Comparative genomics of Lactobacillus crispatus suggests novel mechanisms for the competitive exclusion of Gardnerella vaginalis

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Ojala, Teija ^a   Kankainen, Matti ^a,b   Castro, Joana ^c   Cerca, Nuno ^c   Edelman, Sanna ^d   Westerlund Wikström, Benita ^b   Paulin, Lars ^a   Holm, Liisa ^a,b   Auvinen, Petri ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF MINHO   (Portugal)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

Bacterial vaginosis; Comparative genomics; Competitive exclusion; Core genome; Gardnerella vaginalis; Lactobacillus crispatus; Normal flora; Pan genome

Indexed keywords

ADHESIN; CORE PROTEIN; EXOPOLYSACCHARIDE; PROBIOTIC AGENT; BACTERIAL POLYSACCHARIDE;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; COMPARATIVE STUDY; COMPETITIVE EXCLUSION; CONTROLLED STUDY; CRISPR CAS SYSTEM; GARDNERELLA VAGINALIS; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; HORIZONTAL GENE TRANSFER; LACTOBACILLUS CRISPATUS; MOLECULAR PHYLOGENY; NONHUMAN; PROTEIN FUNCTION; STRAIN DIFFERENCE; ANTIBIOSIS; BIOLOGY; CELL WALL; CLASSIFICATION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; FEMALE; GENE ORDER; GENETICS; GENOMICS; HELA CELL LINE; HUMAN; LACTOBACILLUS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; VIROLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); GARDNERELLA VAGINALIS; LACTOBACILLUS CRISPATUS;

ANTIBIOSIS; BACTERIAL ADHESION; BACTERIOPHAGES; CELL WALL; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; COMPUTATIONAL BIOLOGY; FEMALE; GARDNERELLA VAGINALIS; GENE ORDER; GENE TRANSFER, HORIZONTAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; HELA CELLS; HUMANS; LACTOBACILLUS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE ANNOTATION; MULTIGENE FAMILY; PHYLOGENY; POLYSACCHARIDES, BACTERIAL;

EID: 84924290099     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1070     Document Type: Article

References (115)

1. Siezen RJ, Wilson G: Probiotics genomics. J Microbial Biotechnol 2010,3(1):1-9.
2. Ventura M, O'Flaherty S, Claesson MJ, Turroni F, Klaenhammer TR, van Sinderen D, O'Toole PW: Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 2009,7(1):61-71.
3. Uehara S, Monden K, Nomoto K, Seno Y, Kariyama R, Kumon H: A pilot study evaluating the safety and effectiveness of Lactobacillus vaginal suppositories in patients with recurrent urinary tract infection. Int J Antimicrob Agents 2006,28(Suppl 1):S30-4.
4. Stapleton AE, Au-Yeung M, Hooton TM, Fredricks DN, Roberts PL, Czaja CA, Yarova-Yarovaya Y, Fiedler T, Cox M, Stamm WE: Randomized, placebo-controlled phase 2 trial of a Lactobacillus crispatus probiotic given intravaginally for prevention of recurrent urinary tract infection. Clin Infect Dis 2011,52(10):1212-1217.
5. Hemmerling A, Harrison W, Schroeder A, Park J, Korn A, Shiboski S, Cohen CR: Phase 1 dose-ranging safety trial of Lactobacillus crispatus CTV-05 for the prevention of bacterial vaginosis. Sex Transm Dis 2009,36(9):564-569.
6. Antonio MA, Meyn LA, Murray PJ, Busse B, Hillier SL: Vaginal colonization by probiotic Lactobacillus crispatus CTV-05 is decreased by sexual activity and endogenous Lactobacilli. J Infect Dis 2009,199(10):1506-1513.
7. Lamont RF, Sobel JD, Akins RA, Hassan SS, Chaiworapongsa T, Kusanovic JP, Romero R: The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG 2011,118(5):533-549.
8. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ: Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011,108(Suppl 1):4680-4687.
9. Witkin SS, Linhares IM, Giraldo P: Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol 2007,21(3):347-354.
10. Macklaim J, Fernandes A, Di Bella J, Hammond J, Reid G, Gloor G: Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome 2013,1(1):12.
11. Verstraelen H, Verhelst R, Claeys G, De Backer E, Temmerman M, Vaneechoutte M: Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora. BMC Microbiol 2009, 9:116-2180-9-116.
12. Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM: Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol 2007,45(10):3270-3276.
13. Zárate G, Nader-Macias ME: Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells. Lett Appl Microbiol 2006,43(2):174-180.
14. Osset J, Bartolomé RM, García E, Andreu A: Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J Infect Dis 2001,183(3):485-491.
15. Atassi F, Brassart D, Grob P, Graf F, Servin AL: Vaginal Lactobacillus isolates inhibit uropathogenic Escherichia coli. FEMS Microbiol Lett 2006,257(1):132-138.
16. Teixeira GS, Carvalho FP, Arantes RM, Nunes AC, Moreira JL, Mendonca M, Almeida RB, Farias LM, Carvalho MA, Nicoli JR: Characteristics of Lactobacillus and Gardnerella vaginalis from women with or without bacterial vaginosis and their relationships in gnotobiotic mice. J Med Microbiol 2012,61(Pt 8):1074-1081.
17. Castro J, Henriques A, Machado A, Henriques M, Jefferson KK, Cerca N: Reciprocal interference between Lactobacillus spp. and Gardnerella vaginalis on initial adherence to epithelial cells. Int J Med Sci 2013,10(9):1193-1198.
18. Abbas Hilmi HT, Surakka A, Apajalahti J, Saris PE: Identification of the most abundant lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Appl Environ Microbiol 2007,73(24):7867-7873.
19. Yuki N, Shimazaki T, Kushiro A, Watanabe K, Uchida K, Yuyama T, Morotomi M: Colonization of the stratified squamous epithelium of the nonsecreting area of horse stomach by lactobacilli. Appl Environ Microbiol 2000,66(11):5030-5034.
20. De Angelis M, Siragusa S, Berloco M, Caputo L, Settanni L, Alfonsi G, Amerio M, Grandi A, Ragni A, Gobbetti M: Selection of potential probiotic lactobacilli from pig feces to be used as additives in pelleted feeding. Res Microbiol 2006,157(8):792-801.
21. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP: Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 2001,67(6):2578-2585.
22. Kleerebezem M, Vaughan EE: Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 2009, 63:269-290.
23. Walter J: Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 2008,74(16):4985-4996.
24. Marrazzo JM, Fiedler TL, Srinivasan S, Thomas KK, Liu C, Ko D, Xie H, Saracino M, Fredricks DN: Extravaginal reservoirs of vaginal bacteria as risk factors for incident bacterial vaginosis. J Infect Dis 2012,205(10):1580-1588.
25. Antonio MA, Rabe LK, Hillier SL: Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J Infect Dis 2005,192(3):394-398.
26. Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR, Rusch DB, Mitreva M, Sodergren E, Chinwalla AT, Feldgarden M, Gevers D, Haas BJ, Madupu R, Ward DV, Birren BW, Gibbs RA, Methe B, Petrosino JF, Strausberg RL, Sutton GG, White OR, Wilson RK, Durkin S, Giglio MG, Gujja S, Howarth C, Kodira CD, Kyrpides N, Mehta T, et al.: A catalog of reference genomes from the human microbiome. Science 2010,328(5981):994-999.
27. Ojala T, Kuparinen V, Koskinen JP, Alatalo E, Holm L, Auvinen P, Edelman S, Westerlund-Wikström B, Korhonen TK, Paulin L, Kankainen M: Genome sequence of Lactobacillus crispatus ST1. J Bacteriol 2010,192(13):3547-3548.
28. Salvetti E, Torriani S, Felis G: The Genus Lactobacillus: A Taxonomic Update. Probiotics Antimicrob Proteins 2012,4(4):217-226.
29. Kant R, Blom J, Palva A, Siezen RJ, de Vos WM: Comparative genomics of Lactobacillus. Microb Biotechnol 2011,4(3):323-332.
30. Edelman S, Leskelä S, Ron E, Apajalahti J, Korhonen TK: In vitro adhesion of an avian pathogenic Escherichia coli O78 strain to surfaces of the chicken intestinal tract and to ileal mucus. Vet Microbiol 2003,91(1):41-56.
31. Edelman S: Mucosa-Adherent Lactobacilli: Commensal and Pathogenic Characteristics. University of Helsinki: Faculty of Biosciences, Department of Biological and Environmental Sciences, General Microbiology; 2005.
32. Edelman S, Westerlund-Wikström B, Leskelä S, Kettunen H, Rautonen N, Apajalahti J, Korhonen TK: In vitro adhesion specificity of indigenous Lactobacilli within the avian intestinal tract. Appl Environ Microbiol 2002,68(10):5155-5159.
33. Edelman SM, Lehti TA, Kainulainen V, Antikainen J, Kylväjä R, Baumann M, Westerlund-Wikström B, Korhonen TK: Identification of a high-molecular-mass Lactobacillus epithelium adhesin (LEA) of Lactobacillus crispatus ST1 that binds to stratified squamous epithelium. Microbiology 2012,158(Pt 7):1713-1722.
34. Kaleta P, O'Callaghan J, Fitzgerald GF, Beresford TP, Ross RP: Crucial role for insertion sequence elements in Lactobacillus helveticus evolution as revealed by interstrain genomic comparison. Appl Environ Microbiol 2010,76(1):212-220.
35. Berger B, Pridmore RD, Barretto C, Delmas-Julien F, Schreiber K, Arigoni F, Brussow H: Similarity and differences in the Lactobacillus acidophilus group identified by polyphasic analysis and comparative genomics. J Bacteriol 2007,189(4):1311-1321.
36. Hao P, Zheng H, Yu Y, Ding G, Gu W, Chen S, Yu Z, Ren S, Oda M, Konno T, Wang S, Li X, Ji ZS, Zhao G: Complete sequencing and pan-genomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One 2011,6(1):e15964.
37. Cremonesi P, Chessa S, Castiglioni B: Genome sequence and analysis of Lactobacillus helveticus. Front Microbiol 2012, 3:435.
38. Smokvina T, Wels M, Polka J, Chervaux C, Brisse S, Boekhorst J, van Hylckama Vlieg JE, Siezen RJ: Lactobacillus paracasei comparative genomics: towards species pan-genome definition and exploitation of diversity. PLoS One 2013,8(7):e68731.
39. Douillard FP, Ribbera A, Kant R, Pietila TE, Jarvinen HM, Messing M, Randazzo CL, Paulin L, Laine P, Ritari J, Caggia C, Lahteinen T, Brouns SJ, Satokari R, von Ossowski I, Reunanen J, Palva A, de Vos WM: Comparative genomic and functional analysis of 100 Lactobacillus rhamnosus strains and their comparison with strain GG. PLoS Genet 2013,9(8):e1003683.
40. Raftis EJ, Salvetti E, Torriani S, Felis GE, O'Toole PW: Genomic diversity of Lactobacillus salivarius. Appl Environ Microbiol 2011,77(3):954-965.
41. Toba T, Virkola R, Westerlund B, Björkman Y, Sillanpää J, Vartio T, Kalkkinen N, Korhonen TK: A Collagen-Binding S-Layer Protein in Lactobacillus crispatus. Appl Environ Microbiol 1995,61(7):2467-2471.
42. Sillanpää J, Martinez B, Antikainen J, Toba T, Kalkkinen N, Tankka S, Lounatmaa K, Keränen J, Hook M, Westerlund-Wikström B, Pouwels PH, Korhonen TK: Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 2000,182(22):6440-6450.
43. Antikainen J, Anton L, Sillanpää J, Korhonen TK: Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly. Mol Microbiol 2002,46(2):381-394.
44. Shipitsyna E, Roos A, Datcu R, Hallen A, Fredlund H, Jensen JS, Engstrand L, Unemo M: Composition of the vaginal microbiota in women of reproductive age-sensitive and specific molecular diagnosis of bacterial vaginosis is possible? PLoS One 2013,8(4):e60670.
45. Fredricks DN, Fiedler TL, Marrazzo JM: Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 2005,353(18):1899-1911.
46. Muzny CA, Schwebke JR: Gardnerella vaginalis: Still a Prime Suspect in the Pathogenesis of Bacterial Vaginosis. Curr Infect Dis Rep 2013,15(2):130-135.
47. Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, Hall RW, Ross FJ, McCoy CO, Bumgarner R, Marrazzo JM, Fredricks DN: Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One 2012,7(6):e37818.
48. Benson DA, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW: GenBank. Nucleic Acids Res 2013,41(Database issue):D36-D42.
49. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, Dalay O, Driscoll T, Hix D, Mane SP, Mao C, Nordberg EK, Scott M, Schulman JR, Snyder EE, Sullivan DE, Wang C, Warren A, Williams KP, Xue T, Yoo HS, Zhang C, Zhang Y, Will R, Kenyon RW, Sobral BW: PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun 2011,79(11):4286-4298.
50. Patterson JL, Stull-Lane A, Girerd PH, Jefferson KK: Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Microbiology 2010,156(Pt 2):392-399.
51. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT: Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 2009,25(16):2071-2073.
52. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997,25(17):3389-3402.
53. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J: ACT: the Artemis Comparison Tool. Bioinformatics 2005,21(16):3422-3423.
54. Zhou F, Xu Y: cBar: a computer program to distinguish plasmid-derived from chromosome-derived sequence fragments in metagenomics data. Bioinformatics 2010,26(16):2051-2052.
55. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003,52(5):696-704.
56. Letunic I, Bork P: Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007,23(1):127-128.
57. Kankainen M, Ojala T, Holm L: BLANNOTATOR: enhanced homology-based function prediction of bacterial proteins. BMC Bioinformatics 2012, 13:33-2105-13-33.
58. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O: The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75-2164-9-75.
59. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M: KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007,35(Web Server issue):W182-5.
60. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA: The COG database: an updated version includes eukaryotes. BMC Bioinformatics 2003, 4:41.
61. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A: The Pfam protein families database. Nucleic Acids Res 2008,36(Database issue):D281-8.
62. Eddy SR: A new generation of homology search tools based on probabilistic inference. Genome Inform 2009,23(1):205-211.
63. van Heel AJ, de Jong A, Montalban-Lopez M, Kok J, Kuipers OP: BAGEL3: Automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res 2013,41(Web Server issue):W448-53.
64. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV: Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011,9(6):467-477.
65. Haft DH, Selengut J, Mongodin EF, Nelson KE: A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 2005,1(6):e60.
66. Langille MG, Brinkman FS: IslandViewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics 2009,25(5):664-665.
67. Lima-Mendez G, Van Helden J, Toussaint A, Leplae R: Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 2008,24(6):863-865.
68. Edgar RC: PILER-CR: fast and accurate identification of CRISPR repeats. BMC Bioinformatics 2007, 8:18.
69. Li L, Stoeckert CJ Jr, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003,13(9):2178-2189.
70. Tettelin H, Riley D, Cattuto C, Medini D: Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 2008,11(5):472-477.
71. Ihaka R, Gentleman R: R: A language for data analysis and graphics. J Comput Graph Stat 1996,5(3):299-314.
72. Yeoman CJ, Yildirim S, Thomas SM, Durkin AS, Torralba M, Sutton G, Buhay CJ, Ding Y, Dugan-Rocha SP, Muzny DM, Qin X, Gibbs RA, Leigh SR, Stumpf R, White BA, Highlander SK, Nelson KE, Wilson BA: Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS One 2010,5(8):e12411.
73. Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
74. Chou CH, Chang WC, Chiu CM, Huang CC, Huang HD: FMM: a web server for metabolic pathway reconstruction and comparative analysis. Nucleic Acids Res 2009,37(Web Server issue):W129-34.
75. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M: The KEGG resource for deciphering the genome. Nucleic Acids Res 2004,32(Database issue):D277-80.
76. Karp PD, Riley M, Paley SM, Pellegrini-Toole A: The MetaCyc Database. Nucleic Acids Res 2002,30(1):59-61.
77. Machado A, Almeida C, Salgueiro D, Henriques A, Vaneechoutte M, Haesebrouck F, Vieira MJ, Rodrigues L, Azevedo NF, Cerca N: Fluorescence in situ Hybridization method using Peptide Nucleic Acid probes for rapid detection of Lactobacillus and Gardnerella spp. BMC Microbiol 2013, 13:82-2180-13-82.
78. Siezen RJ, van Hylckama Vlieg JE: Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact 2011,10(Suppl 1):S3-2859-10-S1-S3. Epub 2011 Aug 30
79. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R: The microbial pan-genome. Curr Opin Genet Dev 2005,15(6):589-594.
80. Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ: Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways. BMC Genomics 2012, 13:373-2164-13-373.
81. van Tonder AJ, Mistry S, Bray JE, Hill DM, Cody AJ, Farmer CL, Klugman KP, von Gottberg A, Bentley SD, Parkhill J, Jolley KA, Maiden MC, Brueggemann AB: Defining the estimated core genome of bacterial populations using a Bayesian decision model. PLoS Comput Biol 2014,10(8):e1003788.
82. Broadbent JR, Neeno-Eckwall EC, Stahl B, Tandee K, Cai H, Morovic W, Horvath P, Heidenreich J, Perna NT, Barrangou R, Steele JL: Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genomics 2012, 13:533-2164-13-533.
83. Lawrence JG: Gene transfer, speciation, and the evolution of bacterial genomes. Curr Opin Microbiol 1999,2(5):519-523.
84. Altermann E, Russell WM, Azcarate-Peril MA, Barrangou R, Buck BL, McAuliffe O, Souther N, Dobson A, Duong T, Callanan M, Lick S, Hamrick A, Cano R, Klaenhammer TR: Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci U S A 2005,102(11):3906-3912.
85. Damelin LH, Paximadis M, Mavri-Damelin D, Birkhead M, Lewis DA, Tiemessen CT: Identification of predominant culturable vaginal Lactobacillus species and associated bacteriophages from women with and without vaginal discharge syndrome in South Africa. J Med Microbiol 2011,60(Pt 2):180-183.
86. Kiliç AO, Pavlova SI, Alpay S, Kiliç SS, Tao L: Comparative study of vaginal Lactobacillus phages isolated from women in the United States and Turkey: prevalence, morphology, host range, and DNA homology. Clin Diagn Lab Immunol 2001,8(1):31-39.
87. Pavlova SI, Kiliç AO, Mou SM, Tao L: Phage infection in vaginal lactobacilli: an in vitro study. Infect Dis Obstet Gynecol 1997,5(1):36-44.
88. Barrangou R, Horvath P: CRISPR: new horizons in phage resistance and strain identification. Annu Rev Food Sci Technol 2012, 3:143-162.
89. Deveau H, Garneau JE, Moineau S: CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 2010, 64:475-493.
90. Horvath P, Coute-Monvoisin AC, Romero DA, Boyaval P, Fremaux C, Barrangou R: Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 2009,131(1):62-70.
91. Rho M, Wu YW, Tang H, Doak TG, Ye Y: Diverse CRISPRs evolving in human microbiomes. PLoS Genet 2012,8(6):e1002441.
92. Hammes WP, Vogel RF: The genus Lactobacillus . In The genera of lactic acid bacteria. Edited by: Wood BJB, Holzapfel WH. Glasgow: Blackie Academic & Professional; 1995:19-54.
93. Rajan N, Cao Q, Anderson BE, Pruden DL, Sensibar J, Duncan JL, Schaeffer AJ: Roles of Glycoproteins and Oligosaccharides Found in Human Vaginal Fluid in Bacterial Adherence. Infect Immun 1999,67(10):5027-5032.
94. Callanan M, Kaleta P, O'Callaghan J, O'Sullivan O, Jordan K, McAuliffe O, Sangrador-Vegas A, Slattery L, Fitzgerald GF, Beresford T, Ross RP: Genome sequence of Lactobacillus helveticus, an organism distinguished by selective gene loss and insertion sequence element expansion. J Bacteriol 2008,190(2):727-735.
95. Pridmore RD, Berger B, Desiere F, Vilanova D, Barretto C, Pittet AC, Zwahlen MC, Rouvet M, Altermann E, Barrangou R, Mollet B, Mercenier A, Klaenhammer T, Arigoni F, Schell MA: The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci U S A 2004,101(8):2512-2517.
96. Boris S, Barbés C: Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect 2000,2(5):543-546.
97. McMillan A, Macklaim JM, Burton JP, Reid G: Adhesion of Lactobacillus iners AB-1 to Human fibronectin: a key mediator for persistence in the vagina? Reprod Sci 2013,20(7):791-796.
98. Sun Z, Kong J, Hu S, Kong W, Lu W, Liu W: Characterization of a S-layer protein from Lactobacillus crispatus K313 and the domains responsible for binding to cell wall and adherence to collagen. Appl Microbiol Biotechnol 2013,97(5):1941-1952.
99. Hynönen U, Westerlund-Wikström B, Palva A, Korhonen TK: Identification by flagellum display of an epithelial cell- and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis. J Bacteriol 2002,184(12):3360-3367.
100. O'Hanlon DE, Moench TR, Cone RA: In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 2011, 11:200-2334-11-200.
101. Poirel L, Decousser JW, Nordmann P: Insertion sequence ISEcp1B is involved in expression and mobilization of a bla(CTX-M) beta-lactamase gene. Antimicrob Agents Chemother 2003,47(9):2938-2945.
102. Antonio MA, Hawes SE, Hillier SL: The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 1999,180(6):1950-1956.
103. Nilsen T, Nes IF, Holo H: Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl Environ Microbiol 2003,69(5):2975-2984.
104. Joerger MC, Klaenhammer TR: Cloning, expression, and nucleotide sequence of the Lactobacillus helveticus 481 gene encoding the bacteriocin helveticin J. J Bacteriol 1990,172(11):6339-6347.
105. Diep DB, Godager L, Brede D, Nes IF: Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiology 2006,152(Pt 6):1649-1659.
106. Busarcevic M, Dalgalarrondo M: Purification and genetic characterisation of the novel bacteriocin LS2 produced by the human oral strain Lactobacillus salivarius BGHO1. Int J Antimicrob Agents 2012,40(2):127-134.
107. Koumans EH, Sternberg M, Bruce C, McQuillan G, Kendrick J, Sutton M, Markowitz LE: The prevalence of bacterial vaginosis in the United States, 2001-2004; associations with symptoms, sexual behaviors, and reproductive health. Sex Transm Dis 2007,34(11):864-869.
108. Marrazzo JM, Thomas KK, Fiedler TL, Ringwood K, Fredricks DN: Relationship of specific vaginal bacteria and bacterial vaginosis treatment failure in women who have sex with women. Ann Intern Med 2008,149(1):20-28.
109. Chavagnat F, Haueter M, Jimeno J, Casey MG: Comparison of partial tuf gene sequences for the identification of lactobacilli. FEMS Microbiol Lett 2002,217(2):177-183.
110. Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrene Y, Vanderleyden J, De Keersmaecker SC: Identification of a Gene Cluster for the Biosynthesis of a Long, Galactose-Rich Exopolysaccharide in Lactobacillus rhamnosus GG and Functional Analysis of the Priming Glycosyltransferase. Appl Environ Microbiol 2009,75(11):3554-3563.
111. Denou E, Pridmore RD, Berger B, Panoff JM, Arigoni F, Brussow H: Identification of genes associated with the long-gut-persistence phenotype of the probiotic Lactobacillus johnsonii strain NCC533 using a combination of genomics and transcriptome analysis. J Bacteriol 2008,190(9):3161-3168.
112. Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA: Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 1999,67(10):5170-5175.
113. Boskey ER, Cone RA, Whaley KJ, Moench TR: Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod 2001,16(9):1809-1813.
114. Patterson JL, Girerd PH, Karjane NW, Jefferson KK: Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Am J Obstet Gynecol 2007, 197:170.e1-170.e7.
115. Swidsinski A, Mendling W, Loening-Baucke V, Ladhoff A, Swidsinski S, Hale LP, Lochs H: Adherent biofilms in bacterial vaginosis. Obstet Gynecol 2005,106(5 Pt 1):1013-1023.