Abstract
Nonribosomal peptides (NRPs) and polyketides (PKs) are ecologically important secondary metabolites produced by bacteria and fungi using multidomain enzymes called nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs), respectively. Previous phylogenetic analyses of fungal NRPSs and PKSs have suggested that a few of these genes were acquired by fungi via horizontal gene transfer (HGT) from bacteria, including a hybrid NPS/PKS found in Cochliobolus heterostrophus (Dothideomycetes, Ascomycota). Here, we identify this hybrid gene in fungi representing two additional classes of Ascomycota (Aspergillus spp., Microsporum canis, Arthroderma spp., and Trichophyton spp., Eurotiomycetes; Chaetomium spp. and Metarhizium spp., Sordariomycetes) and use phylogenetic analyses of the most highly conserved domains from NRPSs (adenylation (A) domain) and PKSs (ketoacyl synthase (KS) domain) to examine the hypothesis that the hybrid NPS7/PKS24 was acquired by fungi from bacteria via HGT relatively early in the evolution of the Pezizomycotina. Our results reveal a unique ancestry of the A domain and KS domain in the hybrid gene relative to known fungal NRPSs and PKSs, provide strong evidence for HGT of the hybrid gene from a putative bacterial donor in the Burkholderiales, and suggest the HGT event occurred early in the evolution of the filamentous Ascomycota.
Highlights
Lateral or horizontal gene transfer (HGT) is defined as the transfer of a genetic element from one organism to another without vertical descent [1]
Fungal Clade 1 is distantly related to non-hybrid fungal nonribosomal peptide synthetases (NRPSs) A domain sequences (Fungal Clade 3) and to A domain sequences from Fungal Clade 4 that contain polyketide synthases (PKSs)/NRPS hybrids
The remaining fungal NRPS A domain sequences cluster into a monophyletic group that consists of fungal ACVS genes that have been shown to have arisen from bacteria via HGT [38,39,40,41] and is circumscribed as Fungal Clade 2
Summary
Lateral or horizontal gene transfer (HGT) is defined as the transfer of a genetic element from one organism to another without vertical descent [1]. HGT between eukaryotes has been documented in protists, fungi, and plants [4,5,6,7,8,9]. Studies are showing that some genes residing in the genomes of extant eukaryotes were acquired via horizontal transfer from bacteria [10,11,12,13,14]. Molecular phylogenetic analyses have revealed that an isopenicillin-N-synthase gene was transferred horizontally from a beta-lactam-producing prokaryote to the filamentous Ascomycota, with beta-lactam production observed in some species of Penicillium and Aspergillus [15]. Functional screens combined with phylogenetic analyses have shown that a bglucuronidase gene was transferred from bacteria to fungi [16]. From the earliest endosymbioses and related genomic incorporation that led to the evolution of eukaryotes [17] to events that appear to be recent in evolutionary time [6,17], prokaryote-toeukaryote gene transfers represent a fundamental and intriguing aspect of eukaryote biology
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