Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>

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 i...

Full description

Bibliographic Details
Main Authors: Hey-Min Kim, Christina Magda Rothenberger, Mary Ellen Davey
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/11/9/982
_version_ 1797483886905655296
author Hey-Min Kim
Christina Magda Rothenberger
Mary Ellen Davey
author_facet Hey-Min Kim
Christina Magda Rothenberger
Mary Ellen Davey
author_sort Hey-Min Kim
collection DOAJ
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 <i>Porphyromonas gingivalis</i> strain W50. To conduct these experiments, <i>P. gingivalis</i> 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 <i>P. gingivalis</i> in a concentration-dependent manner. To begin to examine the underlying mechanisms, quantitative PCR was used to evaluate differential expression of genes when <i>P. gingivalis</i> was exposed to cortisol. In particular, we focused on differential expression of T9SS-associated genes, including <i>mfa5,</i> since it was previously shown that Mfa5 is required for cell movement and cell-to-cell interactions. The data show that <i>mfa5</i> is significantly up-regulated in the presence of cortisol. Moreover, an <i>mfa5</i> deletion mutant showed less surface translocation compared to the wild-type <i>P. gingivalis</i> in the presence of cortisol, and the defects of the <i>mfa5</i> deletion mutant were restored by complementation. Overall, cortisol can stimulate <i>P. gingivalis</i> 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 <i>P. gingivalis</i>.
first_indexed 2024-03-09T22:53:32Z
format Article
id doaj.art-b831e776e717437090699de8b7a33672
institution Directory Open Access Journal
issn 2076-0817
language English
last_indexed 2024-03-09T22:53:32Z
publishDate 2022-08-01
publisher MDPI AG
record_format Article
series Pathogens
spelling doaj.art-b831e776e717437090699de8b7a336722023-11-23T18:15:26ZengMDPI AGPathogens2076-08172022-08-0111998210.3390/pathogens11090982Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>Hey-Min Kim0Christina Magda Rothenberger1Mary Ellen Davey2Department of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL 32610, USADepartment of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL 32610, USADepartment of Oral Biology, College of Dentistry, University of Florida, Gainesville, FL 32610, USAStudies 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 <i>Porphyromonas gingivalis</i> strain W50. To conduct these experiments, <i>P. gingivalis</i> 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 <i>P. gingivalis</i> in a concentration-dependent manner. To begin to examine the underlying mechanisms, quantitative PCR was used to evaluate differential expression of genes when <i>P. gingivalis</i> was exposed to cortisol. In particular, we focused on differential expression of T9SS-associated genes, including <i>mfa5,</i> since it was previously shown that Mfa5 is required for cell movement and cell-to-cell interactions. The data show that <i>mfa5</i> is significantly up-regulated in the presence of cortisol. Moreover, an <i>mfa5</i> deletion mutant showed less surface translocation compared to the wild-type <i>P. gingivalis</i> in the presence of cortisol, and the defects of the <i>mfa5</i> deletion mutant were restored by complementation. Overall, cortisol can stimulate <i>P. gingivalis</i> 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 <i>P. gingivalis</i>.https://www.mdpi.com/2076-0817/11/9/982cortisolsurface translocation<i>Porphyromonas gingivalis</i>T9SS
spellingShingle Hey-Min Kim
Christina Magda Rothenberger
Mary Ellen Davey
Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
Pathogens
cortisol
surface translocation
<i>Porphyromonas gingivalis</i>
T9SS
title Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
title_full Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
title_fullStr Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
title_full_unstemmed Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
title_short Cortisol Promotes Surface Translocation of <i>Porphyromonas gingivalis</i>
title_sort cortisol promotes surface translocation of i porphyromonas gingivalis i
topic cortisol
surface translocation
<i>Porphyromonas gingivalis</i>
T9SS
url https://www.mdpi.com/2076-0817/11/9/982
work_keys_str_mv AT heyminkim cortisolpromotessurfacetranslocationofiporphyromonasgingivalisi
AT christinamagdarothenberger cortisolpromotessurfacetranslocationofiporphyromonasgingivalisi
AT maryellendavey cortisolpromotessurfacetranslocationofiporphyromonasgingivalisi