Abstract
The relationship between the selective abilities of bacteria to adhere and their predilections for colonizing different mammalian hosts was investigated by using bacteria indigenous to the tongue dorsum of humans and rats as models. Streptococcus salivarius and S. sanguis averaged 22.6 and 2.8%, respectively, of the cultivable bacteria recovered from swab samples of the tonges of five humans, but these organisms were not indigenous on the tongues of rats (Charles River strain). S. faecalis and serum-requiring diphtheroids were consistently prominant on the tongues of rats, but they were not detected on the tongues of the humans examined. The ability of these organisms to adhere to the tongue surface of the hosts was compared by introducing mixtures of streptomycin-resistant strains into the mouths of human volunteers and rats. S. salivarius adhered in higher proportions to the dorsal tongue surface of humans than did strains of S. faecalis and the serum-requiring diphtheroid. S. sanguis also adhered to human tongues better than the serum-requiring diphtheroid. However, S. faecalis and the serum-requiring diphtheroid sorbed in higher proportions to the tongues of rats. In an in vivo assay, human strains of S. pyogenes and S. salivarius attached in higher numbers to buccal epithelial cells derived from humans than to those obtained from rats, whereas the reverse was observed with a serum-requiring diphtheroid derived from rats. Collectively, these studies show that bacteria sorb with a high degree of specificity to the tissues of different mammalian hosts, and the relative adherence of the organisms studied correlated with their natural host tropisms. The selective adherence of S. salvarius and S. faecalis was similar to the tongues of conventional and germ-free rats, suggesting that the presence of an indigenous bacterial flora did not significantly influence their attachment selectivity. Moreover, the ability of these organisms to colonize the tongues of gnotobiotic rats lacking an indigenous flora paralleled their adherence selectivity. Direct scanning microscopic observations indicated that the tongue dorsum of conventional rats is highly papillated but contains relatively sparse bacterial populations. Indigenous organisms colonized the bases of papillae on the anterior tip and lateral edges of the tongue as discrete microcolonies, but bacteria were rarely observed on other papillae. This localized and restricted pattern of colonization and the spatial distribution of the microcolonies of indigenous bacteria present also suggest that antagonistic interactions are unlikely to account for the bacterial tropisms observed for colonization of the tongues of rats.
MeSH Terms
Animals
Cell Adhesion
Cheek
Drug Resistance, Microbial
Enterococcus faecalis/drug effects,growth & development
Epithelium/microbiology
Germ-Free Life
Humans
Rats
Species Specificity
Streptococcus pyogenes/growth & development
Streptococcus sanguis/drug effects,growth & development
Streptomycin/pharmacology
Tongue/microbiology,ultrastructure
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gibbons R J
Spinell D M
Skobe Z
References (28)
28 references, click to expand
-
Changing agglutination activities of salivary immunoglobulin A preparations against oral streptococci.
Infect Immun. 1975 Mar;11(3):603-6
PMID: 803930
-
Progressive changes of Vibrio serotypes in germ-free mice infected with Vibrio cholerae.
J Bacteriol. 1969 Sep;99(3):688-95
PMID: 5370274
-
Immune responses of specific pathogen-free and gnotobiotic mice to antigens of indigenous and nonindigenous microorganisms.
Infect Immun. 1975 Feb;11(2):320-9
PMID: 1089600
-
Bacterial adherence in oral microbial ecology.
Annu Rev Microbiol. 1975;29:19-44
PMID: 1180512
-
The gastrointestinal epithelium and its autochthonous bacterial flora.
J Exp Med. 1968 Jan 1;127(1):67-76
PMID: 4169441
-
Immunological responses and microorganisms indigenous to the gastrointestinal tract.
Am J Clin Nutr. 1972 Dec;25(12):1364-71
PMID: 4565353
-
Suppression of Candida albicans by human oral streptococci in gnotobiotic mice.
Infect Immun. 1973 Nov;8(5):846-9
PMID: 4584056
-
The relation of streptococci, lactobacilli, and the general oral and fecal flora to the progression of dental caries in the hamster.
J Dent Res. 1957 Oct;36(5):695-708
PMID: 13475558
-
THE SALIVARY SECRETION OF ANTIBODY.
Ala J Med Sci. 1965 Jan;2:15-22
PMID: 14285124
-
Selective bacterial adherence to oral epithelial surfaces and its role as an ecological determinant.
Infect Immun. 1971 Apr;3(4):567-73
PMID: 16558019
-
Immunological response of mice to members of the autochthonous intestinal microflora.
Infect Immun. 1972 Oct;6(4):525-32
PMID: 4628898
-
Experimental Shigella infections in laboratory animals. I. Antagonism by human normal flora components in gnotobiotic mice.
Infect Immun. 1972 Aug;6(2):168-73
PMID: 4631914
-
The oral microbiota of man from birth to senility.
J Periodontol. 1971 Aug;42(8):485-96
PMID: 4998039
-
Biochemical and immunological heterogeneity of Bacteroides melaninogenicus.
Arch Oral Biol. 1967 Dec;12(12):1605-13
PMID: 5237341
-
Adherence as an ecological determinant for streptococci in the human mouth.
Arch Oral Biol. 1971 Oct;16(10):1131-41
PMID: 5289677
-
Laboratory studies with a selective Enterococcus medium.
Appl Microbiol. 1970 Sep;20(3):433-6
PMID: 5485723
-
OBSERVATIONS ON THE FLORA OF THE ALIMENTARY TRACT OF ANIMALS AND FACTORS AFFECTING ITS COMPOSITION.
J Pathol Bacteriol. 1965 Jan;89:95-122
PMID: 14263502
-
A survey of the bacterial flora of the periodontium in the rice rat.
Arch Oral Biol. 1959 Aug;1:1-7
PMID: 14419317
-
Bovine veneral vibriosis: antigenic variation of the bacterium during infection.
Infect Immun. 1975 Feb;11(2):240-4
PMID: 46214
-
Localization of bacteria on the rat tongue with scanning and transmission electron microscopy.
J Dent Res. 1975 Jul-Aug;54(4):777-82
PMID: 1057561
-
Inhibition of streptococcal attachment to receptors on human buccal epithelial cells by antigenically similar salivary glycoproteins.
Infect Immun. 1975 Apr;11(4):711-8
PMID: 1168169
-
Blood-group and Forssman antigenic determinants shared between microbes and mammalian cells.
Prog Allergy. 1971;15:9-77
PMID: 4133332
-
Shigella, indigenous flora interactions in mice.
Am J Clin Nutr. 1972 Dec;25(12):1433-40
PMID: 4565357
-
Parameters affecting the adherence and tissue tropisms of Streptococcus pyogenes.
Infect Immun. 1974 Jan;9(1):85-91
PMID: 4587386
-
Human antibody to Bacteroidaceae.
Am J Clin Nutr. 1972 Dec;25(12):1351-6
PMID: 4629539
-
Persistent genital tract infection with Vibrio fetus intestinalis associated with serotypic alteration of the infecting strain.
Am J Vet Res. 1973 Nov;34(11):1399-403
PMID: 4748723
-
Ability of Veillonella and Neisseria species to attach to oral surfaces and their proportions present indigenously.
Infect Immun. 1971 Sep;4(3):264-8
PMID: 5154885
-
The prevalence of enterococci in the human mouth and their pathogenicity in animal models.
Arch Oral Biol. 1975 Jul;20(7):473-7
PMID: 807189