Abstract
As obligate biotrophic symbionts, arbuscular mycorrhizal fungi (AMF) live in association with most land plants. Among them, Gigaspora margarita has been deeply investigated because of its peculiar features, i.e., the presence of an intracellular microbiota with endobacteria and viruses. The genome sequencing of this fungus revealed the presence of some hybrid non-ribosomal peptide synthases-polyketide synthases (NRPS-PKS) that have been rarely identified in AMF. The aim of this study is to describe the architecture of these NRPS-PKS sequences and to understand whether they are present in other fungal taxa related to G. margarita. A phylogenetic analysis shows that the ketoacyl synthase (KS) domain of one G. margarita NRPS-PKS clusters with prokaryotic sequences. Since horizontal gene transfer (HGT) has often been advocated as a relevant evolutionary mechanism for the spread of secondary metabolite genes, we hypothesized that a similar event could have interested the KS domain of the PKS module. The bacterial endosymbiont of G. margarita, Candidatus Glomeribacter gigasporarum (CaGg), was the first candidate as a donor, since it possesses a large biosynthetic cluster involving an NRPS-PKS. However, bioinformatics analyses do not confirm the hypothesis of a direct HGT from the endobacterium to the fungal host: indeed, endobacterial and fungal sequences show a different evolution and potentially different donors. Lastly, by amplifying a NRPS-PKS conserved fragment and mining the sequenced AMF genomes, we demonstrate that, irrespective of the presence of CaGg, G. margarita, and some other related Gigasporaceae possess such a sequence.
Highlights
Fungi play crucial roles in the life on our planet: one of their most important and investigated feature is the production of secondary metabolites, which include polyketides, nonribosomal peptides, terpenes, and indole alkaloids (Keller et al, 2005)
As a first step of the investigation, the genome of G. margarita (Venice et al, 2020) was screened with the antiSMASH v.5 (Blin et al, 2019) and BIG-SCAPE (Navarro-Muñoz et al, 2020) pipelines for the identification of the three main enzyme classes that participate to the biosynthesis of secondary metabolites in fungi, that is Polyketide synthases (PKS), non-ribosomal peptide synthases (NRPS), and NRPS-PKS hybrids (Keller, 2019)
We found three Type 1 PKS (T1PKS) genes, nine NRPS-like genes and six hybrid NRPS/PKS, five of which consist of isolated genes
Summary
Fungi play crucial roles in the life on our planet: one of their most important and investigated feature is the production of secondary metabolites, which include polyketides, nonribosomal peptides, terpenes, and indole alkaloids (Keller et al, 2005). The genome sequencing of fungi from the Fungal Tree of Life has revealed that the genes encoding PKS are mostly arranged as biosynthetic gene clusters (BGCs) The latter are often associated with non-ribosomal peptide synthases (NRPS), which are involved in siderophore formation (Carroll and Moore, 2018), leading to hybrid BGCs. The latter are often associated with non-ribosomal peptide synthases (NRPS), which are involved in siderophore formation (Carroll and Moore, 2018), leading to hybrid BGCs These genomic regions are frequently co-regulated depending on the ecological function of their encoded product (Keller, 2019), meaning that their expression is modulated by environmental conditions related to a specific development stage of the fungus
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