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Abstract
Extracellular vesicles (EVs) are lipid bilayer structures released by organisms from all kingdoms of life. The diverse biogenesis pathways of EVs result in a wide variety of physical properties and functions across different organisms. Fungal EVs were first described in 2007 and different omics approaches have been fundamental to understand their composition, biogenesis, and function. In this review, we discuss the role of omics in elucidating fungal EVs biology. Transcriptomics, proteomics, metabolomics, and lipidomics have each enabled the molecular characterization of fungal EVs, providing evidence that these structures serve a wide array of functions, ranging from key carriers of cell wall biosynthetic machinery to virulence factors. Omics in combination with genetic approaches have been instrumental in determining both biogenesis and cargo loading into EVs. We also discuss how omics technologies are being employed to elucidate the role of EVs in antifungal resistance, disease biomarkers, and their potential use as vaccines. Finally, we review recent advances in analytical technology and multi-omic integration tools, which will help to address key knowledge gaps in EVs biology and translate basic research information into urgently needed clinical applications such as diagnostics, and immuno- and chemotherapies to fungal infections.
Highlights
Cells secrete a variety of molecules to the extracellular milieu, from the smallest metabolites to large proteins and glycoconjugates
Morphological studies of C. neoformans showed structures resembling multivesicular bodies (MBVs) that can fuse to the plasma membrane, resulting in the release of intraluminal MBV vesicles into the fungal periplasm (Takeo et al, 1973). Those images suggested that populations of fungal Extracellular vesicles (EVs) might correspond to exosomes, which are mammalian EVs released to the extracellular milieu by the fusion of MVBs to the plasma membrane (Raposo and Stoorvogel, 2013). This biogenesis pathway was supported by recent studies in C. neoformans (Park et al, 2020) and Candida albicans (Zarnowski et al, 2018), in which deletion of genes affecting MVB formation resulted in aberrant vesicles and/or decreased EVs production
When we compared the proteomic data of H. capsulatum EVs (Cleare et al, 2020) with whole cells (Burnet et al, 2020), the results showed that EVs were highly enriched in cell wall synthases and hydrolases, such as β-glucanase, β-1,3glucanosyltransferase, chitin synthase, and chitinase (Figure 2)
Summary
Cells secrete a variety of molecules to the extracellular milieu, from the smallest metabolites to large proteins and glycoconjugates. This biogenesis pathway was supported by recent studies in C. neoformans (Park et al, 2020) and Candida albicans (Zarnowski et al, 2018), in which deletion of genes affecting MVB formation resulted in aberrant vesicles and/or decreased EVs production. In P. brasiliensis, 60% of the non-covalently bound cell wall proteins, detected by proteomic analysis of two distinct isolates, have been described in fungal EVs (Longo et al, 2014).
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