Aspergillus fumigatus Acetate Utilization Impacts Virulence Traits and Pathogenicity
Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. Aspergillus fumigatus is a major oppor...
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| Published in | mBio Vol. 12; no. 4; p. e0168221 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Microbiology
31.08.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Aspergillus fumigatus
is an opportunistic fungal pathogen in humans. During infection,
A. fumigatus
is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion.
Aspergillus fumigatus
is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection,
A. fumigatus
needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in
A. fumigatus
and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB.
A. fumigatus
acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected
A. fumigatus
virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of
facB
significantly impaired the
in vivo
virulence of
A. fumigatus
in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in
A. fumigatus
, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies.
IMPORTANCE
Aspergillus fumigatus
is an opportunistic fungal pathogen in humans. During infection,
A. fumigatus
is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that
A. fumigatus
metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape
A. fumigatus
virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for
A. fumigatus
in vivo
virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in
A. fumigatus
and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. |
|---|---|
| AbstractList | Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. IMPORTANCE Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus in vivo virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. IMPORTANCE Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus in vivo virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome.Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. IMPORTANCE Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus in vivo virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of significantly impaired the virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. ABSTRACT Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus, and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. IMPORTANCE Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus in vivo virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus , and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A. fumigatus needs to use host carbon sources, such as acetate, present in the body fluids and peripheral tissues. However, utilization of acetate as a carbon source by fungi in the context of infection has not been investigated. This work shows that acetate is metabolized via different pathways in A. fumigatus and that acetate utilization is under the regulatory control of a transcription factor (TF), FacB. A. fumigatus acetate utilization is subject to carbon catabolite repression (CCR), although this is only partially dependent on the TF and main regulator of CCR CreA. The available extracellular carbon source, in this case glucose and acetate, significantly affected A. fumigatus virulence traits such as secondary metabolite secretion and cell wall composition, with the latter having consequences for resistance to oxidative stress, antifungal drugs, and human neutrophil-mediated killing. Furthermore, deletion of facB significantly impaired the in vivo virulence of A. fumigatus in both insect and mammalian models of invasive aspergillosis. This is the first report on acetate utilization in A. fumigatus , and this work further highlights the importance of available host-specific carbon sources in shaping fungal virulence traits and subsequent disease outcome, and a potential target for the development of antifungal strategies. IMPORTANCE Aspergillus fumigatus is an opportunistic fungal pathogen in humans. During infection, A. fumigatus is predicted to use host carbon sources, such as acetate, present in body fluids and peripheral tissues, to sustain growth and promote colonization and invasion. This work shows that A. fumigatus metabolizes acetate via different pathways, a process that is dependent on the transcription factor FacB. Furthermore, the type and concentration of the extracellular available carbon source were determined to shape A. fumigatus virulence determinants such as secondary metabolite secretion and cell wall composition. Subsequently, interactions with immune cells are altered in a carbon source-specific manner. FacB is required for A. fumigatus in vivo virulence in both insect and mammalian models of invasive aspergillosis. This is the first report that characterizes acetate utilization in A. fumigatus and highlights the importance of available host-specific carbon sources in shaping virulence traits and potentially subsequent disease outcome. |
| Author | Fill, Taicia Almeida, Fausto Duarte-Oliveira, Cláudio Valero, Clara Costa, Jonas Henrique Sze Wah Wong, Sarah Rodrigues, Fernando José Santos Steenwyk, Jacob L. Saborano, Raquel Alves de Castro, Patricia dos Reis, Thaila Fernanda Rokas, Antonis Goldman, Gustavo H. Persinoti, Gabriela Felix Aimanianda, Vishukumar Gonçales, Relber A. Ries, Laure Nicolas Annick Pereira Silva, Lilian Carvalho, Agostinho Duarte, Iola F. |
| Author_xml | – sequence: 1 givenname: Laure Nicolas Annick surname: Ries fullname: Ries, Laure Nicolas Annick organization: Faculdade de Medicina de Ribeirão Preto, Departamento de Bioquímica e Imunologia, Universidade de São Paulo, São Paulo, Brazil – sequence: 2 givenname: Patricia surname: Alves de Castro fullname: Alves de Castro, Patricia organization: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, Brazil – sequence: 3 givenname: Lilian surname: Pereira Silva fullname: Pereira Silva, Lilian organization: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, Brazil – sequence: 4 givenname: Clara surname: Valero fullname: Valero, Clara organization: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, Brazil – sequence: 5 givenname: Thaila Fernanda surname: dos Reis fullname: dos Reis, Thaila Fernanda organization: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, Brazil – sequence: 6 givenname: Raquel surname: Saborano fullname: Saborano, Raquel organization: University of Birmingham, Institute of Cancer and Genomic Sciences, Birmingham, England – sequence: 7 givenname: Iola F. surname: Duarte fullname: Duarte, Iola F. organization: CICECO - Aveiro Institute of Materials, Department of Chemistry, University of Aveiro, Aveiro, Portugal – sequence: 8 givenname: Gabriela Felix surname: Persinoti fullname: Persinoti, Gabriela Felix organization: Brazilian Biorenewables National Laboratory (LNBR), Brazilian Center for Research in Energy and Materials (CNPEM), Campinas, Sao Paulo, Brazil – sequence: 9 givenname: Jacob L. orcidid: 0000-0002-8436-595X surname: Steenwyk fullname: Steenwyk, Jacob L. organization: Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USA – sequence: 10 givenname: Antonis orcidid: 0000-0002-7248-6551 surname: Rokas fullname: Rokas, Antonis organization: Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USA – sequence: 11 givenname: Fausto orcidid: 0000-0002-3782-3698 surname: Almeida fullname: Almeida, Fausto organization: Faculdade de Medicina de Ribeirão Preto, Departamento de Bioquímica e Imunologia, Universidade de São Paulo, São Paulo, Brazil – sequence: 12 givenname: Jonas Henrique orcidid: 0000-0002-6415-3984 surname: Costa fullname: Costa, Jonas Henrique organization: Instituto de Química, Departamento de Química Orgânica, Universidade de Campinas, Campinas, São Paulo, Brazil – sequence: 13 givenname: Taicia surname: Fill fullname: Fill, Taicia organization: Instituto de Química, Departamento de Química Orgânica, Universidade de Campinas, Campinas, São Paulo, Brazil – sequence: 14 givenname: Sarah surname: Sze Wah Wong fullname: Sze Wah Wong, Sarah organization: Molecular Mycology Unit, Institut Pasteur, CNRS, UMR2000, Paris, France – sequence: 15 givenname: Vishukumar orcidid: 0000-0001-5813-7497 surname: Aimanianda fullname: Aimanianda, Vishukumar organization: Molecular Mycology Unit, Institut Pasteur, CNRS, UMR2000, Paris, France – sequence: 16 givenname: Fernando José Santos surname: Rodrigues fullname: Rodrigues, Fernando José Santos organization: Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal, ICVS/3B’s - PT Government Associate Laboratory, Guimarães/Braga, Portugal – sequence: 17 givenname: Relber A. surname: Gonçales fullname: Gonçales, Relber A. organization: Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal, ICVS/3B’s - PT Government Associate Laboratory, Guimarães/Braga, Portugal – sequence: 18 givenname: Cláudio surname: Duarte-Oliveira fullname: Duarte-Oliveira, Cláudio organization: Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal, ICVS/3B’s - PT Government Associate Laboratory, Guimarães/Braga, Portugal – sequence: 19 givenname: Agostinho surname: Carvalho fullname: Carvalho, Agostinho organization: Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal, ICVS/3B’s - PT Government Associate Laboratory, Guimarães/Braga, Portugal – sequence: 20 givenname: Gustavo H. orcidid: 0000-0002-2986-350X surname: Goldman fullname: Goldman, Gustavo H. organization: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Departamento de Ciências Farmacêuticas, Universidade de São Paulo, São Paulo, Brazil |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 Ries et al. Attribution Copyright © 2021 Ries et al. 2021 Ries et al. |
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| DOI | 10.1128/mBio.01682-21 |
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| Editor | Fischer, Reinhard |
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| Keywords | transcription factor secondary metabolites Aspergillus fumigatus cell wall acetate assimilation |
| Language | English |
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| Snippet | Aspergillus fumigatus
is an opportunistic fungal pathogen in humans. During infection,
A. fumigatus
is predicted to use host carbon sources, such as acetate,... Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A.... Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection, A.... ABSTRACT Aspergillus fumigatus is a major opportunistic fungal pathogen of immunocompromised and immunocompetent hosts. To successfully establish an infection,... |
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| SubjectTerms | acetate assimilation Acetates Acetates - metabolism Animals Aspergillosis Aspergillosis - microbiology Aspergillus fumigatus Aspergillus fumigatus - genetics Aspergillus fumigatus - metabolism Aspergillus fumigatus - pathogenicity cell wall Fungal Proteins Fungal Proteins - genetics Fungal Proteins - metabolism Gene Expression Regulation, Fungal Genetics and Molecular Biology Humans Larva Larva - microbiology Life Sciences Male Mice Mice, Inbred C57BL Microbiology and Parasitology Moths Moths - microbiology Mycology Neutrophils Neutrophils - microbiology Phenotype Research Article Secondary Metabolism secondary metabolites transcription factor Virulence |
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| Title | Aspergillus fumigatus Acetate Utilization Impacts Virulence Traits and Pathogenicity |
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