Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro

ABSTRACT Vulvovaginal candidiasis (VVC) is a common clinical condition with symptoms and signs of vaginal inflammation in the presence of Candida species. At least one episode of VVC is experienced in up to 75% of women in the reproductive age group during their lifetime, and 5% to 8% of such women...

Full description

Bibliographic Details
Main Authors: Luca Spaggiari, Arianna Sala, Andrea Ardizzoni, Francesco De Seta, Dhirendra Kumar Singh, Attila Gacser, Elisabetta Blasi, Eva Pericolini
Format: Article
Language:English
Published: American Society for Microbiology 2022-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02696-21
_version_ 1828833225420570624
author Luca Spaggiari
Arianna Sala
Andrea Ardizzoni
Francesco De Seta
Dhirendra Kumar Singh
Attila Gacser
Elisabetta Blasi
Eva Pericolini
author_facet Luca Spaggiari
Arianna Sala
Andrea Ardizzoni
Francesco De Seta
Dhirendra Kumar Singh
Attila Gacser
Elisabetta Blasi
Eva Pericolini
author_sort Luca Spaggiari
collection DOAJ
description ABSTRACT Vulvovaginal candidiasis (VVC) is a common clinical condition with symptoms and signs of vaginal inflammation in the presence of Candida species. At least one episode of VVC is experienced in up to 75% of women in the reproductive age group during their lifetime, and 5% to 8% of such women suffer from the chronic form. Most cases of VVC are still caused by C. albicans. However, the incidence of VVC cases by non-albicans Candida (NAC) species, such as C. parapsilosis, is continuously increasing. Despite the prevalence of VVC from NAC, little is known about these species and almost nothing about the mechanisms that trigger the VVC. Lactobacillus spp. are the most widely before represented microorganisms in the vaginal microbiota of healthy women. Here, cell-free supernatants (CFS) obtained from L. acidophilus, L. plantarum, L. rhamnosus, and L. reuteri were assessed for their effect on C. parapsilosis virulence traits. Moreover, we assessed if such an effect persisted even after the removal of the CFS (CFS preincubation effect). Moreover, a transwell coculture system was employed by which the relevant antifungal effect was shown to be attributable to the compounds released by lactobacilli. Our results suggest that lactobacilli can work (i) by reducing C. parapsilosis virulence traits, as indicated by the reduced fungal proliferation, viability, and metabolic activity, and (ii) by improving epithelial resistance to the fungus. Overall, these data suggest that, in the context of the vaginal microbiota, the lactobacilli may play a role in preventing the onset of mucosal C. parapsilosis infection. IMPORTANCE The incidence of VVC by non-albicans Candida (NAC) species, such as C. parapsilosis, is increasing. Treatment failure is common in NAC-VVC because some species are resistant or poorly susceptible to the antifungal agents normally employed. Research on C. parapsilosis’s pathogenic mechanisms and alternative treatments are still lacking. C. albicans triggers the VVC by producing hyphae, which favor the loss of epithelial tolerance. Differently, C. parapsilosis only produces pseudohyphae. Hence, different virulence factors may trigger the VVC. Likewise, the therapeutic options could also involve different fungal targets. Substantial in vitro and in vivo studies on the pathogenicity mechanisms of C. parapsilosis are lacking. The data presented here ascribe a novel beneficial role to different Lactobacillus spp., whose CFS provides a postbiotic-like activity against C. parapsilosis. Further studies are needed to unravel the mechanisms involved in the bioactivities of such compounds, to better understand the role of single postbiotics in the CFS.
first_indexed 2024-12-12T17:13:50Z
format Article
id doaj.art-ded1913876d54f2284431d959fe17f3f
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-12-12T17:13:50Z
publishDate 2022-06-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-ded1913876d54f2284431d959fe17f3f2022-12-22T00:17:50ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.02696-21Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In VitroLuca Spaggiari0Arianna Sala1Andrea Ardizzoni2Francesco De Seta3Dhirendra Kumar Singh4Attila Gacser5Elisabetta Blasi6Eva Pericolini7Clinical and Experimental Medicine Ph.D. Program, University of Modena and Reggio Emilia, Modena, ItalyDepartment of Surgical, Medical, Dental, and Morphological Sciences with Interest in Transplant, Oncological and Regenerative Medicine, University of Modena and Reggio Emilia, Modena, ItalyDepartment of Surgical, Medical, Dental, and Morphological Sciences with Interest in Transplant, Oncological and Regenerative Medicine, University of Modena and Reggio Emilia, Modena, ItalyDepartment of Medical Sciences, University of Trieste, Institute for Maternal and Child Health- Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), Burlo Garofolo, Trieste, ItalyHungarian Centre of Excellence for Molecular Medicine (HCEMM) - University of Szeged (USZ) Fungal Pathogens Research Group, Department of Microbiology, University of Szeged, Szeged, HungaryHungarian Centre of Excellence for Molecular Medicine (HCEMM) - University of Szeged (USZ) Fungal Pathogens Research Group, Department of Microbiology, University of Szeged, Szeged, HungaryDepartment of Surgical, Medical, Dental, and Morphological Sciences with Interest in Transplant, Oncological and Regenerative Medicine, University of Modena and Reggio Emilia, Modena, ItalyDepartment of Surgical, Medical, Dental, and Morphological Sciences with Interest in Transplant, Oncological and Regenerative Medicine, University of Modena and Reggio Emilia, Modena, ItalyABSTRACT Vulvovaginal candidiasis (VVC) is a common clinical condition with symptoms and signs of vaginal inflammation in the presence of Candida species. At least one episode of VVC is experienced in up to 75% of women in the reproductive age group during their lifetime, and 5% to 8% of such women suffer from the chronic form. Most cases of VVC are still caused by C. albicans. However, the incidence of VVC cases by non-albicans Candida (NAC) species, such as C. parapsilosis, is continuously increasing. Despite the prevalence of VVC from NAC, little is known about these species and almost nothing about the mechanisms that trigger the VVC. Lactobacillus spp. are the most widely before represented microorganisms in the vaginal microbiota of healthy women. Here, cell-free supernatants (CFS) obtained from L. acidophilus, L. plantarum, L. rhamnosus, and L. reuteri were assessed for their effect on C. parapsilosis virulence traits. Moreover, we assessed if such an effect persisted even after the removal of the CFS (CFS preincubation effect). Moreover, a transwell coculture system was employed by which the relevant antifungal effect was shown to be attributable to the compounds released by lactobacilli. Our results suggest that lactobacilli can work (i) by reducing C. parapsilosis virulence traits, as indicated by the reduced fungal proliferation, viability, and metabolic activity, and (ii) by improving epithelial resistance to the fungus. Overall, these data suggest that, in the context of the vaginal microbiota, the lactobacilli may play a role in preventing the onset of mucosal C. parapsilosis infection. IMPORTANCE The incidence of VVC by non-albicans Candida (NAC) species, such as C. parapsilosis, is increasing. Treatment failure is common in NAC-VVC because some species are resistant or poorly susceptible to the antifungal agents normally employed. Research on C. parapsilosis’s pathogenic mechanisms and alternative treatments are still lacking. C. albicans triggers the VVC by producing hyphae, which favor the loss of epithelial tolerance. Differently, C. parapsilosis only produces pseudohyphae. Hence, different virulence factors may trigger the VVC. Likewise, the therapeutic options could also involve different fungal targets. Substantial in vitro and in vivo studies on the pathogenicity mechanisms of C. parapsilosis are lacking. The data presented here ascribe a novel beneficial role to different Lactobacillus spp., whose CFS provides a postbiotic-like activity against C. parapsilosis. Further studies are needed to unravel the mechanisms involved in the bioactivities of such compounds, to better understand the role of single postbiotics in the CFS.https://journals.asm.org/doi/10.1128/spectrum.02696-21C. parapsilosisVVCpostbiotic-like activitycell-free-supernatantsCFSCandida
spellingShingle Luca Spaggiari
Arianna Sala
Andrea Ardizzoni
Francesco De Seta
Dhirendra Kumar Singh
Attila Gacser
Elisabetta Blasi
Eva Pericolini
Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
Microbiology Spectrum
C. parapsilosis
VVC
postbiotic-like activity
cell-free-supernatants
CFS
Candida
title Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
title_full Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
title_fullStr Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
title_full_unstemmed Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
title_short Lactobacillus acidophilus, L. plantarum, L. rhamnosus, and L. reuteri Cell-Free Supernatants Inhibit Candida parapsilosis Pathogenic Potential upon Infection of Vaginal Epithelial Cells Monolayer and in a Transwell Coculture System In Vitro
title_sort lactobacillus acidophilus l plantarum l rhamnosus and l reuteri cell free supernatants inhibit candida parapsilosis pathogenic potential upon infection of vaginal epithelial cells monolayer and in a transwell coculture system in vitro
topic C. parapsilosis
VVC
postbiotic-like activity
cell-free-supernatants
CFS
Candida
url https://journals.asm.org/doi/10.1128/spectrum.02696-21
work_keys_str_mv AT lucaspaggiari lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT ariannasala lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT andreaardizzoni lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT francescodeseta lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT dhirendrakumarsingh lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT attilagacser lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT elisabettablasi lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro
AT evapericolini lactobacillusacidophiluslplantarumlrhamnosusandlreutericellfreesupernatantsinhibitcandidaparapsilosispathogenicpotentialuponinfectionofvaginalepithelialcellsmonolayerandinatranswellcoculturesysteminvitro