Dataset Information

Amino acids as wetting agents: surface translocation by Porphyromonas gingivalis.

ABSTRACT: Our understanding of how oral microbiota adapt in response to changes in their surroundings remains limited. This is particularly true of the slow-growing anaerobes that persist below the gum line. Here, we report that the oral anaerobe Porphyromonas gingivalis strain 381 can surface translocate when sandwiched between two surfaces. We show that during movement, this bacterium alters its metabolism, specifically side products of arginine utilization including citrulline and ornithine accumulated in the translocating cells; while arginine, N-acetyl-arginine, and the polyamine putrescine, which is produced from arginine were consumed. In addition, our results indicate that movement requires modification of the surrounding environment via proteolysis, cell dispersion, cell-on-cell rolling, and sub-diffusive cell-driven motility. We also show that production of fimbriae and fimbriae-associated proteins; as well as the regulation of contact-dependent growth inhibition genes, which are known to be involved in self-nonself discrimination, and the type IX secretion system are central to surface translocation. These studies provide a first glimpse into P. gingivalis motility and its relationship to ecological variables.

SUBMITTER: Moradali MF

PROVIDER: S-EPMC6775972 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Amino acids as wetting agents: surface translocation by Porphyromonas gingivalis.

Moradali M Fata MF Ghods Shirin S Angelini Thomas E TE Davey Mary Ellen ME

The ISME journal 20190219 6

Our understanding of how oral microbiota adapt in response to changes in their surroundings remains limited. This is particularly true of the slow-growing anaerobes that persist below the gum line. Here, we report that the oral anaerobe Porphyromonas gingivalis strain 381 can surface translocate when sandwiched between two surfaces. We show that during movement, this bacterium alters its metabolism, specifically side products of arginine utilization including citrulline and ornithine accumulated ...[more]

PMID: 30783212

Similar Datasets

Project description:Studies are showing that the stress hormone cortisol can reach high levels in the gingival sulcus and induce shifts in the metatranscriptome of the oral microbiome. Interestingly, it has also been shown that cortisol can influence expression levels of Type IX Secretion System (T9SS) genes involved in gliding motility in bacteria belonging to the phylum Bacteroidota. The objective of this study was to determine if cortisol impacts gene expression and surface translocation of Porphyromonas gingivalis strain W50. To conduct these experiments, P. gingivalis was stabbed to the bottom of soft agar plates containing varying cortisol concentrations (0 μM, 0.13 μM, 1.3 μM, and 13 μM), and surface translocation on the subsurface was observed after 48 h of incubation. The results show that when grown with certain nutrients, i.e., in rich medium with the addition of sheep blood, lactate, or pyruvate, cortisol promotes migration of P. gingivalis in a concentration-dependent manner. To begin to examine the underlying mechanisms, quantitative PCR was used to evaluate differential expression of genes when P. gingivalis was exposed to cortisol. In particular, we focused on differential expression of T9SS-associated genes, including mfa5, since it was previously shown that Mfa5 is required for cell movement and cell-to-cell interactions. The data show that mfa5 is significantly up-regulated in the presence of cortisol. Moreover, an mfa5 deletion mutant showed less surface translocation compared to the wild-type P. gingivalis in the presence of cortisol, and the defects of the mfa5 deletion mutant were restored by complementation. Overall, cortisol can stimulate P. gingivalis surface translocation and this coincides with higher expression levels of T9SS-associated genes, which are known to be essential to gliding motility. Our findings support a high possibility that the stress hormone cortisol from the host can promote surface translocation and potentially virulence of P. gingivalis.

Project description:Many bacteria switch between a sessile and a motile mode in response to environmental and host-related signals. Porphyromonas gingivalis, an oral anaerobe implicated in the etiology of chronic periodontal disease, has long been described as a nonmotile bacterium. And yet, recent studies have shown that under certain conditions, P. gingivalis is capable of surface translocation. Considering these findings, this work aimed to increase our understanding of how P. gingivalis transitions between sessile growth and surface migration. Here, we show that the peptidylarginine deiminase secreted by P. gingivalis (PPAD), an enzyme previously shown to be upregulated during surface translocation and to constrain biofilm formation, promotes surface translocation. In the absence of PPAD, the production of outer membrane vesicles (OMVs) was drastically reduced. In turn, there was a reduction in gingipain-mediated proteolysis and a reduced zone of hydration around the site of inoculation. Transcriptome sequencing (RNA-Seq) and metabolomics analyses also showed that these changes corresponded to a shift in arginine metabolism. Overall, this report provides new evidence for the functional relevance of PPAD and proteases, as well as the importance of PPAD activity in OMV biogenesis and release. Our findings support the model that citrullination is a critical mechanism during lifestyle transition between surface-attached growth and surface translocation by modulating OMV-mediated proteolysis and arginine metabolism.IMPORTANCE Gram-negative bacteria produce nanosized OMVs that are actively released into their surroundings. The oral anaerobe P. gingivalis is prolific in OMV production, and many of the proteins packaged in these vesicles are proteolytic or protein-modifying enzymes. This includes key virulence determinants, such as the gingipains and PPAD (a unique peptidylarginine deiminase). Here, we show that PPAD activity (citrullination) is involved in OMV biogenesis. The study revealed an unusual mechanism that allows this bacterium to transform its surroundings. Since OMVs are detected in circulation and in systemic tissues, our study results also support the notion that PPAD activity may be a key factor in the correlation between periodontitis and systemic diseases, further supporting the idea of PPAD as an important therapeutic target.

Dataset Information

Amino acids as wetting agents: surface translocation by Porphyromonas gingivalis.

Publications

Amino acids as wetting agents: surface translocation by Porphyromonas gingivalis.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets