Influence of a model human defensive peroxidase system on oral streptococcal antagonism.
Streptococcus is a dominant genus in the human oral cavity, making up about 20 % of the more than 800 species of bacteria that have been identified, and about 80 % of the early biofilm colonizers. Oral streptococci include both health-compatible (e.g. Streptococcus gordonii and Streptococcus sanguinis) and pathogenic strains (e.g. the cariogenic Streptococcus mutans). Because the streptococci have similar metabolic requirements, they have developed defence strategies that lead to antagonism (also known as bacterial interference). S. mutans expresses bacteriocins that are cytotoxic toward S. gordonii and S. sanguinis, whereas S. gordonii and S. sanguinis differentially produce H(2)O(2) (under aerobic growth conditions), which is relatively toxic toward S. mutans. Superimposed on the inter-bacterial combat are the effects of the host defensive mechanisms. We report here on the multifarious effects of bovine lactoperoxidase (bLPO) on the antagonism between S. gordonii and S. sanguinis versus S. mutans. Some of the effects are apparently counterproductive with respect to maintaining a health-compatible population of streptococci. For example, the bLPO system (comprised of bLPO+SCN(-)+H(2)O(2)) destroys H(2)O(2), thereby abolishing the ability of S. gordonii and S. sanguinis to inhibit the growth of S. mutans. Furthermore, bLPO protein (with or without its substrate) inhibits bacterial growth in a biofilm assay, but sucrose negates the inhibitory effects of the bLPO protein, thereby facilitating adherence of S. mutans in lieu of S. gordonii and S. sanguinis. Our findings may be relevant to environmental pressures that select early supragingival colonizers.
Ashby
Michael T
MT
Department of Chemistry and Biochemistry, University of Oklahoma, Norman, OK 73019, USA.
Kreth
Jens
J
Department of Microbiology and Immunology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA.
Soundarajan
Muthu
M
Department of Chemistry and Biochemistry, University of Oklahoma, Norman, OK 73019, USA.
Sivuilu
Laure Sita
LS
Department of Chemistry and Biochemistry, University of Oklahoma, Norman, OK 73019, USA.
D000818:Animals; D000898:Antibiosis; D018441:Biofilms / Q000254:growth & development; D002374:Catalase / Q000378:metabolism; D002417:Cattle; D006861:Hydrogen Peroxide / Q000378:metabolism; D007784:Lactoperoxidase / Q000378:metabolism*; D009055:Mouth / Q000382:microbiology; D054773:Streptococcus gordonii / Q000254:growth & development*; D013295:Streptococcus mutans / Q000254:growth & development*; D013298:Streptococcus sanguis / Q000254:growth & development*; D013861:Thiocyanates / Q000378:metabolism
D013861:Thiocyanates; C014607:hypothiocyanite ion; D006861:Hydrogen Peroxide; D007784:Lactoperoxidase; D002374:Catalase
Infect Immun. 1983 Feb;39(2):767-78
6832819
Biochim Biophys Acta. 1986 Apr 22;870(3):377-84
3697357
J Clin Microbiol. 2005 Nov;43(11):5721-32
16272510
Arch Biochem Biophys. 2006 Jan 15;445(2):261-8
16111647
Periodontol 2000. 2006;42:80-7
16930307
Caries Res. 2001 Jul-Aug;35(4):258-64
11423721
J Dent Res. 2008 Oct;87(10):900-14
18809743
Odontology. 2006 Sep;94(1):1-9
16998612
J Periodontol. 1995 Sep;66(9):766-74
7500242
J Clin Periodontol. 2005;32 Suppl 6:7-15
16128825
Biochim Biophys Acta. 1981 Apr 14;658(2):238-47
7248302
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14547-52
10588742
J Bacteriol. 2001 Jun;183(12):3770-83
11371542
J Dent Res. 1990 Feb;69 Spec No:653-9; discussion 682-3
2179326
Nature. 2007 Oct 18;449(7164):811-8
17943117
Nat Rev Microbiol. 2008 Sep;6(9):693-9
18587409
Anal Biochem. 2003 Jan 15;312(2):224-7
12531209
J Bacteriol. 2007 Apr;189(8):3166-75
17277061
Biochemistry. 1988 Jan 12;27(1):233-9
3349028
FEMS Microbiol Ecol. 2008 Dec;66(3):637-44
18785881
Arch Biochem Biophys. 1959 May;82(1):70-7
13650640
J Gen Microbiol. 1963 Apr;31:125-33
13941150
J Dent Res. 2001 May;80(5):1436-40
11437215
J Clin Microbiol. 1985 Dec;22(6):996-1006
3905855
Microbes Infect. 2000 Nov;2(13):1599-607
11113379
Biochemistry. 1998 Jun 23;37(25):8965-72
9636038
J Dent Res. 1987 Feb;66(2):616-8
3476578
J Dairy Res. 1986 Nov;53(4):507-14
3794018
J Contemp Dent Pract. 2000 Aug 15;1(3):18-29
12167880
Appl Environ Microbiol. 2006 Oct;72(10):6734-42
17021225
Arch Oral Biol. 1975 Oct;20(10):641-8
1059386
Anal Biochem. 1979 Apr 1;94(1):75-81
37780
J Clin Microbiol. 2008 Apr;46(4):1407-17
18216213
Talanta. 2000 May 5;51(6):1049-58
18967936
Caries Res. 1993;27(1):26-30
8448770
J Anat. 1978 Sep;127(Pt 1):181-91
701194
J Clin Microbiol. 2008 Jun;46(6):2015-21
18385433
J Dent Res. 2005 Dec;84(12):1172-7
16304449
Infect Immun. 1982 Jan;35(1):20-4
7033135
J Bacteriol. 2008 Jul;190(13):4632-40
18441055
Eur J Biochem. 1977 Oct 17;80(1):209-14
562752
Oral Microbiol Immunol. 2008 Jun;23(3):213-9
18402607
J Dent Res. 1987 Feb;66(2):486-91
3040825
Periodontol 2000. 2005;38:135-87
15853940
Infect Immun. 1980 Sep;29(3):1190-2
7429633
FEMS Microbiol Lett. 2000 Dec 1;193(1):1-6
11094270
Caries Res. 2007;41(5):413-22
17713343
J Dent Res. 1977 Dec;56(12):1603-7
277482
Infect Immun. 1994 Feb;62(2):529-35
8300211
J Clin Periodontol. 2001 Jul;28(7):697-700
11422593
Appl Environ Microbiol. 1979 Nov;38(5):821-6
396883
J Appl Microbiol. 2001 Apr;90(4):489-93
11309058
Appl Environ Microbiol. 2001 Jan;67(1):15-21
11133423
Infect Immun. 1983 Apr;40(1):70-80
6832837
J Bacteriol. 1983 Jun;154(3):1236-44
6304008
Adv Dent Res. 1997 Apr;11(1):110-26
9524448
J Gen Microbiol. 1966 Apr;43(1):31-43
5333458
J Dent Res. 1977 Dec;56(12):1608-13
277483
J Dairy Sci. 1985 May;68(5):1095-102
3916277
Dent Clin North Am. 1999 Oct;43(4):599-614, v-vi
10553246
J Clin Microbiol. 2002 Mar;40(3):1001-9
11880430
Infect Immun. 1977 Jul;17(1):112-6
885609
Biochemistry. 1981 May 26;20(11):3273-80
7248282
Arch Oral Biol. 1985;30(7):519-23
3864401
J Dent Res. 1981 Apr;60(4):831-7
6259229
J Oral Pathol. 1987 Sep;16(8):412-6
2826736
Arch Oral Biol. 1995 Aug;40(8):753-63
7487577