Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages

ABSTRACT Phagocytic cells are crucial components of the innate immune system preventing Candida albicans mucosal infections. Streptococcus gordonii and Pseudomonas aeruginosa often colonize mucosal sites, along with C. albicans, and yet interkingdom interactions that might alter the survival and esc...

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Autores principales:	Ornella Salvatori, Rohitashw Kumar, Sarah Metcalfe, Margaret Vickerman, Jason G. Kay, Mira Edgerton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Candida albicans Pseudomonas aeruginosa Streptococcus gordonii hyphal development macrophages microcolonies Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e195b446f71d495cb64c07b85aa29426
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spelling	oai:doaj.org-article:e195b446f71d495cb64c07b85aa294262021-11-15T15:30:51ZBacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages10.1128/mSphere.00689-202379-5042https://doaj.org/article/e195b446f71d495cb64c07b85aa294262020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00689-20https://doaj.org/toc/2379-5042ABSTRACT Phagocytic cells are crucial components of the innate immune system preventing Candida albicans mucosal infections. Streptococcus gordonii and Pseudomonas aeruginosa often colonize mucosal sites, along with C. albicans, and yet interkingdom interactions that might alter the survival and escape of fungi from macrophages are not understood. Murine macrophages were coinfected with S. gordonii or P. aeruginosa, along with C. albicans to evaluate changes in fungal survival. S. gordonii increased C. albicans survival and filamentation within macrophage phagosomes, while P. aeruginosa reduced fungal survival and filamentation. Coinfection with S. gordonii resulted in greater escape of C. albicans from macrophages and increased size of fungal microcolonies formed on macrophage monolayers, while coinfection with P. aeruginosa reduced macrophage escape and produced smaller microcolonies. Microcolonies formed in the presence of P. aeruginosa cells outside macrophages also had significantly reduced size that was not found with P. aeruginosa phenazine deletion mutants. S. gordonii cells, as well as S. gordonii heat-fixed culture supernatants, increased C. albicans microcolony biomass but also resulted in microcolony detachment. A heat-resistant, trypsin-sensitive pheromone processed by S. gordonii Eep was needed for these effects. The majority of fungal microcolonies formed on human epithelial monolayers with S. gordonii supernatants developed as large floating structures with no detectable invasion of epithelium, along with reduced gene expression of C. albicans HYR1, EAP1, and HWP2 adhesins. However, a subset of C. albicans microcolonies was smaller and had greater epithelial invasiveness compared to microcolonies grown without S. gordonii. Thus, bacteria can alter the killing and escape of C. albicans from macrophages and contribute to changes in C. albicans pathogenicity. IMPORTANCE Candida albicans is the predominant fungus colonizing the oral cavity that can have both synergistic and antagonistic interactions with other bacteria. Interkingdom polymicrobial associations modify fungal pathogenicity and are believed to increase microbial resistance to innate immunity. However, it is not known how these interactions alter fungal survival during phagocytic killing. We demonstrated that secreted molecules of S. gordonii and P. aeruginosa alter C. albicans survival within the phagosome of macrophages and alter fungal pathogenic phenotypes, including filamentation and microcolony formation. Moreover, we provide evidence for a dual interaction between S. gordonii and C. albicans such that S. gordonii signaling peptides can promote C. albicans commensalism by decreasing microcolony attachment while increasing invasion in epithelial cells. Our results identify bacterial diffusible factors as an attractive target to modify virulence of C. albicans in polymicrobial infections.Ornella SalvatoriRohitashw KumarSarah MetcalfeMargaret VickermanJason G. KayMira EdgertonAmerican Society for MicrobiologyarticleCandida albicansPseudomonas aeruginosaStreptococcus gordoniihyphal developmentmacrophagesmicrocoloniesMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Candida albicans Pseudomonas aeruginosa Streptococcus gordonii hyphal development macrophages microcolonies Microbiology QR1-502
spellingShingle	Candida albicans Pseudomonas aeruginosa Streptococcus gordonii hyphal development macrophages microcolonies Microbiology QR1-502 Ornella Salvatori Rohitashw Kumar Sarah Metcalfe Margaret Vickerman Jason G. Kay Mira Edgerton Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
description	ABSTRACT Phagocytic cells are crucial components of the innate immune system preventing Candida albicans mucosal infections. Streptococcus gordonii and Pseudomonas aeruginosa often colonize mucosal sites, along with C. albicans, and yet interkingdom interactions that might alter the survival and escape of fungi from macrophages are not understood. Murine macrophages were coinfected with S. gordonii or P. aeruginosa, along with C. albicans to evaluate changes in fungal survival. S. gordonii increased C. albicans survival and filamentation within macrophage phagosomes, while P. aeruginosa reduced fungal survival and filamentation. Coinfection with S. gordonii resulted in greater escape of C. albicans from macrophages and increased size of fungal microcolonies formed on macrophage monolayers, while coinfection with P. aeruginosa reduced macrophage escape and produced smaller microcolonies. Microcolonies formed in the presence of P. aeruginosa cells outside macrophages also had significantly reduced size that was not found with P. aeruginosa phenazine deletion mutants. S. gordonii cells, as well as S. gordonii heat-fixed culture supernatants, increased C. albicans microcolony biomass but also resulted in microcolony detachment. A heat-resistant, trypsin-sensitive pheromone processed by S. gordonii Eep was needed for these effects. The majority of fungal microcolonies formed on human epithelial monolayers with S. gordonii supernatants developed as large floating structures with no detectable invasion of epithelium, along with reduced gene expression of C. albicans HYR1, EAP1, and HWP2 adhesins. However, a subset of C. albicans microcolonies was smaller and had greater epithelial invasiveness compared to microcolonies grown without S. gordonii. Thus, bacteria can alter the killing and escape of C. albicans from macrophages and contribute to changes in C. albicans pathogenicity. IMPORTANCE Candida albicans is the predominant fungus colonizing the oral cavity that can have both synergistic and antagonistic interactions with other bacteria. Interkingdom polymicrobial associations modify fungal pathogenicity and are believed to increase microbial resistance to innate immunity. However, it is not known how these interactions alter fungal survival during phagocytic killing. We demonstrated that secreted molecules of S. gordonii and P. aeruginosa alter C. albicans survival within the phagosome of macrophages and alter fungal pathogenic phenotypes, including filamentation and microcolony formation. Moreover, we provide evidence for a dual interaction between S. gordonii and C. albicans such that S. gordonii signaling peptides can promote C. albicans commensalism by decreasing microcolony attachment while increasing invasion in epithelial cells. Our results identify bacterial diffusible factors as an attractive target to modify virulence of C. albicans in polymicrobial infections.
format	article
author	Ornella Salvatori Rohitashw Kumar Sarah Metcalfe Margaret Vickerman Jason G. Kay Mira Edgerton
author_facet	Ornella Salvatori Rohitashw Kumar Sarah Metcalfe Margaret Vickerman Jason G. Kay Mira Edgerton
author_sort	Ornella Salvatori
title	Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
title_short	Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
title_full	Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
title_fullStr	Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
title_full_unstemmed	Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages
title_sort	bacteria modify <italic toggle="yes">candida albicans</italic> hypha formation, microcolony properties, and survival within macrophages
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/e195b446f71d495cb64c07b85aa29426
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Bacteria Modify <italic toggle="yes">Candida albicans</italic> Hypha Formation, Microcolony Properties, and Survival within Macrophages

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