Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic

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.

First genome-scale insights into the virulence of the snow mold causal fungus Microdochium nivale

“…In our study, genes encoding ferric-chelate reductases, iron transporter MirB, and genes putatively related to the synthesis of siderophores were upregulated after the addition of rye extract, indicating that the presence of host plant metabolites promoted iron uptake by fungal cells. Many virulence factors are transported from fungal cells via extracellular vesicles (Silva et al 2014 ; Bleackley et al 2019 ; Cairns et al 2021 ; Garcia-Ceron et al 2021 ), including those that lack signal peptides (Kijpornyongpan et al 2022 ). This means that extracellular vesicular transport is important for plant-pathogen interaction.…”

Potential of Aspergillus oryzae as a biosynthetic platform for indigoidine, a non-ribosomal peptide pigment with antioxidant activity

“…In filamentous fungi, the mechanism controlling metabolite secretion, particularly that of secondary metabolites, has not been elucidated. A scheme for secondary metabolite production and secretion by filamentous fungi has been previously reported [ 50 ]. Studies have proven that the secondary metabolite biosynthesis particularly in filamentous fungi is generated in endosomes or peroxisomes, wherein synthetases and other tailor-made enzymes exist.…”

Nematophagous Fungi: A Review of Their Phosphorus Solubilization Potential

“…Among the known genera that work as both biocontrol and P solubilizers are Trichoderma , Fusarium , Penicillium , and Aspergillus. Filamentous fungi can secrete hydrolytic enzymes, organic acids, and low molecular weight natural products, which confer several functions, including P solubilization [ 77 ], and are able to solubilize calcium and iron phosphates [ 78 ]. Thus, they hold great potential for the development of biofertilizers, contributing to soil fertility and promoting plant growth [ 79 ], which are essential in sustainable agriculture ( Table 1 ) [ 80 ].…”