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

Leila M Lopes Bezerra (Corresponding Author), Louise A Walker, Gustavo Niño Vega, Héctor M. MoraMontes, Gabriela W P Neves, Hector Villalobos-Duno, Laura Barreto, Karina Garcia, Bernardo Franco, José A. Martínez-Álvarez, Carol A Munro, Neil A R Gow

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Abstract

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 s. str., 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.
Original languageEnglish
Article numbere0006169
JournalPLoS Neglected Tropical Diseases
Volume12
Issue number3
DOIs
Publication statusPublished - 9 Mar 2018

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Sporothrix
Cell Wall
Sporotrichosis
Fungi
Glycogen
Yeasts
Microfibrils
Rhamnose
Chitin
Glucans
Mycoses

Keywords

  • cell wall
  • dimorphic fungi
  • Sporothrix brasiliensis
  • Sporothrix schenckii
  • peptidorhamnomannan
  • beta-glucan
  • chitin
  • glycogen alpha particle
  • human macrophage
  • cell surface

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Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers. / Lopes Bezerra, Leila M (Corresponding Author); Walker, Louise A; Vega, Gustavo Niño ; MoraMontes, Héctor M. ; Neves, Gabriela W P ; Villalobos-Duno, Hector ; Barreto, Laura ; Garcia, Karina ; Franco, Bernardo; Martínez-Álvarez, José A.; Munro, Carol A; Gow, Neil A R.

In: PLoS Neglected Tropical Diseases, Vol. 12, No. 3, e0006169, 09.03.2018.

Research output: Contribution to journalArticle

Lopes Bezerra, Leila M ; Walker, Louise A ; Vega, Gustavo Niño ; MoraMontes, Héctor M. ; Neves, Gabriela W P ; Villalobos-Duno, Hector ; Barreto, Laura ; Garcia, Karina ; Franco, Bernardo ; Martínez-Álvarez, José A. ; Munro, Carol A ; Gow, Neil A R. / Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers. In: PLoS Neglected Tropical Diseases. 2018 ; Vol. 12, No. 3.
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title = "Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers",
abstract = "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 s. str., 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.",
keywords = "cell wall, dimorphic fungi, Sporothrix brasiliensis , Sporothrix schenckii, peptidorhamnomannan, beta-glucan, chitin, glycogen alpha particle, human macrophage, cell surface",
author = "{Lopes Bezerra}, {Leila M} and Walker, {Louise A} and Vega, {Gustavo Ni{\~n}o} and MoraMontes, {H{\'e}ctor M.} and Neves, {Gabriela W P} and Hector Villalobos-Duno and Laura Barreto and Karina Garcia and Bernardo Franco and Mart{\'i}nez-{\'A}lvarez, {Jos{\'e} A.} and Munro, {Carol A} and Gow, {Neil A R}",
note = "This work was supported by the Funda{\cc}{\~a}o Carlos Chagas de Amparo {\`a} Pesquisa do Estado do Rio de Janeiro (FAPERJ), grants E-26/202.974/2015 and Conselho Nacional de Desenvolvimento Cient{\'i}fico e Tecnol{\'o}gico (CNPq), grants 229755/2013-5, Brazil. LMLB is a senior research fellow of CNPq and Faperj. NG acknowledged support from the Wellcome Trust (Trust (097377, 101873, 200208) and MRC Centre for Medical Mycology (MR/N006364/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.",
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T1 - Cell walls of the dimorphic fungal pathogens Sporothrix schenckii and Sporothrix brasiliensis exhibit bilaminate structures and sloughing of extensive and intact layers

AU - Lopes Bezerra, Leila M

AU - Walker, Louise A

AU - Vega, Gustavo Niño

AU - MoraMontes, Héctor M.

AU - Neves, Gabriela W P

AU - Villalobos-Duno, Hector

AU - Barreto, Laura

AU - Garcia, Karina

AU - Franco, Bernardo

AU - Martínez-Álvarez, José A.

AU - Munro, Carol A

AU - Gow, Neil A R

N1 - This work was supported by the Fundação Carlos Chagas de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), grants E-26/202.974/2015 and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grants 229755/2013-5, Brazil. LMLB is a senior research fellow of CNPq and Faperj. NG acknowledged support from the Wellcome Trust (Trust (097377, 101873, 200208) and MRC Centre for Medical Mycology (MR/N006364/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

PY - 2018/3/9

Y1 - 2018/3/9

N2 - 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 s. str., 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.

AB - 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 s. str., 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.

KW - cell wall

KW - dimorphic fungi

KW - Sporothrix brasiliensis

KW - Sporothrix schenckii

KW - peptidorhamnomannan

KW - beta-glucan

KW - chitin

KW - glycogen alpha particle

KW - human macrophage

KW - cell surface

U2 - 10.1371/journal.pntd.0006169

DO - 10.1371/journal.pntd.0006169

M3 - Article

VL - 12

JO - PLoS Neglected Tropical Diseases

JF - PLoS Neglected Tropical Diseases

SN - 1935-2735

IS - 3

M1 - e0006169

ER -