Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events

Cryptococcus neoformans is a fungal pathogen that causes life-threatening infections in immunocompromised individuals. It is surrounded by three concentric structures that separate the cell from the extracellular space: the plasma membrane, the cell wall and the polysaccharide (PS) capsule. Although...

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Main Authors: Glauber R. de S. Araújo, Carolina de L. Alcantara, Noêmia Rodrigues, Wanderley de Souza, Bruno Pontes, Susana Frases
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.609244/full
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author Glauber R. de S. Araújo
Glauber R. de S. Araújo
Carolina de L. Alcantara
Noêmia Rodrigues
Wanderley de Souza
Wanderley de Souza
Bruno Pontes
Bruno Pontes
Susana Frases
Susana Frases
author_facet Glauber R. de S. Araújo
Glauber R. de S. Araújo
Carolina de L. Alcantara
Noêmia Rodrigues
Wanderley de Souza
Wanderley de Souza
Bruno Pontes
Bruno Pontes
Susana Frases
Susana Frases
author_sort Glauber R. de S. Araújo
collection DOAJ
description Cryptococcus neoformans is a fungal pathogen that causes life-threatening infections in immunocompromised individuals. It is surrounded by three concentric structures that separate the cell from the extracellular space: the plasma membrane, the cell wall and the polysaccharide (PS) capsule. Although several studies have revealed the chemical composition of these structures, little is known about their ultrastructural organization and remodeling during C. neoformans budding events. Here, by combining the latest and most accurate light and electron microscopy techniques, we describe the morphological remodeling that occurs among the capsule, cell wall and plasma membrane during budding in C. neoformans. Our results show that the cell wall deforms to generate a specialized region at one of the cell’s poles. This region subsequently begins to break into layers that are slightly separated from each other and with thick tips. We also observe a reorganization of the capsular PS around the specialized regions. While daughter cells present their PS fibers aligned in the direction of budding, mother cells show a similar pattern but in the opposite direction. Also, daughter cells form multilamellar membrane structures covering the continuous opening between both cells. Together, our findings provide compelling ultrastructural evidence for C. neoformans surface remodeling during budding, which may have important implications for future studies exploring these remodeled specialized regions as drug-targets against cryptococcosis.
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spelling doaj.art-50cfa6ed1b8c457982b0ec66ea5dc9d82022-12-21T23:01:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-03-011210.3389/fmicb.2021.609244609244Ultrastructural Study of Cryptococcus neoformans Surface During Budding EventsGlauber R. de S. Araújo0Glauber R. de S. Araújo1Carolina de L. Alcantara2Noêmia Rodrigues3Wanderley de Souza4Wanderley de Souza5Bruno Pontes6Bruno Pontes7Susana Frases8Susana Frases9Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Biofísica de Fungos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilCentro Nacional de Biologia Estrutural e Bioimagem (CENABIO), Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilCentro Nacional de Biologia Estrutural e Bioimagem (CENABIO), Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Pinças Óticas (LPO-COPEA), Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Biofísica de Fungos, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, BrazilCryptococcus neoformans is a fungal pathogen that causes life-threatening infections in immunocompromised individuals. It is surrounded by three concentric structures that separate the cell from the extracellular space: the plasma membrane, the cell wall and the polysaccharide (PS) capsule. Although several studies have revealed the chemical composition of these structures, little is known about their ultrastructural organization and remodeling during C. neoformans budding events. Here, by combining the latest and most accurate light and electron microscopy techniques, we describe the morphological remodeling that occurs among the capsule, cell wall and plasma membrane during budding in C. neoformans. Our results show that the cell wall deforms to generate a specialized region at one of the cell’s poles. This region subsequently begins to break into layers that are slightly separated from each other and with thick tips. We also observe a reorganization of the capsular PS around the specialized regions. While daughter cells present their PS fibers aligned in the direction of budding, mother cells show a similar pattern but in the opposite direction. Also, daughter cells form multilamellar membrane structures covering the continuous opening between both cells. Together, our findings provide compelling ultrastructural evidence for C. neoformans surface remodeling during budding, which may have important implications for future studies exploring these remodeled specialized regions as drug-targets against cryptococcosis.https://www.frontiersin.org/articles/10.3389/fmicb.2021.609244/fullCryptococcus neoformanspolysaccharide capsulecell wallbuddingelectron microscopy
spellingShingle Glauber R. de S. Araújo
Glauber R. de S. Araújo
Carolina de L. Alcantara
Noêmia Rodrigues
Wanderley de Souza
Wanderley de Souza
Bruno Pontes
Bruno Pontes
Susana Frases
Susana Frases
Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
Frontiers in Microbiology
Cryptococcus neoformans
polysaccharide capsule
cell wall
budding
electron microscopy
title Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
title_full Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
title_fullStr Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
title_full_unstemmed Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
title_short Ultrastructural Study of Cryptococcus neoformans Surface During Budding Events
title_sort ultrastructural study of cryptococcus neoformans surface during budding events
topic Cryptococcus neoformans
polysaccharide capsule
cell wall
budding
electron microscopy
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.609244/full
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