Abstract

Early-diverging fungi harbour unprecedented diversity in terms of living forms, biological traits and genome architecture. Before the sequencing era, non-Dikarya fungi were considered unable to produce secondary metabolites (SM); however, this perspective is changing. The main classes of secondary metabolites in fungi include polyketides, nonribosomal peptides, terpenoids and siderophores that serve different biological roles, including iron chelation and plant growth promotion. The same classes of SM are reported for representatives of early-diverging fungal lineages. Encouraged by the advancement in the field, we carried out a systematic survey of SM in Mucoromycotina and corroborated the presence of various SM clusters (SMCs) within the phylum. Among the core findings, considerable representation of terpene and nonribosomal peptide synthetase (NRPS)-like candidate SMCs was found. Terpene clusters with diverse domain composition and potentially highly variable products dominated the landscape of candidate SMCs. A uniform low-copy distribution of siderophore clusters was observed among most assemblies. Mortierellomycotina are highlighted as the most potent SMC producers among the Mucoromycota and as a source of novel peptide products. SMC identification is dependent on gene model quality and can be successfully performed on a batch scale with genomes of different quality and completeness.

Highlights

  • Early-diverging fungi were long considered to be devoid of secondary metabolite (SM)clusters; this perspective has gradually changed with the advancement of genome sequencing of selected representatives

  • The identified secondary metabolite clusters (SMCs) harboured key enzymes involved in SM biosynthesis in Dikarya: polyketide synthases (PKS), nonribosomal peptide synthetases (NRPS), terpene cyclases/synthases (TC), and dimethylallyl tryptophan synthases (DMATS)

  • We found that the Glomeromycotina are unique in coding for candidate SMCs containing fatty acid acyl-CoA AMP ligase (FAAL)

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Summary

Introduction

Early-diverging fungi were long considered to be devoid of secondary metabolite (SM). The main classes of secondary metabolites in fungi include the respective compounds tied to the above core enzymes: polyketides, nonribosomal peptides, terpenoids and siderophores. Experimental studies showed that different Mortierellomycotina representatives produce diverse natural products with interesting properties e.g., malpinin acetylated hexapeptides and malpibaldin cyclic pentapeptides [11] These compounds have been linked to the presence of several NRPS clusters, for example, in the mycelium of Mortierella alpina. Mortierella elongata) and Mycoavidus cysteinexigens symbiosis, several compounds are produced, and the genome of the bacteria encodes NRPS and other metabolite clusters [19]. Fungal secondary metabolites can promote plant growth in harsh conditions This process is mediated by the release of phytohormones; for example, gibberellic acid (a diterpenoid acid) produced by Rhizopus stolonifer [20]), Mortierella antarctica and Podila verticillata

SMC-Encoded Protein Clustering and Annotation
SMC Similarity Network Construction and Visualization
Detection of Genes of Putative Bacterial Origin
Initial Screening
Limits of de Novo Prediction in the Absence of Reference Annotation
De Novo Predicted SMC Candidate Sequences Are Poorly Characterised by Synteny
Taxonomic Distribution
Cluster Types
Presence of Bacterial-Like SMCs
SMC Sequence Clustering
Predominance of Terpene Biosynthesis in Non-Dikarya Genomes
3.10. Non-NRPS Siderophore Synthases Are Conserved in Early-Diverging Fungi
Conclusions
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