Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic
Abstract
:1. Fungal Secretion: The Global Bioeconomy and beyond
2. Polar Growth
2.1. From Dormancy to Growth: Establishing Polarity
2.2. The Classical Secretion Route and Hyphal Polarity
2.3. Endocytosis and Branching
2.4. Repurposing Polar Growth and Classical Secretion in Biotechnology: A Case Study Using A. niger RacA and Glucoamylase
2.5. Controlling Filamentous Growth for Optimal Macromorphologies
2.6. New Additions to the Classical Secretion Pathway: Extracellular Secretory Vesicles
2.7. Summary
3. Breakdown of Macromolecules for Nutrient Acquisition
3.1. A Stomach Outside the Body: Digesting the Extracellular Space
3.2. Secreted Lipases in Industrial Biotechnology: An Exemplar Success Story
3.3. New Frontiers: Degrading Lignocellulose and Plastics
4. Secretion and Micronutrients
4.1. Siderophores and Iron Availability
4.2. Organic Acids May Liberate and Chelate Nutrients from the External Environment
4.3. Summary
5. Removal of Overflow Metabolites
5.1. Organic Acids as Overflow Metabolites
5.2. Increasing Glycolytic Flux for Organic Acid Hypersecretors
5.3. Secretion of Organic Acids and Their Applications
6. Infection
6.1. Secreted Molecules and Immune Evasion during Plant or Human Infection
6.2. Direct Host Attack by Secreted Secondary Metabolites and Proteins
6.2.1. Plants
6.2.2. Humans and Other Mammals
6.3. Applications of Fungal Secretion and Extracellular Molecules
6.3.1. Purified PAMPs in Agriculture
6.3.2. Discovery and Cloning of Resistance Genes in Crop Genomes
6.3.3. Inhibiting Secretion for New Mode of Action Antifungals
6.3.4. Secreted Molecules and Vaccines for Fungal Infection
6.4. Summary
7. Interspecies Communication
7.1. Fungal Extracellular Molecules in Mutualist Interactions: Lichens
7.2. Arbuscular Mycorrhizae and Fungal Secretion
7.3. Summary
8. Intraspecies Communication
8.1. Sexual Reproduction and Secretion of Pheromones
8.2. Applications of Fungal Pheromones
8.3. Applications of Antifungal Proteins
8.4. Summary
9. Surviving in the Community
9.1. Harnessing Fungal Chemical Defence for New Bioactive Molecule Discovery: A Case Study Using Enniatin and Related Compounds
9.2. Secretion of Xenobiotics: Surviving Chemical Attack
9.3. Applications of Fungal Efflux Pumps
9.4. Revisiting Organic Acids: Are They Secreted to Inhibit Competing Neutrophiles?
9.5. Summary
10. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Product Class | Product | Exemplar Producing Fungal Species | Secretion Route and/or Plasma Membrane Transporter | Postulated or Confirmed Function(s) in the Natural Niche | Current or Prospective Application(s) | References |
---|---|---|---|---|---|---|
Enzyme/proteins | Glucoamylase GlaA | A. niger | Classical secretion route | Nutrient acquisition | Food and beverage industries processing starch to glucose | [4,15] |
Cellulases | T. reesei, T. thermophila | Textile, food, and other industries | [16] | |||
Lipases | T. lanuginosus A. oryzae | Applications in biodiesel, dairy, textile, detergent, paper, pharmaceutical, leather and other industries | [17,18] | |||
Agglutinin-like sequence protein Als3 | Candida spp. | Adhesion of fungal cells to host and abiotic surfaces | Possible vaccine in humans | [19,20] | ||
Secreted aspartic protease 2 Sap-2 | Nutrient acquisition, virulence factor | [21] | ||||
Antifungal protein AFP | A. giganteus | Cannibal toxin regulating clonal growth, inhibitor of competing fungi | Prospective antifungal use in clinic or agriculture | [22,23] | ||
Effectors | M. oryzae, Z. tritici, other plant-infecting fungi | Classical secretion route, biotrophic interphase complex, non-classical secretion route, extracellular vesicles | Virulence factors | Cognate receptor and R proteins used to elicit protective crop immunity | [24,25,26] | |
Secondary metabolite | Triacetyl-fusarine C | A. fumigatus | Intermediates generated in mitochondria and peroxisomes plasma membrane transporter unknown | Micronutrient acquisition (iron chelator), necessary for full virulence | Biosynthetic pathway is a possible drug target, siderophores could be used to decontaminate metals from natural ecosystems | [27,28] |
Penicillin | P. chrysogenum | Intermediates generated in peroxisome and vacuoles, possibly secreted via vesicles or unknown plasma membrane transporter | Inhibitor of competing microbes | Antimicrobial with widespread clinical use | [29] | |
Trisporic acid | B. trispora | Unknown | Mating pheromone | Used to elevate yields of β-carotene during fermentation | [30] | |
Enniatin | Fusarium spp., A. niger (heterologous expression host) | Unknown | Prevent predation | Antimicrobial and anti-inflammatory clinical applications | [31] | |
Organic acid | Citric acid | A. niger | Plasma membrane transporter CexA | Micronutrient acquisition (iron chelator), inhibitor of competing microbes, overflow metabolite | Food and beverage as flavour enhancer, cleaning product, many industrial uses as a weak acid and platform chemical | [32] |
Malic acid | Plasma membrane transporter DctA | Inhibitor of competing microbes, overflow metabolite | Industrial uses as a weak acid and platform chemical | [33] | ||
Itaconic acid | A. terreus, U. maydis, A niger (heterologous expression host) | Plasma membrane transporter MfsA (A. terreus) or Itp1 (U. maydis) | Inhibitor of competing microbes, overflow metabolite | Industrial uses as a weak acid and platform chemical | [34] |
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Cairns, T.C.; Zheng, X.; Zheng, P.; Sun, J.; Meyer, V. Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic. J. Fungi 2021, 7, 535. https://doi.org/10.3390/jof7070535
Cairns TC, Zheng X, Zheng P, Sun J, Meyer V. Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic. Journal of Fungi. 2021; 7(7):535. https://doi.org/10.3390/jof7070535
Chicago/Turabian StyleCairns, Timothy C., Xiaomei Zheng, Ping Zheng, Jibin Sun, and Vera Meyer. 2021. "Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic" Journal of Fungi 7, no. 7: 535. https://doi.org/10.3390/jof7070535