Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions

FEMS Microbiology Letters

Volumn 357, Issue 1, 2014, Pages 23-33

  Turroni, Francesca ^a   Serafini, Fausta ^b   Mangifesta, Marta ^c   Arioli, Stefania ^d   Mora, Diego ^d   van Sinderen, Douwe ^a   Ventura, Marco ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY OF PARMA   (Italy)

^c Italy   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

Bifidobacteria; Genomics; Host microorganism interaction; Microorganism microorganism interaction

Indexed keywords

PILIN; SORTASE; BACTERIAL PROTEIN;

ACIDITY; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM PILUS; BIFIDOBACTERIUM; BIFIDOBACTERIUM ADOLESCENTIS; BIFIDOBACTERIUM ANGULATUM; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BIFIDUM PRL2010; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM CATENULATUM; BIFIDOBACTERIUM GALLICUM; BIFIDOBACTERIUM KASHIWANOHENSE; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM PSEUDOLONGUM; CELL AGGREGATION; COCULTURE; COMMENSALISM; CONTROLLED STUDY; FIMA GENE; FIMP GENE; FLOW CYTOMETRY; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; INTESTINE FLORA; LACTOBACILLUS PARACASEI; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; OSMOTIC STRESS; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TEMPERATURE STRESS; BACTERIAL GENOME; ENVIRONMENT; FIMBRIA; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM BIFIDUM;

BACTERIAL PROTEINS; BIFIDOBACTERIUM; ENVIRONMENT; FIMBRIAE, BACTERIAL; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS;

EID: 84905575478     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12509     Document Type: Article

References (39)

1. Bottacini F, O'Connell Motherway M, Kuczynski J et al. (2014) Comparative genomics of the Bifidobacterium breve taxon. BMC Genomics 15: 170.
2. Chenoll E, Casinos B, Bataller E et al. (2011) Novel probiotic Bifidobacterium bifidum CECT 7366 strain active against the pathogenic bacterium Helicobacter pylori. Appl Environ Microbiol 77: 1335-1343.
3. Collins MD, Phillips BA & Zanoni P (1989) Deoxyribonucleic-acid homology studies of Lactobacillus-casei, Lactobacillus-paracasei sp-nov, subsp. paracasei and subsp. tolerans, and Lactobacillus-rhamnosus sp-nov, comb-nov. Int J Syst Bacteriol 39: 105-108.
4. Cronin UP & Wilkinson MG (2010) The potential of flow cytometry in the study of Bacillus cereus. J Appl Microbiol 108: 1-16.
5. Danne C & Dramsi S (2012) Pili of gram-positive bacteria: roles in host colonization. Res Microbiol 163: 645-658.
6. Del Re B, Sgorbati B, Miglioli M & Palenzona D (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31: 438-442.
7. Foroni E, Serafini F, Amidani D et al. (2011) Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb Cell Fact 10(Suppl 1): S16.
8. Gunasekera TS, Veal DA & Attfield PV (2003) Potential for broad applications of flow cytometry and fluorescence techniques in microbiological and somatic cell analyses of milk. Int J Food Microbiol 85: 269-279.
9. Handley PS, Harty DW, Wyatt JE, Brown CR, Doran JP & Gibbs AC (1987) A comparison of the adhesion, coaggregation and cell-surface hydrophobicity properties of fibrillar and fimbriate strains of Streptococcus salivarius. J Gen Microbiol 133: 3207-3217.
10. Hendrickx APA, Bonten MJM, van Luit-Asbroek M, Schapendonk CME, Kragten AHM & Willems RJL (2008) Expression of two distinct types of pili by a hospital-acquired Enterococcus faecium isolate. Microbiology 154: 3212-3223.
11. Hidalgo-Cantabrana C, Sanchez B, Milani C, Ventura M, Margolles A & Ruas-Madiedo P (2014) Genomic overview and biological functions of exopolysaccharide biosynthesis in Bifidobacterium spp. Appl Environ Microbiol 80: 9-18.
12. Jiang SM, Park SE, Yadav P, Paoletti LC & Wessels MR (2012) Regulation and function of pilus island 1 in group B Streptococcus. J Bacteriol 194: 2479-2490.
13. 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.
14. Milani C, Duranti S, Lugli GA et al. (2013) Comparative genomics of Bifidobacterium animalis subsp. lactis reveals a strict monophyletic bifidobacterial taxon. Appl Environ Microbiol 79: 4304-4315.
15. Mishra A, Wu CG, Yang JH, Cisar JO, Das A & Ton-That H (2010) The Actinomyces oris type 2 fimbrial shaft FimA mediates co-aggregation with oral streptococci, adherence to red blood cells and biofilm development. Mol Microbiol 77: 841-854.
16. Miyake T, Watanabe K, Watanabe T & Oyaizu H (1998) Phylogenetic analysis of the genus Bifidobacterium and related genera based on 16S rDNA sequences. Microbiol Immunol 42: 661-667.
17. Morita H, Nakano A, Onoda H et al. (2011) Bifidobacterium kashiwanohense sp. nov., isolated from healthy infant faeces. Int J Syst Evol Microbiol 61: 2610-2615.
18. Motherway MO, Zomer A, Leahy SC et al. (2011) Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. P Natl Acad Sci USA 108: 11217-11222.
19. Nakata M, Koeller T, Moritz K et al. (2009) Mode of expression and functional characterization of FCT-3 pilus region-encoded proteins in Streptococcus pyogenes serotype M49. Infect Immun 77: 32-44.
20. Okahashi N, Nakata M, Terao Y et al. (2011) Pili of oral Streptococcus sanguinis bind to salivary amylase and promote the biofilm formation. Microb Pathog 50: 148-154.
21. Pokusaeva K, Fitzgerald GF & van Sinderen D (2011) Carbohydrate metabolism in Bifidobacteria. Genes Nutr 6: 285-306.
22. Scardovi V & Crociani F (1974) Bifidobacterium-catenulatum, Bifidobacterium-dentium, and Bifidobacterium-angulatum - 3 new species and their deoxyribonucleic-acid homology relationships. Int J Syst Bacteriol 24: 6-20.
23. Schell MA, Karmirantzou M, Snel B et al. (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. P Natl Acad Sci USA 99: 14422-14427.
24. Schiller LR (2012) Definitions, pathophysiology, and evaluation of chronic diarrhoea. Best Pract Res Clin Gastroenterol 26: 551-562.
25. Sela DA, Chapman J, Adeuya A et al. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. P Natl Acad Sci USA 105: 18964-18969.
26. Serafini F, Strati F, Ruas-Madiedo P et al. (2013) Evaluation of adhesion properties and antibacterial activities of the infant gut commensal Bifidobacterium bifidum PRL2010. Anaerobe 21: 9-17.
27. Sincock SA & Robinson JP (2001) Flow cytometric analysis of microorganisms. Methods Cell Biol 64: 511-537.
28. Sonnenburg JL, Chen CTL & Gordon JI (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4: 2213-2226.
29. Ton-That H & Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50: 1429-1438.
30. Turroni F, Bottacini F, Foroni E et al. (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. P Natl Acad Sci USA 107: 19514-19519.
31. Turroni F, Foroni E, Montanini B et al. (2011a) Global genome transcription profiling of Bifidobacterium bifidum PRL2010 under in vitro conditions and identification of reference genes for quantitative real-time PCR. Appl Environ Microbiol 77: 8578-8587.
32. Turroni F, Foroni E, Serafini F et al. (2011b) Ability of Bifidobacterium breve to grow on different types of milk: exploring the metabolism of milk through genome analysis. Appl Environ Microbiol 77: 7408-7417.
33. Turroni F, Peano C, Pass DA et al. (2012) Diversity of bifidobacteria within the infant gut microbiota. PLoS ONE 7: e36957.
34. Turroni F, Serafini F, Foroni E et al. (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. P Natl Acad Sci USA 110: 11151-11156.
35. Ventura M, Canchaya C, van Sinderen D, Fitzgerald GF & Zink R (2004a) Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Appl Environ Microbiol 70: 3110-3121.
36. Ventura M, Canchaya C, Zink R, Fitzgerald GF & van Sinderen D (2004b) Characterization of the groEL and groES loci in Bifidobacterium breve UCC 2003: genetic, transcriptional, and phylogenetic analyses. Appl Environ Microbiol 70: 6197-6209.
37. Ventura M, Canchaya C, Zhang ZD, Bernini V, Fitzgerald GF & van Sinderen D (2006) How high G + C gram-positive bacteria and in particular bifidobacteria cope with heat stress: protein players and regulators. FEMS Microbiol Rev 30: 734-759.
38. Ventura M, Turroni F, Motherway MO, MacSharry J & van Sinderen D (2012) Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends Microbiol 20: 467-476.
39. Yeung MK & Ragsdale PA (1997) Synthesis and function of Actinomyces naeslundii T14V type 1 fimbriae require the expression of additional fimbria-associated genes. Infect Immun 65: 2629-2639.