. Leser TD, Molbak L (2009) Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ Microbiol 11: 219422206.
15. Booijink CC, Zoetendal EG, Kleerebezem M, de Vos WM (2007) Microbial communities in the human small intestine: coupling diversity to metagenomics. Future Microbiol 2: 2852295.
16. Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, et al. (2013) Microbiota conservation and BMI signatures in adult monozygotic twins. Isme J 7: 7072717.
17. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
18. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27: 5782579.
19. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, et al. (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 342223423.
20. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC genomics 9: 75.
21. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, et al. (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29: 22228.
22. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 179221797.
23. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 6962704.
24. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 3572358.
25. de Jong A, van Heel AJ, Kok J, Kuipers OP (2010) BAGEL2: mining for bacteriocins in genomic data. Nucleic Acids Res 38: W6472651.
26. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69: 1832215.
27. Havarstein LS (2010) Increasing competence in the genus Streptococcus. Mol Microbiol 78: 5412544.
28. Siguier P, Filee J, Chandler M (2006) Insertion sequences in prokaryotic genomes. Curr Opin Microbiol 9: 5262531.
29. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32236.
30. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 294722948.
31. Martin B, Humbert O, Camara M, Guenzi E, Walker J, et al. (1992) A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 20: 347923483.
32. Claverys JP, Martin B (1998) Competence regulons, genomics and streptococci. Mol Microbiol 29: 112621127.
33. Oggioni MR, Claverys JP (1999) Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology 145 (Pt 10): 264722653.
34. Croucher NJ, Vernikos GS, Parkhill J, Bentley SD (2011) Identification, variation and transcription of pneumococcal repeat sequences. BMC Genomics 12: 120.
35. Durbin R, S.R E, A K, Mitchison G (1998) Biological sequence analysis: probabilistic models of proteins and nucleic acids. Cambridge, United Kingdom: Cambridge University Press.
36. Kanehisa M (2002) The KEGG database. Novartis Found Symp 247: 912101; discussion 1012103, 1192128, 2442152.
37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 4032410.
38. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 3652386.
39. Salonen A, Nikkila J, Jalanka-Tuovinen J, Immonen O, Rajilić- Stojanović M, et al. (2010) Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Methods 81: 1272134.
40. Zoetendal EG, Booijink CC, Klaassens ES, Heilig HG, Kleerebezem M, et al. (2006) Isolation of RNA from bacterial samples of the human gastrointestinal tract. Nat Protoc 1: 9542959.
41. Zoetendal EG, Heilig HG, Klaassens ES, Booijink CC, Kleerebezem M, et al. (2006) Isolation of DNA from bacterial samples of the human gastrointestinal tract. Nat Protoc 1: 8702873.
42. Lefébure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus : positive selection, recombination, and genome composition. Genome Biol 8: R71.
43. Lukjancenko O, Ussery DW, Wassenaar TM (2012) Comparative genomics of Bifidobacterium, Lactobacillus and related probiotic genera. Microb Ecol 63: 6512673.
44. Kant R, Blom J, Palva A, Siezen RJ, de Vos WM (2011) Comparative genomics of Lactobacillus. Microb Biotechnol 4: 3232332.
45. Human Microbiome Jumpstart Reference Strains C, Nelson KE, Weinstock GM, Highlander SK, Worley KC, et al. (2010) A catalog of reference genomes from the human microbiome. Science 328: 9942999.
46. Poyart C, Quesne G, Trieu-Cuot P (2002) Taxonomic dissection of the Streptococcus bovis group by analysis of manganese-dependent superoxide dismutase gene (sodA) sequences: reclassification of 'Streptococcus infantarius subsp. coli' as Streptococcus lutetiensis sp. nov. and of Streptococcus bovis biotype 11.2 as Streptococcus pasteurianus sp. nov. International Journal of Systematic and Evolutionary Microbiology 52: 124721255.
47. Delorme C, Poyart C, Ehrlich SD, Renault P (2007) Extent of horizontal gene transfer in evolution of Streptococci of the salivarius group. J Bacteriol 189: 133021341.
48. Giammarinaro P, Sicard M, Gasc AM (1999) Genetic and physiological studies of the CiaH-CiaR two-component signal-transducing system involved in cefotaxime resistance and competence of Streptococcus pneumoniae. Microbiology 145 (Pt 8): 185921869.
49. Quach D, van Sorge NM, Kristian SA, Bryan JD, Shelver DW, et al. (2009) The CiaR response regulator in group B Streptococcus promotes intracellular survival and resistance to innate immune defenses. J Bacteriol 191: 202322032.
50. Mashburn-Warren L, Morrison DA, Federle MJ (2010) A novel double-tryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol Microbiol 78: 5892606.
51. Mascher T, Zahner D, Merai M, Balmelle N, de Saizieu AB, et al. (2003) The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. J Bacteriol 185: 60270.
52. Fontaine L, Boutry C, de Frahan MH, Delplace B, Fremaux C, et al. (2010) A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol 192: 144421454.
53. Kleerebezem M (2004) Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides 25: 140521414.
54. van Kraaij C, de Vos WM, Siezen RJ, Kuipers OP (1999) Lantibiotics: biosynthesis, mode of action and applications. Nat Prod Rep 16: 5752587.
55. Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3: 7772788.
56. Lamy MC, Zouine M, Fert J, Vergassola M, Couve E, et al. (2004) CovS/CovR of group B streptococcus : a two-component global regulatory system involved in virulence. Mol Microbiol 54: 125021268.
57. Tran-Winkler HJ, Love JF, Gryllos I, Wessels MR (2011) Signal transduction through CsrRS confers an invasive phenotype in group A Streptococcus. PLoS Pathog 7: e1002361.
58. Cheng Q, Stafslien D, Purushothaman SS, Cleary P (2002) The group B streptococcal C5a peptidase is both a specific protease and an invasin. Infect Immun 70: 240822413.
59. Wexler DE, Chenoweth DE, Cleary PP (1985) Mechanism of action of the group A streptococcal C5a inactivator. Proc Natl Acad Sci U S A 82: 814428148.
60. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, et al. (2004) Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22: 155421558.
61. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ, et al. (2003) Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149: 271922732.
62. Detmers FJ, Kunji ER, Lanfermeijer FC, Poolman B, Konings WN (1998) Kinetics and specificity of peptide uptake by the oligopeptide transport system of Lactococcus lactis. Biochemistry 37: 16671216679.
63. Kunji ER, Fang G, Jeronimus-Stratingh CM, Bruins AP, Poolman B, et al. (1998) Reconstruction of the proteolytic pathway for use of beta-casein by Lactococcus lactis. Mol Microbiol 27: 110721118.
64. Rogers AH (1973) The vitamin requirements of some oral streptococci. Arch Oral Biol 18: 2272232.
65. Kandler O (1983) Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 49: 2092224.
66. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100: 199021995.
67. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 8492852.
68. Siezen RJ, Bayjanov JR, Felis GE, van der Sijde MR, Starrenburg M, et al. (2011) Genome-scale diversity and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays. Microb Biotechnol 4: 3832402.
69. Kreft J, Vazquez-Boland JA (2001) Regulation of virulence genes in Listeria. Int J Med Microbiol 291: 1452157.
70. Hutkins RW, Ponne C (1991) Lactose Uptake Driven by Galactose Efflux in Streptococcus thermophilus: Evidence for a Galactose-Lactose Antiporter. Appl Environ Microbiol 57: 9412944.
71. Lessard C, Cochu A, Lemay JD, Roy D, Vaillancourt K, et al. (2003) Phosphorylation of Streptococcus salivarius lactose permease (LacS) by HPr(His ∼ P) and HPr(Ser-P)(His ∼ P) and effects on growth. J Bacteriol 185: 676426772.
72. Von Wright A, Axelsson L (2012) Lactic Acid Bacteria: An Introduction. In: Lahtinen S, Ouwehand AC, Salminen S, Von Wright A, editors. Lactic Acid Bacteria, Microbiological and functional aspects: CRC Press, Taylor & Francis Group.
73. Russell RR, Aduse-Opoku J, Sutcliffe IC, Tao L, Ferretti JJ (1992) A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem 267: 463124637.
74. Busuioc M, Mackiewicz K, Buttaro BA, Piggot PJ (2009) Role of intracellular polysaccharide in persistence of Streptococcus mutans. J Bacteriol 191: 731527322.
75. Rusniok C, Couve E, Da Cunha V, El Gana R, Zidane N, et al. (2010) Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol 192: 226622276.
76. Whitehead TR, Cotta MA (1995) Identification of intracellular amylase activity in Streptococcus bovis and Streptococcus salivarius. Curr Microbiol 30: 1432148.
77. Simpson CL, Russell RR (1998) Intracellular alpha-amylase of Streptococcus mutans. J Bacteriol 180: 471124717.