Coaggregation and biofilm growth of Granulicatella spp. with Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans

Maribasappa Karched 1, Radhika G Bhardwaj 2, Sirkka E Asikainen 3

Affiliations

doi: 10.1186/s12866-015-0439-z

Abstract

Background: Members of fastidious Granulicatella and Aggregatibacter genera belong to normal oral flora bacteria that can cause serious infections, such as infective endocarditis. Aggregatibacter actinomycetemcomitans has long been implicated in aggressive periodontitis, whereas DNA-based methods only recently showed an association between Granulicatella spp. and dental diseases. As bacterial coaggregation is a key phenomenon in the development of oral and nonoral multispecies bacterial communities it would be of interest knowing coaggregation pattern of Granulicatella species with A. actinomycetemcomitans in comparison with the multipotent coaggregator Fusobacterium nucleatum. The aim was to investigate coaggregation and biofilm formation of Granulicatella elegans and Granulicatella adiacens with A. actinomycetemcomitans and F. nucleatum strains.

Results: F. nucleatum exhibited significantly (p < 0.05) higher autoaggregation than all other test species, followed by A. actinomycetemcomitans SA269 and G. elegans. A. actinomycetemcomitans CU1060 and G. adiacens did not autoaggregate. G. elegans with F. nucleatum exhibited significantly (p < 0.05) higher coaggregation than most others, but failed to grow as biofilm together or separately. With F. nucleatum as partner, A. actinomycetemcomitans strains SA269, a rough-colony wild-type strain, and CU1060, a spontaneous smooth-colony laboratory variant, and G. adiacens were the next in coaggregation efficiency. These dual species combinations also were able to grow as biofilms. While both G. elegans and G. adiacens coaggregated with A. actinomycetemcomitans strain SA269, but not with CU1060, they grew as biofilms with both A. actinomycetemcomitans strains.

Conclusions: G. elegans failed to form biofilm with F. nucleatum despite the strongest coaggregation with it. The ability of Granulicatella spp. to coaggregate and/or form biofilms with F. nucleatum and A. actinomycetemcomitans strains suggests that Granulicatella spp. have the potential to integrate into dental plaque biofilms.

Figures

Fig. 1 Pleomorphic cell morphology of Granulicatella spp. G. elegans CCUG 38949 and G. adiacens CCUG 27809-T were grown on chocolate blood agar supplemented with or without pyridoxal as described in the methods section. Scanning electron microscopy was performed as described in methods. The images were acquired at 10,000× magnification using Zeiss Leo SUPRA® 50VP scanning electron microscope. Bar represents 2 μm

Fig. 1 Pleomorphic cell morphology of Granulicatella spp. G. elegans CCUG 38949 and G. adiacens CCUG 27809-T were grown on chocolate blood agar supplemented with or without pyridoxal as described in the methods section. Scanning electron microscopy was performed as described in methods. The images were acquired at 10,000× magnification using Zeiss Leo SUPRA® 50VP scanning electron microscope. Bar represents 2 μm

Fig. 2 Autoaggregation and coaggregation of Granulicatella spp. Cell suspensions of each test bacterial strain separately or in combination with a partner species were prepared as described in the methods section. OD600 was measured every 15 min and the OD600 values were converted into percent autoaggregation (panel A) or coaggregation (panel B) using the formula described in the methods part. Abbreviations: Aa A. actinomycetemcomitans; Ge G. elegans; Ga G. adiacens and Fn F. nucleatum. The results are means (SD) from 3 independent experiments. *p < 0.05

Fig. 2 Autoaggregation and coaggregation of Granulicatella spp. Cell suspensions of each test bacterial strain separately or in combination with a partner species were prepared as described in the methods section. OD600 was measured every 15 min and the OD600 values were converted into percent autoaggregation (panel A) or coaggregation (panel B) using the formula described in the methods part. Abbreviations: Aa A. actinomycetemcomitans; Ge G. elegans; Ga G. adiacens and Fn F. nucleatum. The results are means (SD) from 3 independent experiments. *p < 0.05

Fig. 3 Auto- and coaggregation of Granulicatella spp. Bacterial cell suspensions of test species alone or in combination of the partner species were prepared as described in the methods section. A 10-μl aliquot from each suspension was applied on a glass slide with a cover slip and autoaggregation (panel A) and coaggregation (panel B) were assessed visually by observing at 1000× using phase contrast optics on a Leica DMLM microscope. Abbreviations: Fn F. nucleatum, Ge G. elegans, Ga G. adiacens, Aa A. actinomycetemcomitans

Fig. 3 Auto- and coaggregation of Granulicatella spp. Bacterial cell suspensions of test species alone or in combination of the partner species were prepared as described in the methods section. A 10-μl aliquot from each suspension was applied on a glass slide with a cover slip and autoaggregation (panel A) and coaggregation (panel B) were assessed visually by observing at 1000× using phase contrast optics on a Leica DMLM microscope. Abbreviations: Fn F. nucleatum, Ge G. elegans, Ga G. adiacens, Aa A. actinomycetemcomitans

Fig 4 Biofilm formation by Granulicatella spp. in the presence or absence of F. nucleatum and A. actinomycetemcomitans strains. Bacterial strains were cultured separately or together with a partner species in 24-well plates in brucella broth in anaerobic atmosphere for 3 days as described in the methods section. After the incubation period, biofilms were washed gently to remove unattached cells and stained with 2 % crystal violet for quantifying biofilm mass. Abbreviations: Fn F. nucleatum, Ge G elegans, Ga G. adiacens, Aa A. actinomycetemcomitans. The results are means (SD) from 3 independent experiments. *p < 0.05

Fig 4 Biofilm formation by Granulicatella spp. in the presence or absence of F. nucleatum and A. actinomycetemcomitans strains. Bacterial strains were cultured separately or together with a partner species in 24-well plates in brucella broth in anaerobic atmosphere for 3 days as described in the methods section. After the incubation period, biofilms were washed gently to remove unattached cells and stained with 2 % crystal violet for quantifying biofilm mass. Abbreviations: Fn F. nucleatum, Ge G elegans, Ga G. adiacens, Aa A. actinomycetemcomitans. The results are means (SD) from 3 independent experiments. *p < 0.05

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