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Nutrient Sensing at the Plasma Membrane of Fungal Cells

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  • Authors: Patrick Van Dijck1,2, Neil Andrew Brown3, Gustavo H. Goldman4, Julian Rutherford5, Chaoyang Xue6, Griet Van Zeebroeck7,8
  • Editors: Joseph Heitman9, Neil A. R. Gow10
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: VIB-KU Leuven Center for Microbiology KU Leuven, Flanders, Belgium; 2: Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, KU Leuven, B-3001 Leuven, Belgium; 3: Plant Biology and Crop Science, Rothamsted Research, Harpenden, AL5 2JQ, United Kingdom; 4: Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil; 5: Institute for Cell and Molecular Biosciences, Medical School, Newcastle University, Newcastle upon Tyne, NE2 4HH, United Kingdom; 6: Public Health Research Institute, Department of Microbiology, Biochemistry and Molecular Genetics, Rutgers Biomedical and Health Sciences, Newark, NJ 07103; 7: VIB-KU Leuven Center for Microbiology KU Leuven, Flanders, Belgium; 8: Laboratory of Molecular Cell Biology, Institute of Botany and Microbiology, KU Leuven, B-3001 Leuven, Belgium; 9: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 10: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
    • Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0031-2016
  • Received 12 November 2016 Accepted 11 December 2016 Published 10 March 2017
  • P. Van Dijck, [email protected]
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  • Abstract:

    To respond to the changing environment, cells must be able to sense external conditions. This is important for many processes including growth, mating, the expression of virulence factors, and several other regulatory effects. Nutrient sensing at the plasma membrane is mediated by different classes of membrane proteins that activate downstream signaling pathways: nontransporting receptors, transceptors, classical and nonclassical G-protein-coupled receptors, and the newly defined extracellular mucin receptors. Nontransporting receptors have the same structure as transport proteins, but have lost the capacity to transport while gaining a receptor function. Transceptors are transporters that also function as a receptor, because they can rapidly activate downstream signaling pathways. In this review, we focus on these four types of fungal membrane proteins. We mainly discuss the sensing mechanisms relating to sugars, ammonium, and amino acids. Mechanisms for other nutrients, such as phosphate and sulfate, are discussed briefly. Because the model yeast has been the most studied, especially regarding these nutrient-sensing systems, each subsection will commence with what is known in this species.

  • Citation: Van Dijck P, Brown N, Goldman G, Rutherford J, Xue C, Van Zeebroeck G. 2017. Nutrient Sensing at the Plasma Membrane of Fungal Cells. Microbiol Spectrum 5(2):FUNK-0031-2016. doi:10.1128/microbiolspec.FUNK-0031-2016.

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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0031-2016
2017-03-10
2019-08-25

Abstract:

To respond to the changing environment, cells must be able to sense external conditions. This is important for many processes including growth, mating, the expression of virulence factors, and several other regulatory effects. Nutrient sensing at the plasma membrane is mediated by different classes of membrane proteins that activate downstream signaling pathways: nontransporting receptors, transceptors, classical and nonclassical G-protein-coupled receptors, and the newly defined extracellular mucin receptors. Nontransporting receptors have the same structure as transport proteins, but have lost the capacity to transport while gaining a receptor function. Transceptors are transporters that also function as a receptor, because they can rapidly activate downstream signaling pathways. In this review, we focus on these four types of fungal membrane proteins. We mainly discuss the sensing mechanisms relating to sugars, ammonium, and amino acids. Mechanisms for other nutrients, such as phosphate and sulfate, are discussed briefly. Because the model yeast has been the most studied, especially regarding these nutrient-sensing systems, each subsection will commence with what is known in this species.

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Nutrient Sensing at the Plasma Membrane of Fungal Cells
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Citation: Van Dijck P, Brown N, Goldman G, Rutherford J, Xue C, Van Zeebroeck G. 2017. Nutrient sensing at the plasma membrane of fungal cells. microbiolspec 5(2): doi:10.1128/microbiolspec.FUNK-0031-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0031-2016.fig1
FIGURE 1
Sugar-sensing proteins in the plasma membrane of fungal cells. Nutrient-sensing proteins in general can be divided into nontransporting receptors, transceptors, and G-protein-coupled receptors (GPCRs). Nontransporting sugar receptors include the () glucose sensors Snf3/Rgt2, the () glucose sensor Rag4, the () glucose sensor Hxs1, the () glucose sensor Hgt4, the () inositol sensor Itr1, the () cellobiose sensor Crt1, and the cellodextrin sensor Clp1. Sugar transceptors include the glucose sensor Hgt12, the hexose sensors Hxs1/2, the hexose sensor Gcr1, the () sugar sensor Rco3, the () hexose sensor Hxt4, the () hexose sensor Hxt1, the cellobiose sensors Cdt1/2, and the () cellobiose sensor Stp1. Sugar GPCRs include the glucose sensor Gpr1, the glucose sensors Gpr4/5, the glucose sensor Gpr4, the () glucose sensors GprD/H, the () glucose sensors GprC/D, and the () glucose sensors GprA/C/J/K/R.
microbiolspec/5/2/FUNK-0031-2016-fig1_thmb.gif
microbiolspec/5/2/FUNK-0031-2016-fig1.gif
Image of FIGURE 1
FIGURE 1

Sugar-sensing proteins in the plasma membrane of fungal cells. Nutrient-sensing proteins in general can be divided into nontransporting receptors, transceptors, and G-protein-coupled receptors (GPCRs). Nontransporting sugar receptors include the () glucose sensors Snf3/Rgt2, the () glucose sensor Rag4, the () glucose sensor Hxs1, the () glucose sensor Hgt4, the () inositol sensor Itr1, the () cellobiose sensor Crt1, and the cellodextrin sensor Clp1. Sugar transceptors include the glucose sensor Hgt12, the hexose sensors Hxs1/2, the hexose sensor Gcr1, the () sugar sensor Rco3, the () hexose sensor Hxt4, the () hexose sensor Hxt1, the cellobiose sensors Cdt1/2, and the () cellobiose sensor Stp1. Sugar GPCRs include the glucose sensor Gpr1, the glucose sensors Gpr4/5, the glucose sensor Gpr4, the () glucose sensors GprD/H, the () glucose sensors GprC/D, and the () glucose sensors GprA/C/J/K/R.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0031-2016
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FIGURE 2
Nitrogen-sensing proteins in the plasma membrane of fungal cells. Nutrient-sensing proteins, in general, can be divided into nontransporting receptors, transceptors, and G-protein-coupled receptors (GPCRs). Nontransporting nitrogen receptors include the () amino acid sensor Ssy1, the () amino acid sensor Csy1, and an unknown () amino acid sensor. Nitrogen transceptors include the amino acid sensor Gap1, the amino acid sensors Gap1/2/6, the ammonium sensor Mep2, the ammonium sensor Mep2, the () ammonium sensor Ump2, the () ammonium sensors MepA-C, the () ammonium sensors Amt1-3, the () ammonium sensor Amt1, and the () ammonium sensors MepA-C. Nitrogen GPCRs include the methionine sensor Gpr1, the amino acid sensor Gpr4, the () tryptophan sensor GprH, the () proline sensor GprC/D, the () nitrogen sensor Stm1, and the ammonium sensor GprR.
microbiolspec/5/2/FUNK-0031-2016-fig2_thmb.gif
microbiolspec/5/2/FUNK-0031-2016-fig2.gif
Image of FIGURE 2
FIGURE 2

Nitrogen-sensing proteins in the plasma membrane of fungal cells. Nutrient-sensing proteins, in general, can be divided into nontransporting receptors, transceptors, and G-protein-coupled receptors (GPCRs). Nontransporting nitrogen receptors include the () amino acid sensor Ssy1, the () amino acid sensor Csy1, and an unknown () amino acid sensor. Nitrogen transceptors include the amino acid sensor Gap1, the amino acid sensors Gap1/2/6, the ammonium sensor Mep2, the ammonium sensor Mep2, the () ammonium sensor Ump2, the () ammonium sensors MepA-C, the () ammonium sensors Amt1-3, the () ammonium sensor Amt1, and the () ammonium sensors MepA-C. Nitrogen GPCRs include the methionine sensor Gpr1, the amino acid sensor Gpr4, the () tryptophan sensor GprH, the () proline sensor GprC/D, the () nitrogen sensor Stm1, and the ammonium sensor GprR.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0031-2016
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FIGURE 3
Surface-sensing proteins in the plasma membrane of fungal cells. Characterized surface-sensing proteins can be divided into G-protein-coupled receptors (GPCRs) and the interacting Sho receptors and the extracellular mucin receptors. The nonclassical, Pth11-type, GPCRs include the () Pth11 receptor of hydrophobic surfaces and the () Gpr32, Gpr36, and Gpr39 putative lignocellulose receptors. The Sho receptors include the orthologous (), () and , hydrophobic surface Sho1 receptors. The extracellular mucins include the orthologous (), , , , Msb2 hydrophobic surface receptors, in addition to the Msb2 receptors of () and () that have not been characterized as detecting surfaces, plus the additional Cbp1 mucin receptor of hydrophobic surfaces from .
microbiolspec/5/2/FUNK-0031-2016-fig3_thmb.gif
microbiolspec/5/2/FUNK-0031-2016-fig3.gif
Image of FIGURE 3
FIGURE 3

Surface-sensing proteins in the plasma membrane of fungal cells. Characterized surface-sensing proteins can be divided into G-protein-coupled receptors (GPCRs) and the interacting Sho receptors and the extracellular mucin receptors. The nonclassical, Pth11-type, GPCRs include the () Pth11 receptor of hydrophobic surfaces and the () Gpr32, Gpr36, and Gpr39 putative lignocellulose receptors. The Sho receptors include the orthologous (), () and , hydrophobic surface Sho1 receptors. The extracellular mucins include the orthologous (), , , , Msb2 hydrophobic surface receptors, in addition to the Msb2 receptors of () and () that have not been characterized as detecting surfaces, plus the additional Cbp1 mucin receptor of hydrophobic surfaces from .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0031-2016
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FIGURE 4
Nutrient- and surface-sensing proteins in the plasma membrane of fungal cells and the downstream signal transduction pathways they trigger. Examples for the different classes of nutrient (nontransporting receptors, transceptors, and GPCRs) and surface (mucin and Sho) sensing proteins are shown. Sensing of nutrients by nontransporting receptors and sugar transceptors results in the induction of nutrient transporter genes. Nitrogen transceptors (e.g., Gap1) result in the activation of the PKA pathway upon sensing appropriate nitrogen sources. Depending on the type of GPCR, they can activate the cAMP-PKA pathway, the MAPK pathway, or both. The surface receptors activate the MAPK pathway.
microbiolspec/5/2/FUNK-0031-2016-fig4_thmb.gif
microbiolspec/5/2/FUNK-0031-2016-fig4.gif
Image of FIGURE 4
FIGURE 4

Nutrient- and surface-sensing proteins in the plasma membrane of fungal cells and the downstream signal transduction pathways they trigger. Examples for the different classes of nutrient (nontransporting receptors, transceptors, and GPCRs) and surface (mucin and Sho) sensing proteins are shown. Sensing of nutrients by nontransporting receptors and sugar transceptors results in the induction of nutrient transporter genes. Nitrogen transceptors (e.g., Gap1) result in the activation of the PKA pathway upon sensing appropriate nitrogen sources. Depending on the type of GPCR, they can activate the cAMP-PKA pathway, the MAPK pathway, or both. The surface receptors activate the MAPK pathway.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0031-2016
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