The highly autoaggregative and adhesive phenotype of the vaginal lactobacillus plantarum strain cmpg5300 is sortase dependent

Applied and Environmental Microbiology

Volumn 79, Issue 15, 2013, Pages 4576-4585

  Malik, Shweta ^a,b   Petrova, Mariya I ^a,b   Claes, Ingmar J J ^a,b   Verhoeven, Tine L A ^a   Busschaert, Pieter ^c,d   Vaneechoutte, Mario ^e   Lievens, Bart ^c,d   Lambrichts, Ivo ^f   Siezen, Roland J ^g   Balzarini, Jan ^h   Vanderleyden, Jos ^a   Lebeer, Sarah ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c Associatie KULeuven   (Belgium)

^d Scientia Terrae Research Institute   (Belgium)

^e GHENT UNIVERSITY   (Belgium)

^f HASSELT UNIVERSITY   (Belgium)

^g RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^h REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACES; EPITHELIAL CELLS; GENE DELETION MUTANTS; HOST CELLS; KEY DETERMINANTS; LACTOBACILLUS PLANTARUM; MUTANT ANALYSIS; VAGINAL LACTOBACILLI;

ADHESION; CELL MEMBRANES; GENE ENCODING;

BACILLI;

AMINOACYLTRANSFERASE; BACTERIAL PROTEIN; CYSTEINE PROTEINASE; SORTASE A;

BACTERIUM; BIOFILM; ENZYME ACTIVITY; MOLECULAR ANALYSIS; PHENOTYPE; PROTEIN;

ARTICLE; BACTERIUM ADHERENCE; DNA SEQUENCE; EPITHELIUM CELL; FEMALE; GENE DELETION; GENETICS; HUMAN; LACTOBACILLUS PLANTARUM; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY; SEQUENCE ANALYSIS; VAGINA;

AMINOACYLTRANSFERASES; BACTERIAL ADHESION; BACTERIAL PROTEINS; CLONING, MOLECULAR; CYSTEINE ENDOPEPTIDASES; EPITHELIAL CELLS; FEMALE; GENE DELETION; HUMANS; LACTOBACILLUS PLANTARUM; MOLECULAR SEQUENCE DATA; PHENOTYPE; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; VAGINA;

EID: 84880691804     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00926-13     Document Type: Article

References (62)

1. Bayo M, Berlanga M, Agut M. 2002. Vaginal microbiota in healthy pregnant women and prenatal screening of group B streptococci (GBS). Int. Microbiol. 5:87-90.
2. 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. 2011. Vaginal microbiome of reproductiveage women. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl. 1):4680-4687.
3. Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL. 2003. Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin. Infect. Dis. 36:663-668.
4. Sha BE, Zariffard MR, Wang QJ, Chen HY, Bremer J, Cohen MH, Spear GT. 2005. Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis. J. Infect. Dis. 191:25-32.
5. Reid G, Bruce AW. 2003. Urogenital infections in women: can probiotics help? Postgrad. Med. J. 79:428-432.
6. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2010. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8:171-184.
7. Reid G, Burton J. 2002. Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect. 4:319-324.
8. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72:728-764.
9. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MW, Stiekema W, Lankhorst RM, Bron PA, Hoffer SM, Groot MN, Kerkhoven R, de Vries M, Ursing B, de Vos WM, Siezen RJ. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. U. S. A. 100:1990-1995.
10. 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. 2005. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. U. S. A. 102:3906-3912.
11. Claesson MJ, Li Y, Leahy S, Canchaya C, van Pijkeren JP, Cerdeno-Tarraga AM, Parkhill J, Flynn S, O'Sullivan GC, Collins JK, Higgins D, Shanahan F, Fitzgerald GF, van Sinderen D, O'Toole PW. 2006. Multireplicon genome architecture of Lactobacillus salivarius. Proc. Natl. Acad. Sci. U. S. A. 103:6718-6723.
12. Azcarate-Peril MA, Altermann E, Goh YJ, Tallon R, Sanozky-Dawes RB, Pfeiler EA, O'Flaherty S, Buck B.L, Dobson A, Duong T, Miller MJ, Barrangou R, Klaenhammer TR. 2008. Analysis of the genome sequence of Lactobacillus gasseri ATCC 33323 reveals the molecular basis of an autochthonous intestinal organism. Appl. Environ. Microbiol. 74:4610-4625.
13. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx AP, Lebeer S, De Keersmaecker SC, Vanderleyden J, Hamalainen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjarvi T, Auvinen P, de Vos WM. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. U. S. A. 106:17193-17198.
14. Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G. 2011. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc. Natl. Acad. Sci. U. S. A. 108(Suppl. 1):4688-4695.
15. Anukam K, Macklaim JM, Gloor GB, Reid G, Boekhorst J, Renckens B, van Hijum SA, Siezen RJ. 2013. Genome sequence of Lactobacillus pentosus KCA1: vaginal isolate from a healthy premenopausal woman. PLoS One 8:e59239. doi:10.1371/journal.pone.0059239.
16. Boris S, Suarez JE, Barbes C. 1997. Characterization of the aggregation promoting factor from Lactobacillus gasseri, a vaginal isolate. J. Appl. Microbiol. 83:413-420.
17. Juarez Tomas MS, Wiese B, Nader-Macias ME. 2005. Effects of culture conditions on the growth and auto-aggregation ability of vaginal Lactobacillus johnsonii CRL 1294. J. Appl. Microbiol. 99:1383-1391.
18. Goh YJ, Klaenhammer TR. 2010. Functional roles of aggregationpromoting-like factor in stress tolerance and adherence of Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 76:5005-5012.
19. Kos B, Suskovic J, Vukovic S, Simpraga M, Frece J, Matosic S. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94:981-987.
20. Cesena C, Morelli L, Alander M, Siljander T, Tuomola E, Salminen S, Mattila-Sandholm T, Vilpponen-Salmela T, von Wright A. 2001. Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J. Dairy Sci. 84:1001-1010.
21. Boris S, Suarez JE, Vazquez F, Barbes C. 1998. Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect. Immun. 66:1985-1989.
22. Dieye Y, Oxaran V, Ledue-Clier F, Alkhalaf W, Buist G, Juillard V, Lee CW, Piard JC. 2010. Functionality of sortase A in Lactococcus lactis. Appl. Environ. Microbiol. 76:7332-7337.
23. Lebeer S, Verhoeven TL, Francius G, Schoofs G, Lambrichts I, Dufrene Y, Vanderleyden J, De Keersmaecker SC. 2009. 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. 75:3554-3563.
24. Lebeer S, Verhoeven TL, Perea Velez M, Vanderleyden J, De Keersmaecker SC. 2007. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 73:6768-6775.
25. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16:276-277.
26. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
27. Zhou M, Boekhorst J, Francke C, Siezen RJ. 2008. LocateP: genomescale subcellular-location predictor for bacterial proteins. BMC Bioinformatics 9:173.
28. Boekhorst J, de Been MW, Kleerebezem M, Siezen RJ. 2005. Genomewide detection and analysis of cell wall-bound proteins with LPXTG-like sorting motifs. J. Bacteriol. 187:4928-4934.
29. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8:785-786.
30. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Berthier F, Zagorec M, Champomier-Verge's M, Ehrlich SD, Morel-Deville F. 1996. Efficient transformation of Lactobacillus sake by electroporation. Microbiology 142:1273-1279.
32. Mason CK, Collins MA, Thompson K. 2005. Modified electroporation protocol for lactobacilli isolated from the chicken crop facilitates transformation and the use of a genetic tool. J. Microbiol. Methods 60:353-363.
33. Reference deleted.
34. De Keersmaecker SC, Braeken K, Verhoeven TL, Perea Velez M, Lebeer S, Vanderleyden J, Hols P. 2006. Flow cytometric testing of green fluorescent protein-tagged Lactobacillus rhamnosus GG for response to defensins. Appl. Environ. Microbiol. 72:4923-4930.
35. Josson K, Scheirlinck T, Michiels F, Platteeuw C, Stanssens P, Joos H, Dhaese P, Zabeau M, Mahillon J. 1989. Characterization of a grampositive broad-host-range plasmid isolated from Lactobacillus hilgardii. Plasmid 21:9-20.
36. Lambert JM, Bongers RS, Kleerebezem M. 2007. Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl. Environ. Microbiol. 73:1126-1135.
37. Fichorova RN, Rheinwald JG, Anderson DJ. 1997. Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissuespecific differentiation proteins. Biol. Reprod. 57:847-855.
38. Remus DM, Bongers RS, Meijerink M, Fusetti F, Poolman B, de Vos P, Wells JM, Kleerebezem M, Bron PA. 2013. Impact of Lactobacillus plantarum sortase on target protein sorting, gastrointestinal persistence, and host immune response modulation. J. Bacteriol. 195:502-509.
39. Chang TL, Chang CH, Simpson DA, Xu Q, Martin PK, Lagenaur LA, Schoolnik GK, Ho DD, Hillier SL, Holodniy M, Lewicki JA, Lee PP. 2003. Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4. Proc. Natl. Acad. Sci. U. S. A. 100:11672-11677.
40. Mackenzie DA, Jeffers F, Parker ML, Vibert-Vallet A, Bongaerts RJ, Roos S, Walter J, Juge N. 2010. Strain-specific diversity of mucusbinding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156:3368-3378.
41. Atassi F, Brassart D, Grob P, Graf F, Servin AL. 2006. Lactobacillus strains isolated from the vaginal microbiota of healthy women inhibit Prevotella bivia and Gardnerella vaginalis in coculture and cell culture. FEMS Immunol. Med. Microbiol. 48:424-432.
42. Anukam KC, Osazuwa E, Osemene GI, Ehigiagbe F, Bruce AW, Reid G. 2006. Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect. 8:2772-2776.
43. Pretzer G, Snel J, Molenaar D, Wiersma A, Bron PA, Lambert J, de Vos WM, van der Meer R, Smits MA, Kleerebezem M. 2005. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J. Bacteriol. 187: 6128-6136.
44. Gross G, van der Meulen J, Snel J, van der Meer R, Kleerebezem M, Niewold TA, Hulst MM, Smits MA. 2008. Mannose-specific interaction of Lactobacillus plantarum with porcine jejunal epithelium. FEMS Immunol. Med. Microbiol. 54:215-223.
45. van Pijkeren JP, Canchaya C, Ryan KA, Li Y, Claesson MJ, Sheil B, Steidler L, O'Mahony L, Fitzgerald GF, van Sinderen D, O'Toole PW. 2006. Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl. Environ. Microbiol. 72:4143-4153.
46. Denou E, Pridmore RD, Berger B, PanoffJM, Arigoni F, Brussow H. 2008. 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. 190: 3161-3168.
47. Munoz-Provencio D, Rodriguez-Diaz J, Collado MC, Langella P, Bermudez-Humaran LG, Monedero V. 2012. Functional analysis of the Lactobacillus casei BL23 sortases. Appl. Environ. Microbiol. 78:8684-8693.
48. Jones SE, Versalovic J. 2009. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9:35.
49. Strus M, Kucharska A, Kukla G, Brzychczy-Wloch M, Maresz K, Heczko PB. 2005. The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida. Infect. Dis. Obstet. Gynecol. 13:69-75.
50. Verstraelen H, Swidsinski A. 2013. The biofilm in bacterial vaginosis: implications for epidemiology, diagnosis and treatment. Curr. Opin. Infect. Dis. 26:86-89.
51. Martin R, Soberon N, Vaneechoutte M, Florez AB, Vazquez F, Suarez JE. 2008. Characterization of indigenous vaginal lactobacilli from healthy women as probiotic candidates. Int. Microbiol. 11:261-266.
52. Terraf MC, Juarez Tomas MS, Nader-Macias ME, Silva C. 2012. Screening of biofilm formation by beneficial vaginal lactobacilli and influence of culture media components. J. Appl. Microbiol. 113:1517-1529.
53. Lebeer S, Claes I, Tytgat HL, Verhoeven TL, Marien E, von Ossowski I, Reunanen J, Palva A, Vos WM, Keersmaecker SC, Vanderleyden J. 2012. Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 78:185-193.
54. Levesque CM, Voronejskaia E, Huang YC, Mair RW, Ellen RP, Cvitkovitch DG. 2005. Involvement of sortase anchoring of cell wall proteins in biofilm formation by Streptococcus mutans. Infect. Immun. 73:3773-3777.
55. Konto-Ghiorghi Y, Mairey E, Mallet A, Dumenil G, Caliot E, Trieu-Cuot P, Dramsi S. 2009. Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog. 5:e1000422. doi:10.1371/journal.ppat.1000422.
56. Plyusnin I, Holm L, Kankainen M. 2009. LOCP-locating pilus operons in gram-positive bacteria. Bioinformatics 25:1187-1188.
57. Clancy KW, Melvin JA, McCafferty DG. 2010. Sortase transpeptidases: insights into mechanism, substrate specificity, and inhibition. Biopolymers 94:385-396.
58. Koren O, Knights D, Gonzalez A, Waldron L, Segata N, Knight R, Huttenhower C, Ley RE. 2013. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput. Biol. 9:e1002863. doi:10.1371/journal.pcbi.1002863.
59. Pascual LM, Daniele MB, Ruiz F, Giordano W, Pajaro C, Barberis L. 2008. Lactobacillus rhamnosus L60, a potential probiotic isolated from the human vagina. J. Gen. Appl. Microbiol. 54:141-148.
60. Gustafsson RJ, Ahrne S, Jeppsson B, Benoni C, Olsson C, Stjernquist M, Ohlsson B. 2011. The Lactobacillus flora in vagina and rectum of fertile and postmenopausal healthy Swedish women. BMC Womens Health 11:17.
61. Hummelen R, Changalucha J, Butamanya NL, Cook A, Habbema JD, Reid G. 2010. Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 to prevent or cure bacterial vaginosis among women with HIV. Int. J. Gynaecol. Obstet. 111:245-248.
62. Kohler GA, Assefa S, Reid G. 2012. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect. Dis. Obstet. Gynecol. 2012: 636474. doi:10.1155/2012/636474.