Advertisement

Sex Pheromones and the Plasmid-Encoded Mating Response in Enterococcus faecalis

  • Don B. Clewell

Abstract

Plasmid-related conjugation in gram-positive, nonstreptomycete bacteria was first reported in 1974 by Jacob and Hobbs (38). They identified an R-plasmid (pJH1) and a hemolysin/ bacteriocin plasmid (pJH2) in a clinical isolate of Enterococcus (formerly Streptococcus) faecalis and found both capable of transfer in broth matings (38, 39). Independently, and at about the same time, Tomura et al (67), in Japan, reported on the transferability of a hemolysin/bacteriocin determinant in E. faecalis. Although physical evidence for plasmid involvement was not presented, it is highly likely that this was indeed the case, as the frequency of transfer was quite high (10−2 per donor in broth matings); and subsequent studies showed that the hemolysin/bacteriocin trait exhibited by many E. faecalis strains usually involved a conjugative plasmid (4, 6).

Keywords

Culture Filtrate Enterococcus Faecalis Plasmid Transfer Aggregation Substance Conjugative Plasmid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Brock, T.D., and Davie, J.M., 1963, Probable identity of group D hemolysin with bacteriocin, J. Bacteriol. 86: 708–712.PubMedGoogle Scholar
  2. 2.
    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.PubMedCrossRefGoogle Scholar
  3. 3.
    Christie, P.J., Kao, 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: 5156–5168.Google Scholar
  4. 4.
    Clewell, D.B., 1981, Plasmids, drug resistance, and gene transfer in the genus Streptococcus, Microbiol. Rev. 45: 409–436.PubMedGoogle Scholar
  5. 5.
    Clewell, D.B., 1985, Sex pheromones, plasmids, and conjugation in Streptococcus faecalis, in: The Origin and Evolution of Sex (H.O. Halvorson and A. Monroy, eds.), MBL lecture Series in Biology, Vol. 7, Alan R. Liss, New York, pp. 13–28.Google Scholar
  6. 6.
    Clewell, D.B., 1990, Movable genetic elements and antibiotic resistance in enterococci, Europ. J. Clinic. Microbiol. Infect. Dis. 9: 90–102.CrossRefGoogle Scholar
  7. 7.
    Clewell, D.B., and Brown, B.L., 1980, Sex pheromone cAD1 in Streptococcus faecalis: induction of a function related to plasmid transfer, J. Bacteriol. 143: 1063–1065.PubMedGoogle Scholar
  8. 8.
    Clewell, D.B., and Weaver, K.E., 1989, Sex pheromones and plasmid transfer in Enterococcus faecalis (a review), Plasmid 21: 175–184.PubMedCrossRefGoogle Scholar
  9. 9.
    Clewell, D.B., Tomich, P.K., Gawron-Burke, M.C., Franke, A.E., Yagi, Y., and An, F.Y., 1982, Mapping of Streptococcus faecalis plasmids pAD1 and pAD2 and studies relating to transposition of Tn917, J. Bacteriol. 152: 1220–1230.PubMedGoogle Scholar
  10. 10.
    Clewell, D.B., Yagi, Y., Ike, Y., Craig, R.A., Brown, B.L., and An, F., 1982, Sex pheromones in Streptococcus faecalis: multiple pheromone systems in strain DS5, similarities of pAD1 and pAMyl, and mutants of pAD1 altered in conjugative properties, in: Microbiology-1982 ( D. Schlessinger, ed.), American Society for Microbiology, Washington, DC, pp. 97–100.Google Scholar
  11. 11.
    Clewell, D.B., An, F.Y., White, B.A., and Gawron-Burke, C., 1985, Streptococcus faecalis sex pheromone (cAM373) also produced by Staphylococcus aureus and identification of a conjugative transposon (Tn918), J. Bacteriol. 162: 1212–1220.Google Scholar
  12. 12.
    Clewell, D.B., Ehrenfeld, E.E., Kessler, R.E., Ike, Y., Franke, A.E., Madion, M., Shaw, J.H., Wirth, R., An, F., Mori, M., Kitada, C., Fujino, M., and Suzuki, A., 1986, Sex-pheromone systems in Streptococcus faecalis, in: Banbury Report 24: Antibiotic Resistance Genes: Ecology, Transfer and Expression, Cold Spring Harbor, Cold Spring Harbor, New York, pp. 131–142.Google Scholar
  13. 13.
    Clewell, D.B., An, F.Y., Mori, M., Ike, Y., and Suzuki, A., 1987, Streptococcus faecalis sex pheromone (cAD1) response: evidence that the peptide inhibitor excreted by pAD1-containing cells may be plasmid determined, Plasmid 17: 65–68.Google Scholar
  14. 14.
    Clewell, D.B., Pontius, L.T., An, FY., Ike, Y., Suzuki, A., and Nakayama, J., 1990, Nucleotide sequence of the sex pheromone inhibitor (iAD1) determinant of Enterococcus faecalis conjugative plasmid pAD1, Plasmid 24: 156–161.PubMedCrossRefGoogle Scholar
  15. 15.
    Clewell, D.B., Pontius, L.T., Weaver, K.E., An, F.Y., Ike, Y., Suzuki, A., and Nakayama, J., 1991, Enterococcus faecalis hemolysin/bacteriocin plasmid pAD1: regulation of the pheromone response, in: Genetics and Molecular Biology of Streptococci, Lactococci, and Enterococci (G. Dunny, P Cleary, and L. McKay, eds.), American Society for Microbiology, Washington, DC, pp. 3–8.Google Scholar
  16. 16.
    Colmar, I., and Horaud, T, 1987, Enterococcus faecalis hemolysin-bacteriocin plasmids belong to the same incompatibility group, Appl. Environ. Microbiol. 53: 567–570.Google Scholar
  17. 17.
    Dunny, G.M., 1990, Genetic functions and cell-cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis, Molec. Microbiol. 4: 689–696.CrossRefGoogle Scholar
  18. 18.
    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.PubMedCrossRefGoogle Scholar
  19. 19.
    Dunny, G.M., Craig, R.A., Carron, R.L., and Clewell, D.B., 1979, Plasmid transfer in Streptococcus faecalis: production of multiple sex pheromones by recipients, Plasmid 2: 454–465.PubMedCrossRefGoogle Scholar
  20. 20.
    Dunny, G.M., Funk, C., and Adsit, J., 1981, Direct stimulation of the transfer of antibiotic resistance by sex pheromones in Streptococcus faecalis, Plasmid 6: 270–278.PubMedCrossRefGoogle Scholar
  21. 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.PubMedCrossRefGoogle Scholar
  22. 22.
    Ehrenfeld, E.E., and Clewell, D.B., 1987, Transfer functions of the Streptococcus faecalis plasmid pAD1: organization of plasmid DNA encoding response to sex pheromone, J. Bacteriol. 169: 3473–3481.PubMedGoogle Scholar
  23. 23.
    Ehrenfeld, E.E., Kessler, R.E., and Clewell, D.B., 1986, Identification of pheromone-induced surface proteins in Streptococcus faecalis and evidence of a role for lipoteichoic acid in formation of mating aggregates, J. Bacteriol. 168: 6–12.PubMedGoogle Scholar
  24. 24.
    Eisenstein, B.1., 1981, Phase variation of type I fimbriae in Escherichia coli is under transcriptional control, Science 214: 337–339.CrossRefGoogle Scholar
  25. 25.
    Ember, J.A., and Hugh, T.E., 1989, Characterization of the human neutrophil response to sex pheromones from Streptococcus faecalis, Am. J. Pathol. 134: 797–805.PubMedGoogle Scholar
  26. 26.
    Galli, D., and Wirth, R., 1991, Comparative analysis of Enterococcus faecalis sex pheromone plasmids identifies a single homologous DNA region which codes for aggregation substance, J. Bacteriol. 173: 30293033.Google Scholar
  27. 27.
    Galli, D., Wirth, R., and Wanner, G., 1989, Identification of aggregation substances of Enterococcus faecalis cells after induction by sex pheromones. An immunological and ultrastructural investigation, Arch. Microbiol. 151: 486–490.PubMedCrossRefGoogle Scholar
  28. 28.
    Galli, D., Lottspeich, F., and Wirth, R., 1990, Sequence analysis of Enterococcus faecalis aggregation substance encoded by the sex pheromone plasmid pAD1, Molec. Microbiol. 4: 895–904.CrossRefGoogle Scholar
  29. 29.
    Handwerger, S., Ricci, M.J., and Kolokathis, A., 1990, Vancomycin resistance is encoded on a pheromone response plasmid in Enterococcus faecium 228, Antimicrob. Ag. Chemother. 34: 358–360.CrossRefGoogle Scholar
  30. 30.
    Hiles, I.D., Higgins, C.F., 1986, Peptide uptake by Salmonella typhimurium. The periplasmic oligopeptidebinding protein Europ. J. Biochem. 158:561–567. Google Scholar
  31. 31.
    Hollingshead, S.K., Fischetti, V.A., and Scott, J.R., 1986, Complete nucleotide sequence of type 6M protein of the group A Streptococcus—repetitive structure and membrane anchor, J. Biol. Chem.. 261: 1677 1686.Google Scholar
  32. 32.
    Ike, Y., and Clewell, D.B., 1984, Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn917 as an insertional mutagen. J. Bacteriol. 158: 777–783.PubMedGoogle Scholar
  33. 33.
    Ike, Y., and Clewell, D.B., 1987, High incidence of hemolysin production by Streptococcus faecalis strains associated with human parenteral infections: structure of hemolysin plasmids, in: Streptococcal Genetics ( J. Ferretti and R. Curtiss III, eds.), American Society for Microbiology, Washington, DC, pp. 159–164.Google Scholar
  34. 34.
    Ike, Y., Craig, R.C., White, B.A., Yagi, Y., and Clewell, D.B., 1983, Modification of Streptococcus faecalis sex pheromones after acquisition of plasmid DNA, Proc. Natl. Acad. Sci. USA 80: 5369–5373.CrossRefGoogle Scholar
  35. 35.
    Ike, Y., Hashimoto, H., and Clewell, D.B., 1984, Hemolysin of Streptococcus faecalis subsp. zymogenes contributes to virulence in mice Infect. Immun. 45:528–530. Google Scholar
  36. 36.
    Ike, Y., Hashimoto, H., and Clewell, D.B., 1987, High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections, J. Clin. Microbiol. 25: 1524 1528.Google Scholar
  37. 37.
    Ike, Y., Clewell, D.B., Segarra, R.A., and Gilmore, M.S., 1990, Genetic analysis of the pAD1 hemolysin/ bacteriocin determinant in Enterococcus faecalis: Tn917 insertional mutagenesis and cloning, J. Bacteriol. 172: 155–163.PubMedGoogle Scholar
  38. 38.
    Jacob, A., and Hobbs, S.J., 1974, Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes, J. Bacteriol. 117: 360–372.PubMedGoogle Scholar
  39. 39.
    Jacob, A., Douglas, G.I., and Hobbs, S.J., 1975, Self-transferable plasmids determining the hemolysin and bacteriocin of Streptococcus faecalis var. zymogenes, J. Bacteriol. 121: 863–872.PubMedGoogle Scholar
  40. 40.
    Kao, S., Olmsted, S.B., Viksnins, A.S., Gallo, J.C., and Dunny, G.M., 1991, Molecular and genetic analysis of a region of the plasmid pCF10 containing positive control genes and structural genes encoding surface proteins involved in pheromone-inducible conjugation in Enterococcus faecalis, J. Bacteriol. 173: 7650–7664.PubMedGoogle Scholar
  41. 41.
    Kashiwagi, K., Yamaguchi, Y., Sakai, Y., Kobayashi, H., and Igarashi, K., 1990, Identification of the polyamine-induced protein as a periplasmic oligopeptide binding protein, J. Biol. Chem. 265: 8387–8391.PubMedGoogle Scholar
  42. 42.
    Kessler, R., and Yagi, Y., 1983, Identification and partial characterization of a pheromone-induced adhesive surface antigen of Streptococcus faecalis, J. Bacteriol. 155: 714–721.PubMedGoogle Scholar
  43. 43.
    Kitada, C., Fujino, M., Mori, M., Sakagami, Y., Isogai, A., Suzuki, A., Clewell, D., and Craig, R., 1985, Synthesis and structure-activity relationships of Streptococcus faecalis sex pheromones, cPD1 and cAD1, in: Peptide Chemistry 1984 ( N. Izumiya, ed.), Protein Research Foundation, Osaka, pp. 43–48.Google Scholar
  44. 44.
    Kreft, B., Marre, R., Schramm, U., and Wirth, R., 1992, Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells, Infect. Immun. 60: 25–30.PubMedGoogle Scholar
  45. 45.
    Lacks, S., 1977, Binding and entry of DNA in bacterial transformation, in: Microbiol Interactions Series B. Receptors and Recognition, Vol. 3 ( J.L. Reissig, ed.), Chapman and Hall, London, pp. 177–232.Google Scholar
  46. 46.
    LeBlanc, D.J., Lee, L.N., Clewell, D.B., and Behnke, D., 1983, Broad geographical distribution of a cytotoxin gene mediating 3-hemolysis and bacteriocin activity among Streptococcus faecalis strains, Infect. Immun. 40: 1015–1022.PubMedGoogle Scholar
  47. 47.
    Mori, M., Sakagami, Y., Narita, M., Isogai, A., Fujino, M., Kitada, C., Craig, R., Clewell, D., and Suzuki, A., 1984, Isolation and structure of the bacterial sex pheromone, cADI, that induces plasmid transfer in Streptococcus faecalis, FEBS Leu. 178: 97–100.CrossRefGoogle Scholar
  48. 48.
    Mori, M., Isogai, A., Sakagami, Y., Fujino, M., Kitada, C., Clewell, D.B., and Suzuki, A., 1986, Isolation and structure of Streptococcus faecalis sex pheromone inhibitor, iAD1, that is excreted by donor strains harboring plasmid pAD1, Agric. Biol. Chem. 50: 539–541.CrossRefGoogle Scholar
  49. 49.
    Mori, M., Tanaka, H., Sakagami, Y., Isogai, A., Fujino, M., Kitada, C., White, B.A., An, EY., Clewell, D.B., and Suzuki, A., 1986, Isolation and structure of the Streptococcus faecalis sex pheromone, cAM373, FEBS Lett. 206: 69–72.PubMedCrossRefGoogle Scholar
  50. 50.
    Mori, M., Tanaka, H., Sakagami, Y., Isogai, A., Fujino, M., Kitada, C., Clewell, D.B., and Suzuki, A., 1987, Isolation and structure of the sex pheromone inhibitor, iPD1, excreted by Streptococcus faecalis donor strains harboring plasmid pPD1, J. Bacteriol. 169: 1747–1749.PubMedGoogle Scholar
  51. 51.
    Mori, M., Sakagami, Y., Ishii, Y., Isogai, A., Kitada, C., Fujino, M., Kitada, C., Adsit, J.C., Dunny, G.M., and Suzuki, A., 1988, Structure of cCF10, a peptide sex pheromone which induces conjugative transfer of the Streptococcus faecalis tetracycline-resistance plasmid, pCF10, J. Biol. Chem. 263:14, 574–14, 578.Google Scholar
  52. 52.
    Murray, B.E., An, F., and Clewell, D.B., 1988, Plasmids and pheromone response of the f3-lactamase producer Streptococcus (Enterococcus) faecalis HH22, Antimicrob. Agents Chemother. 32: 547–551.PubMedCrossRefGoogle Scholar
  53. 53.
    Nakayama, J., Nagasawa, H., Isogai, A., Clewell, D.B., and Suzuki, A., 1990, Amino acid sequence of pheromone-inducible surface protein in Enterococcus faecalis that is encoded on the conjugative plasmid pPD1, FEBS Leu. 268: 245–248.CrossRefGoogle Scholar
  54. 54.
    Nakayama, J., Watarai, H., Isogai, A., Clewell, D.B., and Suzuki, A., 1992, C-terminal identification of AD74, a proteolytic product of Enterococcus faecalis aggregation substance: application of liquid chromatography/mass spectrometry, Biosci. Biotech. Biochem. 56: 127–131.CrossRefGoogle Scholar
  55. 55.
    Nakayama, J,. Watarai, H., Nagasawa, H., Isogai, A., Clewell, D.B., and Suzuki, A., 1992, Immunological characterization of pheromone-induced proteins associated with sexual aggregation in Enterococcus faecalis, Biosci. Biotech. Biochem. 56: 264–269.CrossRefGoogle Scholar
  56. 56.
    Oliver, D.R., Brown, B.L., and Clewell, D.B., 1977, Characterization of plasmids determining hemolysin and bacteriocin production in Streptococcus faecalis 5952, J. Bacteriol. 130: 948–950.PubMedGoogle Scholar
  57. 57.
    Olmsted, S.B., Kao, S., van Putte, L.J., Gallo, J.C., Dunny, G.M., 1991, Role of pheromone-inducible surface protein Asc10 in mating aggregate formation and conjugal transfer of the Enterococcus faecalis plasmid pCF10, J. Bacteriol. 173: 7665–7672.PubMedGoogle Scholar
  58. 58.
    Pontius, L.T., and Clewell, D.B., 1991, A phase variation event that activates conjugation functions encoded by the Enterococcus faecalis plasmid pAD1, Plasmid 26: 172–185.PubMedCrossRefGoogle Scholar
  59. 59.
    Pontius, L.T., and Clewell, D.B., 1992, Regulation of the pAD1-encoded sex pheromone response in Enterococcus faecalis: nucleotide sequence analysis of traA, J. Bacteriol. 174: 1821–1827.PubMedGoogle Scholar
  60. 60.
    Pontius, L.T., and Clewell, D.B., 1992, Conjugative transfer of Enterococcus faecalis plasmid pAD1: nucleotide sequence and transcriptional fusion analysis of a region involved in positive regulation, J. Bacteriol. 174: 3152–3160.PubMedGoogle Scholar
  61. 61.
    Safer, M.H., Jr., Werner, P.K., and Muller, M., 1989, Insertion of proteins into bacterial membranes: mechanism, characteristics, and comparisons with the eucaryotic process, Microbiol. Rev. 53: 333–366.Google Scholar
  62. 62.
    Sannomiya, P., Craig, R.A., Clewell, D.B., Suzuki, A., Fujino, M., Till, G.O., and Marasco, W.A., 1990, Characterization of a new class of Enterococcus faecalis derived neutrophil chemotactic peptides: the sex pheromones, Proc. Natl. Acad. Sci. USA 87: 66–70.PubMedCrossRefGoogle Scholar
  63. 63.
    Suzuki, A., Mori, M., Sakagami, Y., Isogai, A., Fujino, M., Kitada, C., Craig, R.A., and Clewell, D.B., 1984, Isolation and structure of bacterial sex pheromone cPD1, Science 226; 849–850.PubMedCrossRefGoogle Scholar
  64. 64.
    Tomasz, A., 1969, Some aspects of the competent state in genetic transformation, Annu. Rev. Genet. 3: 217–232.CrossRefGoogle Scholar
  65. 65.
    Tomich, P.K., An, F.Y., Damle, S.P, and Clewell, D.B., 1979, Plasmid related transmissibility and multiple drug resistance in Streptococcus faecalis subs. zymogenes strain DS16, Antimicrob. Agents Chemother. 15: 828–830.PubMedCrossRefGoogle Scholar
  66. 66.
    Tomich, P.K., An, F.Y., and ClewelL, D.B., 1980, Properties of erythromycin-inducible transposon Tn917 in Streptococcus faecalis, J. Bacteriol. 141: 1366–1374.PubMedGoogle Scholar
  67. 67.
    Tomura, T., Hirano, T., Ito, T., and Yoshioka, M., 1973, Transmission of bacteriocinogenicity by conjugation in group D streptococci, Japan J. Microbiol. 17: 445–452.Google Scholar
  68. 68.
    Tortorello, M.L., and Dunny, G.M., 1985, Identification of multiple surface antigens associated with the sex pheromone response of Streptococcus faecalis, J. Bacteriol. 162: 131–137.PubMedGoogle Scholar
  69. 69.
    Trotter, K.M., and Dunny, G.M., 1990, Mutants of Enterococcus faecalis deficient as recipients in mating with donors carrying pheromone-inducible plasmids, Plasmid 24: 57–67.PubMedCrossRefGoogle Scholar
  70. 70.
    Wanner, G., Formanek, H., Galli, D., and Wirth, R., 1989, Localization of aggregation substances of Enterococcus faecalis after induction by sex pheromones. An ultrastructural comparison using immunolabeling, transmission and high resolution scanning electron microscopic techniques, Arch. Microbiol. 151: 491–497.PubMedCrossRefGoogle Scholar
  71. 71.
    Weaver, K.E., and Clewell, D.B., 1987, Transposon Tn917 delivery vectors for mutagenesis in Streptococcus faecalis, in: Streptococcal Genetics ( J. Ferretti and R. Curtiss III, eds.), American Society for Microbiology, Washington, DC, pp. 17–21.Google Scholar
  72. 72.
    Weaver, K.E., and Clewell, D.B., 1988, Regulation of the pAD1 sex pheromone response in Enterococcus faecalis: construction and characterization of lacZ transcriptional fusions in a key control region of the plasmid, J. Bacteriol. 170: 4343–4352.PubMedGoogle Scholar
  73. 73.
    Weaver, K.E., and Clewell, D.B., 1989, Construction of Enterococcus faecalis pADI miniplasmids: identification of a minimal pheromone response regulatory region and evaluation of a novel pheromone-dependent growth inhibition, Plasmid 22: 106–119.PubMedCrossRefGoogle Scholar
  74. 74.
    Weaver, K.E., and Clewell, D.B., 1990, Regulation of the pAD1 sex pheromone response in Enterococcus faecalis: effects of host strain and traA, traB, and C region mutants on expression of an E region pheromone-inducible lacZ fusion, J. Bacteriol. 172: 2633–2641.PubMedGoogle Scholar
  75. 75.
    Weaver, K.E., and Clewell, D.B., 1991, Control of Enterococcus faecalis sex pheromone cAD1 elaboration: effect of culture aeration and pAD1 plasmid-encoded determinants, Plasmid 25: 177–189.PubMedCrossRefGoogle Scholar
  76. 76.
    Wicken, A.J., Elliott, S.D., and Baddiley, J., 1963, The identity of streptococcal group D antigen with teichoic acid, J. Gen. Microbiol. 31: 231–239.PubMedGoogle Scholar
  77. 77.
    Yagi, Y., Kessler, R.E., Shaw, J.H., Lopatin, D.E., An, F.Y., and Clewell, D.B., 1983, Plasmid content of Streptococcus faecalis strain 39–5 and identification of a pheromone (cPD1)-induced surface antigen, J. Gen. Microbiol. 129: 1207–1215.PubMedGoogle Scholar
  78. 78.
    Youngman, P.J., 1987, Plasmid vectors for recovering and exploiting Tn917 transposition in Bacillus and other gram-positives, in: Plasmids: A Practical Approach ( K. Hardy, ed.), IRL Press, Oxford, pp. 79–103.Google Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Don B. Clewell
    • 1
  1. 1.Department of Biologic and Materials Sciences, School of Dentistry and Department of Microbiology and Immunology, School of MedicineThe University of MichiganAnn ArborUSA

Personalised recommendations