Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism

Background: Infections caused by Candida species and Staphylococcus aureus are associated with biofilm formation. C. albicans–S. aureus interactions are synergistic due to the significant increase in mixed biofilms and improved resistance to vancomycin of S. aureus. C. glabrata and S. aureus both ar...

Full description

Bibliographic Details
Main Authors: Omar Camarillo-Márquez, Itzel M. Córdova-Alcántara, Cesar H. Hernández-Rodríguez, Blanca E. García-Pérez, María A. Martínez-Rivera, Aida V. Rodríguez-Tovar
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02031/full
id doaj-68d8af756e5745bea743d33aa9a3c9c6
record_format Article
spelling doaj-68d8af756e5745bea743d33aa9a3c9c62020-11-25T00:55:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-08-01910.3389/fmicb.2018.02031398664Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic MechanismOmar Camarillo-Márquez0Itzel M. Córdova-Alcántara1Cesar H. Hernández-Rodríguez2Blanca E. García-Pérez3María A. Martínez-Rivera4Aida V. Rodríguez-Tovar5Laboratorio de Micología Médica, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratorio de Micología Médica, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratorio de Biología Molecular de Bacterias y Levaduras, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratorio de Microbiología General, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratorio de Micología Médica, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratorio de Micología Médica, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoBackground: Infections caused by Candida species and Staphylococcus aureus are associated with biofilm formation. C. albicans–S. aureus interactions are synergistic due to the significant increase in mixed biofilms and improved resistance to vancomycin of S. aureus. C. glabrata and S. aureus both are nosocomial pathogens that cause opportunistic infections in similar host niches. However, there is scarce information concerning the interaction between these last microorganisms.Results: The relationship between C. glabrata and S. aureus was evaluated by estimating the viability of both microorganisms in co-culture of planktonic cells and in single and mixed biofilms. An antagonistic behavior of S. aureus and their cell-free bacterial supernatant (CFBS) toward C. glabrata, both in planktonic form and in biofilms, was demonstrated. Scanning electron microscopy (SEM), transmission electron microscopy (TEM), and confocal laser scanning microscopy (CLSM) images showed yeast cells surrounded by bacteria, alterations in intracytoplasmic membranes, and non-viable blastoconidia with intact cell walls. Concomitantly, S. aureus cells remained viable and unaltered. The antagonistic activity of S. aureus toward C. glabrata was not due to cell-to-cell contact but the presence of CFBS, which causes a significant decrement in yeast viability and the formation of numerous lipid droplets (LDs), reactive oxygen species (ROS) accumulation, as well as nuclear alterations, and DNA fragmentation indicating the induction of an apoptotic mechanism.Conclusion: Our results demonstrate that the S. aureus CFBS causes cell death in C. glabrata by an apoptotic mechanism.https://www.frontiersin.org/article/10.3389/fmicb.2018.02031/fullmixed biofilmCandida glabrataStaphylococcus aureusantagonist interactioncell-free bacterial supernatantapoptosis
collection DOAJ
language English
format Article
sources DOAJ
author Omar Camarillo-Márquez
Itzel M. Córdova-Alcántara
Cesar H. Hernández-Rodríguez
Blanca E. García-Pérez
María A. Martínez-Rivera
Aida V. Rodríguez-Tovar
spellingShingle Omar Camarillo-Márquez
Itzel M. Córdova-Alcántara
Cesar H. Hernández-Rodríguez
Blanca E. García-Pérez
María A. Martínez-Rivera
Aida V. Rodríguez-Tovar
Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
Frontiers in Microbiology
mixed biofilm
Candida glabrata
Staphylococcus aureus
antagonist interaction
cell-free bacterial supernatant
apoptosis
author_facet Omar Camarillo-Márquez
Itzel M. Córdova-Alcántara
Cesar H. Hernández-Rodríguez
Blanca E. García-Pérez
María A. Martínez-Rivera
Aida V. Rodríguez-Tovar
author_sort Omar Camarillo-Márquez
title Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
title_short Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
title_full Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
title_fullStr Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
title_full_unstemmed Antagonistic Interaction of Staphylococcus aureus Toward Candida glabrata During in vitro Biofilm Formation Is Caused by an Apoptotic Mechanism
title_sort antagonistic interaction of staphylococcus aureus toward candida glabrata during in vitro biofilm formation is caused by an apoptotic mechanism
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-08-01
description Background: Infections caused by Candida species and Staphylococcus aureus are associated with biofilm formation. C. albicans–S. aureus interactions are synergistic due to the significant increase in mixed biofilms and improved resistance to vancomycin of S. aureus. C. glabrata and S. aureus both are nosocomial pathogens that cause opportunistic infections in similar host niches. However, there is scarce information concerning the interaction between these last microorganisms.Results: The relationship between C. glabrata and S. aureus was evaluated by estimating the viability of both microorganisms in co-culture of planktonic cells and in single and mixed biofilms. An antagonistic behavior of S. aureus and their cell-free bacterial supernatant (CFBS) toward C. glabrata, both in planktonic form and in biofilms, was demonstrated. Scanning electron microscopy (SEM), transmission electron microscopy (TEM), and confocal laser scanning microscopy (CLSM) images showed yeast cells surrounded by bacteria, alterations in intracytoplasmic membranes, and non-viable blastoconidia with intact cell walls. Concomitantly, S. aureus cells remained viable and unaltered. The antagonistic activity of S. aureus toward C. glabrata was not due to cell-to-cell contact but the presence of CFBS, which causes a significant decrement in yeast viability and the formation of numerous lipid droplets (LDs), reactive oxygen species (ROS) accumulation, as well as nuclear alterations, and DNA fragmentation indicating the induction of an apoptotic mechanism.Conclusion: Our results demonstrate that the S. aureus CFBS causes cell death in C. glabrata by an apoptotic mechanism.
topic mixed biofilm
Candida glabrata
Staphylococcus aureus
antagonist interaction
cell-free bacterial supernatant
apoptosis
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02031/full
work_keys_str_mv AT omarcamarillomarquez antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
AT itzelmcordovaalcantara antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
AT cesarhhernandezrodriguez antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
AT blancaegarciaperez antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
AT mariaamartinezrivera antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
AT aidavrodrigueztovar antagonisticinteractionofstaphylococcusaureustowardcandidaglabrataduringinvitrobiofilmformationiscausedbyanapoptoticmechanism
_version_ 1725230258955747328