Enterococcus faecalispCF10-encoded surface proteins PrgA, PrgB (aggregation substance) and PrgC contribute to plasmid transfer, biofilm formation and virulence

Molecular Microbiology

Volumn 95, Issue 4, 2015, Pages 660-677

  Bhatty, Minny ^a   Cruz, Melissa R ^a   Frank, Kristi L ^b   Laverde Gomez, Jenny A ^a   Andrade, Fernando ^a   Garsin, Danielle A ^a   Dunny, Gary M ^b   Kaplan, Heidi B ^a   Christie, Peter J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; EXTRACELLULAR DNA; MEMBRANE PROTEIN; PHEROMONE; PROTEIN PRGA; PROTEIN PRGB; PROTEIN PRGC; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BIOFILM; CAENORHABDITIS ELEGANS; CELL AGGREGATION; CONTROLLED STUDY; ENTEROCOCCAL INFECTION; ENTEROCOCCUS FAECALIS; GENE CLUSTER; GENE DELETION; GENE FREQUENCY; GENE FUNCTION; MUTATIONAL ANALYSIS; NONHUMAN; PLASMID; PRGA GENE; PRGB GENE; PRGC GENE; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; BACTERIUM CONJUGATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

CAENORHABDITIS ELEGANS; ENTEROCOCCUS; MAMMALIA;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CAENORHABDITIS ELEGANS; CONJUGATION, GENETIC; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; PLASMIDS; PROMOTER REGIONS, GENETIC; SEQUENCE DELETION; TRANSCRIPTION, GENETIC; VIRULENCE; VIRULENCE FACTORS;

EID: 84922567810     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12893     Document Type: Article

References (57)

1. Alvarez-Martinez, C.E., and Christie, P.J. (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
2. Banin, R., Brady, K.M., and Greenberg, E.P. (2006) Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 72: 2064-2069.
3. Barnes, A.M., Ballering, K.S., Leibman, R.S., Wells, C.L., and Dunny, G.M. (2012) Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. MBio 3: e00193-12. doi: 10.1128/mBio.00193-12.
4. Bhatty, M., Laverde Gomez, J.A., and Christie, P.J. (2013) The expanding bacterial type IV secretion lexicon. Res Microbiol 164: 620-639.
5. Cavaliere, R., Ball, J.L., Turnbull, L., and Whitchurch, C.B. (2014) The biofilm matrix destabilizers, EDTA and DNaseI, enhance the susceptibility of nontypeable Hemophilus influenzae biofilms to treatment with ampicillin and ciprofloxacin. Microbiologyopen 3: 557-5676.
6. Chang, C., Huang, I.H., Hendrickx, A.P., and Ton-That, H. (2013) Visualization of Gram-positive bacterial pili. Methods Mol Biol 966: 77-95.
7. Chatterjee, A., Cook, L.C., Shu, C.C., Chen, Y., Manias, D.A., Ramkrishna, D., etal. (2013) Antagonistic self-sensing and mate-sensing signaling controls antibiotic-resistance transfer. Proc Natl Acad Sci USA 110: 7086-7090.
8. Chen, Y., Staddon, J.H., and Dunny, G.M. (2007) Specificity determinants of conjugative DNA processing in the Enterococcus faecalis plasmid pCF10 and the Lactococcus lactis plasmid pRS01. Mol Microbiol 63: 1549-1564.
9. Chen, Y., Zhang, X., Manias, D., Yeo, H.J., Dunny, G.M., and Christie, P.J. (2008) Enterococcus faecalis PcfC, a spatially localized substrate receptor for type IV secretion of the pCF10 transfer intermediate. J Bacteriol 190: 3632-3645.
10. Christie, P.J., and Dunny, G.M. (1986) Identification of regions of the Streptococcus faecalis plasmid pCF-10 that encode antibiotic resistance and pheromone response functions. Plasmid 15: 230-241.
11. Christie, P.J., Kao, S.M., Adsit, J.C., and Dunny, G.M. (1988) Cloning and expression of genes encoding pheromone-inducible antigens of Enterococcus (Streptococcus) faecalis. J Bacteriol 170: 5161-5168.
12. Chuang, O.N., Schlievert, P.M., Wells, C.L., Manias, D.A., Tripp, T.J., and Dunny, G.M. (2009) Multiple functional domains of Enterococcus faecalis aggregation substance Asc10 contribute to endocarditis virulence. Infect Immun 77: 539-548.
13. Chuang-Smith, O.N., Wells, C.L., Henry-Stanley, M.J., and Dunny, G.M. (2010) Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS ONE 5: e15798. doi: 10.1371/journal.pone.0015798.
14. Cook, L.C., and Dunny, G.M. (2013) Effects of biofilm growth on plasmid copy number and expression of antibiotic resistance genes in Enterococcus faecalis. Antimicrob Agents Chemother 57: 1850-1856.
15. Cook, L.C., Chatterjee, A., Barnes, A., Yarwood, J., Hu, W.-S., and Dunny, G.M. (2011) Biofilm growth alters regulation of conjugation by a bacterial pheromone. Mol Microbiol 81: 1499-1510.
16. Das, T., Sehar, S., Koop, L., Wong, Y.K., Ahmed, S., Siddiqui, K.S., and Manefield, M. (2014) Influence of calcium in extracellular DNA mediated bacterial aggregation and biofilm formation. PLoS ONE 9: e91935. doi: 10.1371/journal.pone.0091935.
17. Dunny, G., Funk, C., and Adsit, J. (1981) Direct stimulation of the transfer of antibiotic resistance by sex pheromones in Streptococcus faecalis. Plasmid 6: 270-278.
18. Dunny, G.M. (2013) Enterococcal sex pheromones: signaling, social behavior, and evolution. Annu Rev Genet 47: 457-482.
19. Dunny, G.M., and Clewell, D.B. (1975) Transmissible toxin (hemolysin) plasmid in Streptococcus faecalis and its mobilization of a noninfectious drug resistance plasmid. J Bacteriol 124: 784-790.
20. Dunny, G.M., Brown, B.L., and Clewell, D.B. (1978) Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc Natl Acad Sci USA 75: 3479-3483.
21. Dunny, G.M., Zimmerman, D.L., and Tortorello, M.L. (1985) Induction of surface exclusion (entry exclusion) by Streptococcus faecalis sex pheromones: use of monoclonal antibodies to identify an inducible surface antigen involved in the exclusion process. Proc Natl Acad Sci USA 82: 8582-8586.
22. Dunny, G.M., Lee, L.N., and LeBlanc, D.J. (1991) Improved electroporation and cloning vector system for Gram-positive bacteria. Appl Environ Microbiol 57: 1194-1201.
23. Dunny, G.M., Hancock, L.E., and Shankar, N. (2014) Enterococcal biofilm structure and role in colonization and disease. In Enterococci: From Commensals to Leading Causes of Drug Resistant Infection [Internet]. Gilmore, M.S., Clewell, D.B., Ike, Y., and Shankar, N. (eds). Boston: Massachusetts Eye and Ear Infirmary. URL http://www.ncbi.nlm.nih.gov/books/NBK190433/
24. Flemming, H.C., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
25. Frank, K.L., Barnes, A.M., Grindle, S.M., Manias, D.A., Schlievert, P.M., and Dunny, G.M. (2012) Use of recombinase-based in vivo expression technology to characterize Enterococcus faecalis gene expression during infection identifies in vivo-expressed antisense RNAs and implicates the protease Eep in pathogenesis. Infect Immun 80: 539-549.
26. Garsin, D.A., Sifri, C.D., Mylonakis, E., Qin, X., Singh, K.V., Murray, B.E., etal. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci USA 98: 10892-10897.
27. Garsin, D.A., Frank, K.L., Silanpaa, J., Ausubel, F.M., Hartke, A., Shankar, N., and Murray, B.E. (2014) Pathogenesis and models of enterococcal infection. In Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Gilmore, M.S., Clewell, D.B., Ike, Y., and Shankar, N. (eds). Boston: Massachusetts Eye and Ear Infirmary. URL http://www.ncbi.nlm.nih.gov/books/NBK190424/6/
28. Hirt, H., Erlandsen, S.L., and Dunny, G.M. (2000) Heterologous inducible expression of Enterococcus faecalis pCF10 aggregation substance Asc10 in Lactococcus lactis and Streptococcus gordonii contributes to cell hydrophobicity and adhesion to fibrin. J Bacteriol 182: 2299-2306.
29. Hirt, H., Manias, D.A., Bryan, E.M., Klein, J.R., Marklund, J.K., Staddon, J.H., etal. (2005) Characterization of the pheromone response of the Enterococcus faecalis conjugative plasmid pCF10: complete sequence and comparative analysis of the transcriptional and phenotypic responses of pCF10-containing cells to pheromone induction. J Bacteriol 187: 1044-1054.
30. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
31. Kristich, C.J., Chandler, J.R., and Dunny, G.M. (2007) Development of a host-genotype-independent counterselectable marker and a high-frequency conjugative delivery system and their use in genetic analysis of Enterococcus faecalis. Plasmid 57: 131-144.
32. Leenhouts, K., Buist, G., Bolhuis, A., ten Berge, A., Kiel, J., Mierau, I., etal. (1996) A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol Gen Genet 253: 217-224.
33. Li, F., Alvarez-Martinez, C., Chen, Y., Choi, K.J., Yeo, H.J., and Christie, P.J. (2012) Enterococcus faecalis PrgJ, a VirB4-like ATPase, mediates pCF10 conjugative transfer through substrate binding. J Bacteriol 194: 4041-4051.
34. Liu, H.H., Yang, Y.R., Shen, X.C., Zhang, Z.L., Shen, P., and Xie, Z.X. (2008) Role of DNA in bacterial aggregation. Curr Microbiol 57: 139-144.
35. Lovdok, L., Bentele, K., Vladimirov, N., Muller, A., Pop, F.S., Lebiedz, D., etal. (2009) Role of translational coupling in robustness of bacterial chemotaxis pathway. PLoS Biol 7: e1000171. doi: 10.1371/journal.pbio.1000171.
36. Manson, J.M., Hancock, L.E., and Gilmore, M.S. (2010) Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits. Proc Natl Acad Sci USA 107: 12269-12274.
37. Mohamed, J.A., Huang, W., Nallapareddy, S.R., Teng, F., and Murray, B.E. (2004) Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect Immun 72: 3658-3663.
38. Navarre, W.W., and Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
39. Oli, M.W., Otoo, H.N., Crowley, P.J., Heim, K.P., Nascimento, M.M., Ramsook, C.B., etal. (2012) Functional amyloid formation by Streptococcus mutans. Microbiology 158: 2903-2916.
40. Olmsted, S.B., Kao, S.M., van Putte, L.J., Gallo, J.C., and Dunny, G.M. (1991) Role of the pheromone-inducible surface protein Asc10 in mating aggregate formation and conjugal transfer of the Enterococcus faecalis plasmid pCF10. J Bacteriol 173: 7665-7672.
41. Olmsted, S.B., Erlandsen, S.L., Dunny, G.M., and Wells, C.L. (1993) High-resolution visualization by field emission scanning electron microscopy of Enterococcus faecalis surface proteins encoded by the pheromone-inducible conjugative plasmid pCF10. J Bacteriol 175: 6229-6237.
42. O'Toole, G.A., and Kolter, R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449-461.
43. Qin, X., Singh, K.V., Weinstock, G.M., and Murray, B.E. (2001) Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J Bacteriol 183: 3372-3382.
44. Rakita, R.M., Vanek, N.N., Jacques-Palaz, K., Mee, M., Mariscalco, M.M., Dunny, G.M., etal. (1999) Enterococcus faecalis bearing aggregation substance is resistant to killing by human neutrophils despite phagocytosis and neutrophil activation. Infect Immun 67: 6067-6075.
45. Rice, K.C., Mann, E.E., Endres, J.L., Weiss, E.C., Cassat, J.E., Smeltzer, M.S., and Bayles, K.W. (2007) The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc Natl Acad Sci USA 104: 8113-8118.
46. Schlievert, P.M., Gahr, P.J., Assimacopoulos, A.P., Dinges, M.M., Stoehr, J.A., Harmala, J.W., etal. (1998) Aggregation and binding substances enhance pathogenicity in rabbit models of Enterococcus faecalis endocarditis. Infect Immun 66: 218-223.
47. Schlievert, P.M., Chuang-Smith, O.N., Peterson, M.L., Cook, L.C., and Dunny, G.M. (2010) Enterococcus faecalis endocarditis severity in rabbits is reduced by IgG Fabs interfering with aggregation substance. PLoS ONE 5: e13194. doi: 10.1371/journal.pone.0013194.
48. Sifri, C.D., Mylonakis, E., Singh, K.V., Qin, X., Garsin, D.A., Murray, B.E., etal. (2002) Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70: 5647-5650.
49. Singh, K.V., Nallapareddy, S.R., Sillanpaa, J., and Murray, B.E. (2010) Importance of the collagen adhesin Ace in pathogenesis and protection against Enterococcus faecalis experimental endocarditis. PLoS Pathog 6: e1000716. doi: 10.1371/journal.ppat.1000716.
50. Staddon, J.H., Bryan, E.M., Manias, D.A., Chen, Y., and Dunny, G.M. (2006) Genetic characterization of the conjugative DNA processing system of enterococcal plasmid pCF10. Plasmid 56: 102-111.
51. Sussmuth, S.D., Muscholl-Silberhorn, A., Wirth, R., Susa, M., Marre, R., and Rozdzinski, E. (2000) Aggregation substance promotes adherence, phagocytosis, and intracellular survival of Enterococcus faecalis within human macrophages and suppresses respiratory burst. Infect Immun 68: 4900-4906.
52. Thomas, V.C., Thurlow, L.R., Boyle, D., and Hancock, L.E. (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190: 5690-5698.
53. Tribble, G.D., Rigney, T.W., Dao, D.H., Wong, C.T., Kerr, J.E., Taylor, B.E., etal. (2012) Natural competence is a major mechanism for horizontal DNA transfer in the oral pathogen Porphyromonas gingivalis. MBio 3: e00231-11. doi: 10.1128/mBio.00231-11.
54. Wastfelt, M., Stalhammar-Carlemalm, M., Delisse, A.M., Cabezon, T., and Lindahl, G. (1996) Identification of a family of streptococcal surface proteins with extremely repetitive structure. J Biol Chem 271: 18892-18897.
55. Waters, C.M., and Dunny, G.M. (2001) Analysis of functional domains of the Enterococcus faecalis pheromone-induced surface protein aggregation substance. J Bacteriol 183: 5659-5667.
56. Waters, C.M., Hirt, H., McCormick, J.K., Schlievert, P.M., Wells, C.L., and Dunny, G.M. (2004) An amino-terminal domain of Enterococcus faecalis aggregation substance is required for aggregation, bacterial internalization by epithelial cells and binding to lipoteichoic acid. Mol Microbiol 52: 1159-1171.
57. Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., and Mattick, J.S. (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.