Extracellular Vesicles Regulate Biofilm Formation and Yeast-to-Hypha Differentiation in Candida albicans

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ABSTRACT

In this study, we investigated the influence of fungal extracellular vesicles (EVs) during biofilm formation and morphogenesis in Candida albicans. Using crystal violet staining and scanning electron microscopy (SEM), we demonstrated that C. albicans EVs inhibited biofilm formation in vitro. By time-lapse microscopy and SEM, we showed that C. albicans EV treatment stopped filamentation and promoted pseudohyphae formation with multiple budding sites. The ability of C. albicans EVs to regulate dimorphism was further compared to EVs isolated from different C. albicans strains, Saccharomyces cerevisiae, and Histoplasma capsulatum. C. albicans EVs from distinct strains inhibited yeast-to-hyphae differentiation with morphological changes occurring in less than 4 h. EVs from S. cerevisiae and H. capsulatum modestly reduced morphogenesis, and the effect was evident after 24 h of incubation. The inhibitory activity of C. albicans EVs on phase transition was promoted by a combination of lipid compounds, which were identified by gas chromatography-tandem mass spectrometry analysis as sesquiterpenes, diterpenes, and fatty acids. Remarkably, C. albicans EVs were also able to reverse filamentation. Finally, C. albicans cells treated with C. albicans EVs for 24 h lost their capacity to penetrate agar and were avirulent when inoculated into Galleria mellonella. Our results indicate that fungal EVs can regulate yeast-to-hypha differentiation, thereby inhibiting biofilm formation and attenuating virulence.

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Most cited references 70

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Candida albicans morphogenesis and host defence: discriminating invasion from colonization.

Neil Gow, Frank van de Veerdonk, Alistair Brown … (2011)

Candida albicans is a common fungal pathogen of humans that colonizes the skin and mucosal surfaces of most healthy individuals. Until recently, little was known about the mechanisms by which mucosal antifungal defences tolerate colonizing C. albicans but react strongly when hyphae of the same microorganism attempt to invade tissue. In this Review, we describe the properties of yeast cells and hyphae that are relevant to their interaction with the host, and the immunological mechanisms that differentially recognize colonizing versus invading C. albicans.

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Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol.

J Hornby, E. C. Jensen, A Lisec … (2001)

The inoculum size effect in the dimorphic fungus Candida albicans results from production of an extracellular quorum-sensing molecule (QSM). This molecule prevents mycelial development in both a growth morphology assay and a differentiation assay using three chemically distinct triggers for germ tube formation (GTF): L-proline, N-acetylglucosamine, and serum (either pig or fetal bovine). In all cases, the presence of QSM prevents the yeast-to-mycelium conversion, resulting in actively budding yeasts without influencing cellular growth rates. QSM exhibits general cross-reactivity within C. albicans in that supernatants from strain A72 are active on five other strains of C. albicans and vice versa. The QSM excreted by C. albicans is farnesol (C(15)H(26)O; molecular weight, 222.37). QSM is extracellular, and is produced continuously during growth and over a temperature range from 23 to 43 degrees C, in amounts roughly proportional to the CFU/milliliter. Production is not dependent on the type of carbon source nor nitrogen source or on the chemical nature of the growth medium. Both commercial mixed isomer and (E,E)-farnesol exhibited QSM activity (the ability to prevent GTF) at a level sufficient to account for all the QSM activity present in C. albicans supernatants, i.e., 50% GTF at ca. 30 to 35 microM. Nerolidol was ca. two times less active than farnesol. Neither geraniol (C(10)), geranylgeraniol (C(20)), nor farnesyl pyrophosphate had any QSM activity.

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Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport.

Marcio L Rodrigues, Leonardo Nimrichter, Débora L Oliveira … (2007)

The mechanisms by which macromolecules are transported through the cell wall of fungi are not known. A central question in the biology of Cryptococcus neoformans, the causative agent of cryptococcosis, is the mechanism by which capsular polysaccharide synthesized inside the cell is exported to the extracellular environment for capsule assembly and release. We demonstrate that C. neoformans produces extracellular vesicles during in vitro growth and animal infection. Vesicular compartments, which are transferred to the extracellular space by cell wall passage, contain glucuronoxylomannan (GXM), a component of the cryptococcal capsule, and key lipids, such as glucosylceramide and sterols. A correlation between GXM-containing vesicles and capsule expression was observed. The results imply a novel mechanism for the release of the major virulence factor of C. neoformans whereby polysaccharide packaged in lipid vesicles crosses the cell wall and the capsule network to reach the extracellular environment.

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Author and article information

Contributors

Leonardo Nimrichter:

ORCID: https://orcid.org/0000-0001-9281-6856

David R. Andes: Role: Invited Editor

Bernhard Hube: Role: Editor

Journal

Journal ID (nlm-ta): mBio

Journal ID (iso-abbrev): mBio

Journal ID (publisher-id): mbio

Title: mBio

Publisher: American Society for Microbiology (1752 N St., N.W., Washington, DC )

ISSN (Electronic): 2150-7511

Publication date (Electronic, pub): 14 April 2022

Publication date (Electronic, collection): May-Jun 2022

Publication date PMC-release: 14 April 2022

Volume: 13

Issue: 3

Electronic Location Identifier: e00301-22

Affiliations

[a ] Laboratório de Glicobiologia de Eucariotos, Departamento de Microbiologia Geral, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

[b ] Department of Biological Sciences, Border Biomedical Research Center, University of Texas at El Paso, El Paso, Texas, USA

[c ] Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filhos (IBCCF), Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

[d ] LPO-COPEA, Instituto de Ciências Biomédicas & Centro Nacional de Biologia Estrutural e Bioimagem (CENABIO), Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

[e ] Laboratório de Citotoxicidade e Genotoxicidade, Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

[f ] Laboratório de Bioquímica e Imunologia das Micoses, Departamento de Microbiologia e Parasitologia, Instituto Biomédico, Universidade Federal Fluminense, Niterói, Brazil

[g ] Department of Microbiology and Immunology, Stony Brook Universitygrid.36425.36, , Stony Brook, New York, USA

[h ] Department of Microbiology and Immunology and Division of Infectious Diseases, Stony Brook Universitygrid.36425.36, , Stony Brook, New York, USA

[i ] Veterans Affairs Medical Center, Northport, New York, USA

[j ] Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, USA

[k ] Division of Infectious Diseases, Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, USA

[l ] Instituto Carlos Chagas (ICC), Fundação Oswaldo Cruz (FIOCRUZ), Curitiba, Brazil

[m ] Centro de Desenvolvimento Tecnológico em Saúde (CDTS), Fundação Oswaldo Cruz, Rio de Janeiro, Brazil

[n ] Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

University of Wisconsin—Madison

Leibniz Institute for Natural Product Research and Infection Biology–Hans Knoell Institute Jena (HKI)

Author notes

[*]

Present address: Maria Tays Mendes, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, USA.

Leandro Honorato and Joana Feital Demetrio de Araujo contributed equally to this work. Author order was determined in agreement between both Co-first authors.

The authors declare a conflict of interest. Dr. Maurizio Del Poeta, M.D. is a Co-Founder and Chief Scientific Officer (CSO) of MicroRid Technologies Inc.

Author information

Leandro Honorato https://orcid.org/0000-0003-0370-5682

Maurizio Del Poeta https://orcid.org/0000-0001-8418-3120

Daniel Zamith-Miranda https://orcid.org/0000-0001-7532-2432

Lysangela Ronalte Alves https://orcid.org/0000-0002-1972-2658

Igor C. Almeida https://orcid.org/0000-0002-2443-8213

Leonardo Nimrichter https://orcid.org/0000-0001-9281-6856

Article

Publisher ID: 00301-22 Publisher ID: mbio.00301-22

DOI: 10.1128/mbio.00301-22

PMC ID: 9239257

PubMed ID: 35420476

SO-VID: b8171fad-7fd1-4246-a7e2-5d5ef44bea08

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

History

Date received : 10 February 2022

Date accepted : 9 March 2022

Page count

supplementary-material: 0, Figures: 8, Tables: 2, Equations: 0, References: 70, Pages: 21, Words: 14253

Funding

Funded by: MCTI | Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), FundRef https://doi.org/10.13039/501100003593;

Award ID: 311179/2017-7

Award ID: 408711/2017-7

Award Recipient : Leonardo Nimrichter

Funded by: Fundação Oswaldo Cruz (FIOCRUZ), FundRef https://doi.org/10.13039/501100006507;

Award ID: VPPCB-007-FIO-18

Award ID: VPPIS-001-FIO18

Award Recipient : Lysangela Ronalte Alves Award Recipient : Marcio Rodrigues

Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), FundRef https://doi.org/10.13039/501100002322;

Award ID: Finance Code 001

Award Recipient : Leandro Honorato Award Recipient : Joana Feital Demetrio de Araujo Award Recipient : Maria Tays Mendes

Funded by: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), FundRef https://doi.org/10.13039/501100004586;

Award ID: E-26/202.809/2018

Award Recipient : Leonardo Nimrichter

Funded by: Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), FundRef https://doi.org/10.13039/501100004586;

Award ID: E-26/202.696/2018

Award Recipient : Allan Jefferson Guimarães

Funded by: HHS | National Institutes of Health (NIH), FundRef https://doi.org/10.13039/100000002;

Award ID: AI124797

Award Recipient : Joshua D. Nosanchuk

Funded by: HHS | National Institutes of Health (NIH), FundRef https://doi.org/10.13039/100000002;

Award ID: AI136934

Award ID: AI116420

Award ID: AI125770

Award Recipient : Maurizio Del Poeta

Funded by: Merit Review Grant;

Award ID: I01BX002924

Award Recipient : Maurizio Del Poeta

Funded by: HHS | NIH | National Institute on Minority Health and Health Disparities (NIMHD), FundRef https://doi.org/10.13039/100006545;

Award ID: 5U54MD007592

Award Recipient : Robert A. Kirken (PI) Award Recipient : Igor C. Almeida (Co-I)

Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), FundRef https://doi.org/10.13039/501100002322;

Award ID: 013622/2013-07

Award Recipient : Maria Tays Mendes

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cover-date May/June 2022

ScienceOpen disciplines: Life sciences

Keywords: biofilm,candida albicans,extracellular vesicles,lipids,yeast-to-hypha inhibition

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: biofilm, candida albicans, extracellular vesicles, lipids, yeast-to-hypha inhibition

Extracellular Vesicles Regulate Biofilm Formation and Yeast-to-Hypha Differentiation in Candida albicans

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ABSTRACT

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Bacterial extracellular vesicles

Most cited references 70

Candida albicans morphogenesis and host defence: discriminating invasion from colonization.

Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol.

Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport.

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