Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.

Sporotrichosis is a subcutaneous mycosis caused by pathogenic species of the Sporothrix genus. A new emerging species, Sporothrix brasiliensis, is related to cat-transmitted sporotrichosis and has severe clinical manifestations. The cell wall of pathogenic fungi is a unique structure and impacts dir...

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Main Authors: Leila M Lopes-Bezerra, Louise A Walker, Gustavo Niño-Vega, Héctor M Mora-Montes, Gabriela W P Neves, Hector Villalobos-Duno, Laura Barreto, Karina Garcia, Bernardo Franco, José A Martínez-Álvarez, Carol A Munro, Neil A R Gow
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-03-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0006169
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spelling doaj-1b33ae0f297443c6899c14afbdd036452021-03-03T08:30:23ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352018-03-01123e000616910.1371/journal.pntd.0006169Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.Leila M Lopes-BezerraLouise A WalkerGustavo Niño-VegaHéctor M Mora-MontesGabriela W P NevesHector Villalobos-DunoLaura BarretoKarina GarciaBernardo FrancoJosé A Martínez-ÁlvarezCarol A MunroNeil A R GowSporotrichosis is a subcutaneous mycosis caused by pathogenic species of the Sporothrix genus. A new emerging species, Sporothrix brasiliensis, is related to cat-transmitted sporotrichosis and has severe clinical manifestations. The cell wall of pathogenic fungi is a unique structure and impacts directly on the host immune response. We reveal and compare the cell wall structures of Sporothrix schenckii and S. brasiliensis using high-pressure freezing electron microscopy to study the cell wall organization of both species. To analyze the components of the cell wall, we also used infrared and 13C and 1H NMR spectroscopy and the sugar composition was determined by quantitative high-performance anion-exchange chromatography. Our ultrastructural data revealed a bi-layered cell wall structure for both species, including an external microfibrillar layer and an inner electron-dense layer. The inner and outer layers of the S. brasiliensis cell wall were thicker than those of S. schenckii, correlating with an increase in the chitin and rhamnose contents. Moreover, the outer microfibrillar layer of the S. brasiliensis cell wall had longer microfibrils interconnecting yeast cells. Distinct from those of other dimorphic fungi, the cell wall of Sporothrix spp. lacked α-glucan component. Interestingly, glycogen α-particles were identified in the cytoplasm close to the cell wall and the plasma membrane. The cell wall structure as well as the presence of glycogen α-particles varied over time during cell culture. The structural differences observed in the cell wall of these Sporothrix species seemed to impact its uptake by monocyte-derived human macrophages. The data presented here show a unique cell wall structure of S. brasiliensis and S. schenckii during the yeast parasitic phase. A new cell wall model for Sporothrix spp. is therefore proposed that suggests that these fungi molt sheets of intact cell wall layers. This observation may have significant effects on localized and disseminated immunopathology.https://doi.org/10.1371/journal.pntd.0006169
collection DOAJ
language English
format Article
sources DOAJ
author Leila M Lopes-Bezerra
Louise A Walker
Gustavo Niño-Vega
Héctor M Mora-Montes
Gabriela W P Neves
Hector Villalobos-Duno
Laura Barreto
Karina Garcia
Bernardo Franco
José A Martínez-Álvarez
Carol A Munro
Neil A R Gow
spellingShingle Leila M Lopes-Bezerra
Louise A Walker
Gustavo Niño-Vega
Héctor M Mora-Montes
Gabriela W P Neves
Hector Villalobos-Duno
Laura Barreto
Karina Garcia
Bernardo Franco
José A Martínez-Álvarez
Carol A Munro
Neil A R Gow
Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
PLoS Neglected Tropical Diseases
author_facet Leila M Lopes-Bezerra
Louise A Walker
Gustavo Niño-Vega
Héctor M Mora-Montes
Gabriela W P Neves
Hector Villalobos-Duno
Laura Barreto
Karina Garcia
Bernardo Franco
José A Martínez-Álvarez
Carol A Munro
Neil A R Gow
author_sort Leila M Lopes-Bezerra
title Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
title_short Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
title_full Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
title_fullStr Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
title_full_unstemmed Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
title_sort cell walls of the dimorphic fungal pathogens sporothrix schenckii and sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers.
publisher Public Library of Science (PLoS)
series PLoS Neglected Tropical Diseases
issn 1935-2727
1935-2735
publishDate 2018-03-01
description Sporotrichosis is a subcutaneous mycosis caused by pathogenic species of the Sporothrix genus. A new emerging species, Sporothrix brasiliensis, is related to cat-transmitted sporotrichosis and has severe clinical manifestations. The cell wall of pathogenic fungi is a unique structure and impacts directly on the host immune response. We reveal and compare the cell wall structures of Sporothrix schenckii and S. brasiliensis using high-pressure freezing electron microscopy to study the cell wall organization of both species. To analyze the components of the cell wall, we also used infrared and 13C and 1H NMR spectroscopy and the sugar composition was determined by quantitative high-performance anion-exchange chromatography. Our ultrastructural data revealed a bi-layered cell wall structure for both species, including an external microfibrillar layer and an inner electron-dense layer. The inner and outer layers of the S. brasiliensis cell wall were thicker than those of S. schenckii, correlating with an increase in the chitin and rhamnose contents. Moreover, the outer microfibrillar layer of the S. brasiliensis cell wall had longer microfibrils interconnecting yeast cells. Distinct from those of other dimorphic fungi, the cell wall of Sporothrix spp. lacked α-glucan component. Interestingly, glycogen α-particles were identified in the cytoplasm close to the cell wall and the plasma membrane. The cell wall structure as well as the presence of glycogen α-particles varied over time during cell culture. The structural differences observed in the cell wall of these Sporothrix species seemed to impact its uptake by monocyte-derived human macrophages. The data presented here show a unique cell wall structure of S. brasiliensis and S. schenckii during the yeast parasitic phase. A new cell wall model for Sporothrix spp. is therefore proposed that suggests that these fungi molt sheets of intact cell wall layers. This observation may have significant effects on localized and disseminated immunopathology.
url https://doi.org/10.1371/journal.pntd.0006169
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