Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>

<p>Abstract</p> <p>Background</p> <p><it>Porphyromonas gingivalis</it>, a periodontal pathogen, expresses a number of virulence factors, including long (FimA) and short (Mfa) fimbriae as well as gingipains comprised of arginine-specific (Rgp) and lysine-spec...

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Main Authors: Tribble Gena D, Nakayama Koji, Hamada Nobushiro, Inaba Hiroaki, Yamamoto Yumiko, Hashino Ei, Amano Atsuo, Kuboniwa Masae, Lamont Richard J, Shizukuishi Satoshi
Format: Article
Language:English
Published: BMC 2009-05-01
Series:BMC Microbiology
Online Access:http://www.biomedcentral.com/1471-2180/9/105
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spelling doaj-5f1608bddcd444f492da796f127e2d8d2020-11-24T23:15:52ZengBMCBMC Microbiology1471-21802009-05-019110510.1186/1471-2180-9-105Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>Tribble Gena DNakayama KojiHamada NobushiroInaba HiroakiYamamoto YumikoHashino EiAmano AtsuoKuboniwa MasaeLamont Richard JShizukuishi Satoshi<p>Abstract</p> <p>Background</p> <p><it>Porphyromonas gingivalis</it>, a periodontal pathogen, expresses a number of virulence factors, including long (FimA) and short (Mfa) fimbriae as well as gingipains comprised of arginine-specific (Rgp) and lysine-specific (Kgp) cysteine proteinases. The aim of this study was to examine the roles of these components in homotypic biofilm development by <it>P. gingivalis</it>, as well as in accumulation of exopolysaccharide in biofilms.</p> <p>Results</p> <p>Biofilms were formed on saliva-coated glass surfaces in PBS or diluted trypticase soy broth (dTSB). Microscopic observation showed that the wild type strain formed biofilms with a dense basal monolayer and dispersed microcolonies in both PBS and dTSB. A FimA deficient mutant formed patchy and small microcolonies in PBS, but the organisms proliferated and formed a cohesive biofilm with dense exopolysaccharides in dTSB. A Mfa mutant developed tall and large microcolonies in PBS as well as dTSB. A Kgp mutant formed markedly thick biofilms filled with large clumped colonies under both conditions. A RgpA/B double mutant developed channel-like biofilms with fibrillar and tall microcolonies in PBS. When this mutant was studied in dTSB, there was an increase in the number of peaks and the morphology changed to taller and loosely packed biofilms. In addition, deletion of FimA reduced the autoaggregation efficiency, whereas autoaggregation was significantly increased in the Kgp and Mfa mutants, with a clear association with alteration of biofilm structures under the non-proliferation condition. In contrast, this association was not observed in the Rgp-null mutants.</p> <p>Conclusion</p> <p>These results suggested that the FimA fimbriae promote initial biofilm formation but exert a restraining regulation on biofilm maturation, whereas Mfa and Kgp have suppressive and regulatory roles during biofilm development. Rgp controlled microcolony morphology and biovolume. Collectively, these molecules seem to act coordinately to regulate the development of mature <it>P. gingivalis </it>biofilms.</p> http://www.biomedcentral.com/1471-2180/9/105
collection DOAJ
language English
format Article
sources DOAJ
author Tribble Gena D
Nakayama Koji
Hamada Nobushiro
Inaba Hiroaki
Yamamoto Yumiko
Hashino Ei
Amano Atsuo
Kuboniwa Masae
Lamont Richard J
Shizukuishi Satoshi
spellingShingle Tribble Gena D
Nakayama Koji
Hamada Nobushiro
Inaba Hiroaki
Yamamoto Yumiko
Hashino Ei
Amano Atsuo
Kuboniwa Masae
Lamont Richard J
Shizukuishi Satoshi
Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
BMC Microbiology
author_facet Tribble Gena D
Nakayama Koji
Hamada Nobushiro
Inaba Hiroaki
Yamamoto Yumiko
Hashino Ei
Amano Atsuo
Kuboniwa Masae
Lamont Richard J
Shizukuishi Satoshi
author_sort Tribble Gena D
title Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
title_short Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
title_full Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
title_fullStr Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
title_full_unstemmed Distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>Porphyromonas gingivalis</it>
title_sort distinct roles of long/short fimbriae and gingipains in homotypic biofilm development by <it>porphyromonas gingivalis</it>
publisher BMC
series BMC Microbiology
issn 1471-2180
publishDate 2009-05-01
description <p>Abstract</p> <p>Background</p> <p><it>Porphyromonas gingivalis</it>, a periodontal pathogen, expresses a number of virulence factors, including long (FimA) and short (Mfa) fimbriae as well as gingipains comprised of arginine-specific (Rgp) and lysine-specific (Kgp) cysteine proteinases. The aim of this study was to examine the roles of these components in homotypic biofilm development by <it>P. gingivalis</it>, as well as in accumulation of exopolysaccharide in biofilms.</p> <p>Results</p> <p>Biofilms were formed on saliva-coated glass surfaces in PBS or diluted trypticase soy broth (dTSB). Microscopic observation showed that the wild type strain formed biofilms with a dense basal monolayer and dispersed microcolonies in both PBS and dTSB. A FimA deficient mutant formed patchy and small microcolonies in PBS, but the organisms proliferated and formed a cohesive biofilm with dense exopolysaccharides in dTSB. A Mfa mutant developed tall and large microcolonies in PBS as well as dTSB. A Kgp mutant formed markedly thick biofilms filled with large clumped colonies under both conditions. A RgpA/B double mutant developed channel-like biofilms with fibrillar and tall microcolonies in PBS. When this mutant was studied in dTSB, there was an increase in the number of peaks and the morphology changed to taller and loosely packed biofilms. In addition, deletion of FimA reduced the autoaggregation efficiency, whereas autoaggregation was significantly increased in the Kgp and Mfa mutants, with a clear association with alteration of biofilm structures under the non-proliferation condition. In contrast, this association was not observed in the Rgp-null mutants.</p> <p>Conclusion</p> <p>These results suggested that the FimA fimbriae promote initial biofilm formation but exert a restraining regulation on biofilm maturation, whereas Mfa and Kgp have suppressive and regulatory roles during biofilm development. Rgp controlled microcolony morphology and biovolume. Collectively, these molecules seem to act coordinately to regulate the development of mature <it>P. gingivalis </it>biofilms.</p>
url http://www.biomedcentral.com/1471-2180/9/105
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