Abstract
Anaerobic fungi (class Neocallimastigomycetes) thrive as low-abundance members of the herbivore digestive tract. The genomes of anaerobic gut fungi are poorly characterized and have not been extensively mined for the biosynthetic enzymes of natural products such as antibiotics. Here, we investigate the potential of anaerobic gut fungi to synthesize natural products that could regulate membership within the gut microbiome. Complementary 'omics' approaches were combined to catalog the natural products of anaerobic gut fungi from four different representative species: Anaeromyces robustus (Arobustus), Caecomyces churrovis (Cchurrovis), Neocallimastix californiae (Ncaliforniae), and Piromyces finnis (Pfinnis). In total, 146 genes were identified that encode biosynthetic enzymes for diverse types of natural products, including nonribosomal peptide synthetases and polyketide synthases. In addition, N. californiae and C. churrovis genomes encoded seven putative bacteriocins, a class of antimicrobial peptides typically produced by bacteria. During standard laboratory growth on plant biomass or soluble substrates, 26% of total core biosynthetic genes in all four strains were transcribed. Across all four fungal strains, 30% of total biosynthetic gene products were detected via proteomics when grown on cellobiose. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) characterization of fungal supernatants detected 72 likely natural products from A. robustus alone. A compound produced by all four strains of anaerobic fungi was putatively identified as the polyketide-related styrylpyrone baumin. Molecular networking quantified similarities between tandem mass spectrometry (MS/MS) spectra among these fungi, enabling three groups of natural products to be identified that are unique to anaerobic fungi. Overall, these results support the finding that anaerobic gut fungi synthesize natural products, which could be harnessed as a source of antimicrobials, therapeutics, and other bioactive compounds.
Highlights
Certain fungal genera, such as Aspergillus, are disproportionately studied, they represent only a fraction of sequenced fungal genomes [6]
Some of the biosynthetic genes of anaerobic fungi were similar to those found in bacteria, suggesting the possibility of horizontal gene transfer between fungi and bacteria in the rumen microbiome
Many of the biosynthetic genes of anaerobic fungi were similar to bacteria, their regulation may still be typical of fungal secondary metabolism
Summary
Certain fungal genera, such as Aspergillus, are disproportionately studied, they represent only a fraction of sequenced fungal genomes [6]. Anaerobic gut fungi (class Neocallimastigomycetes) are understudied organisms that thrive as members of a consortium of archaea, bacteria, and protozoa in the digestive tracts of large herbivores [10,11,12]. In these habitats, fungi are vastly outnumbered by prokaryotic microorganisms by several orders of magnitude [10,11,12]. We show that these early-branching fungi produce a wealth of secondary metabolites (natural products) that may act to regulate the gut microbiome. M.A.F. is a guest editor invited by the Editorial Board
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