Abstract

Filamentous fungi are found in virtually every marine and terrestrial habitat. Vital to this success is their ability to secrete a diverse range of molecules, including hydrolytic enzymes, organic acids, and small molecular weight natural products. Industrial biotechnologists have successfully harnessed and re-engineered the secretory capacity of dozens of filamentous fungal species to make a diverse portfolio of useful molecules. The study of fungal secretion outside fermenters, e.g., during host infection or in mixed microbial communities, has also led to the development of novel and emerging technological breakthroughs, ranging from ultra-sensitive biosensors of fungal disease to the efficient bioremediation of polluted environments. In this review, we consider filamentous fungal secretion across multiple disciplinary boundaries (e.g., white, green, and red biotechnology) and product classes (protein, organic acid, and secondary metabolite). We summarize the mechanistic understanding for how various molecules are secreted and present numerous applications for extracellular products. Additionally, we discuss how the control of secretory pathways and the polar growth of filamentous hyphae can be utilized in diverse settings, including industrial biotechnology, agriculture, and the clinic.

Highlights

  • Chair of Applied and Molecular Microbiology, Institute of Biotechnology, Technische Universität Berlin, Straße des 17

  • While sporespecies dispersal can occur across largeof distances, fungi are in the vast majority of cases non-motile, and filamenmesh of polysaccharides and proteins

  • This study focused on the glucoamylase GlaA, a major A. niger secreted protein which is used to saccharify starch to glucose in a variety of food industries with a global value of over $1 billion/year [15,71]

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Summary

Fungal Secretion

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. Filamentous fungi inhabit virtually all marine and terrestrial environments as free living microbes, symbionts, commensals, and pathogens [1,2] This global colonization is dependent on their ability to secrete a diverse repertoire of protein, organic acid, and secondary metabolite molecules, which enable nutrient acquisition, growth of polar cells termed hyphae, and a number of specialized, niche-dependent functions, ranging from host tissue invasion, symbiosis, sexual reproduction, or killing competing microbes. Industrial biotechnologists have repurposed filamentous fungal secretion for over a century, where cheap, readily available renewable biomass has been converted to megatons of useful products including hydrolytic enzymes, platform chemicals, and pharmaceuticals [3,4,5] This efficient recycling of biomass has recently been identified as an important component in the global transition from a petroleum-based economy to a sustainable circular economy, which may mitigate climate change, achieve international food security, and protect natural ecosystems (Figure 1 [6,7]).

Schematic representation of secondary metabolite secretion by filamentous
From Dormancy to Growth
The Classical Secretion Route and Hyphal Polarity
Endocytosis and Branching
Controlling Filamentous Growth for Optimal Macromorphologies
New Additions to the Classical Secretion Pathway
Summary
A Stomach Outside the Body
Secreted Lipases in Industrial Biotechnology
New Frontiers
Secretion and Micronutrients
Siderophores and Iron Availability
Organic Acids as Overflow Metabolites
Increasing Glycolytic Flux for Organic Acid Hypersecretors
Secretion of Organic Acids and Their Applications
Infection
Secreted Molecules and Immune Evasion during Plant or Human Infection
Plants
Humans and Other Mammals
Purified PAMPs in Agriculture
Discovery and Cloning of Resistance Genes in Crop Genomes
Inhibiting Secretion for New Mode of Action Antifungals
Secreted Molecules and Vaccines for Fungal Infection
Interspecies Communication
Fungal Extracellular Molecules in Mutualist Interactions
Arbuscular Mycorrhizae and Fungal Secretion
Intraspecies Communication
Sexual Reproduction and Secretion of Pheromones
Applications of Fungal Pheromones
Applications of Antifungal Proteins
Surviving in the Community
Secretion of Xenobiotics
Applications of Fungal Efflux Pumps
Revisiting Organic Acids
Findings
10. Concluding Remarks
Full Text
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