Genome of lethal Lepiota venenata and insights into the evolution of toxin-biosynthetic genes

et al. 2020

Preprint

Background Amanitin-producing mushrooms, mainly distributed in the genera Amanita , Galerina and Lepiota , possess MSDIN gene family for the biosynthesis of many cyclopeptides catalyzed by prolyl oligopeptidase (POP). Recently, transcriptome sequencing has proven to be a efficient way to mine MSDIN and POP genes in these lethal mushrooms. Until now, only A . palloides and A. bisporigera from North America and A . exitialis from Asia have been studied based on transcriptome analysis. However, MSDIN and POP genes of many amanitin-producing mushrooms in China remain unstudied, and hence the transcriptomes of these speices deserve to be analysed. Results In this study, the MSDIN and POP genes from ten Amanita species, two Galerina species and Lepiota venenata were studied and the phylogenetic relationships of their MSDIN and POP genes were analyzed. Through transcriptome sequencing and PCR cloning, 19 POP genes and 151 MSDIN genes predicted to encode 98 non-duplicated cyclopeptides, including α-amanitin, β-amanitin, phallacidin, phalloidin and 94 unknown peptides, were found in these species. Phylogenetic analysis showed that toxin peptide genes were clustered depending on the chemical substance within genus while depending on the taxonomy between genus and that the POPA genes of Amanita , Galerina and Lepiota were clustered and separated in three different groups, but the POPB genes of the three distinct genera were clustered in a highly monophyletic group. Conclusions These results above indicate that lethal Amanita species have the genetic capacity to produce numerous cyclopeptides, most of which are unknown, while lethal Galerina and Lepiota species seem to only have the genetic capacity to produce α-amanitin. Additionally, the POPB phylogeny of Amanita , Galerina and Lepiota conflicts with the taxonomic status of the three genera, suggesting that horizontal gene transfer might occur among the three genera.

Section: Discussionmentioning

confidence: 51%

Section: Discussionmentioning

confidence: 99%

Diversity of MSDIN family members in amanitin-producing mushrooms and the phylogeny of the MSDIN and prolyl oligopeptidase genes

et al. 2020

Preprint

“…It has been reported that HGT is very common in prokaryotes and may be an important source of their biological evolution, and HGT also occurs in eukaryotes at a lower frequency than in prokaryotes [32][33][34][35]. The most recent reports suggest that HGT may be responsible for the α-amanitin biosynthetic pathway found in the three distantly related genera Amanita, Galerina and Lepiota [8,9]. It has been reported that in amanitin-producing mushrooms, the POPB gene product catalyses the cleavage and cyclization of the toxin precursor peptide, while the POPA gene is a housekeeping gene that is unrelated to toxin biosynthesis [7,12].…”

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Diversity of MSDIN family members in amanitin-producing mushrooms and the phylogeny of the MSDIN and prolyl oligopeptidase genes

et al. 2020

Preprint

Background: Amanitin-producing mushrooms, mainly distributed in the genera Amanita , Galerina and Lepiota , possess MSDIN gene family for the biosynthesis of many cyclopeptides catalysed by prolyl oligopeptidase (POP). Recently, transcriptome sequencing has proven to be an efficient way to mine MSDIN and POP genes in these lethal mushrooms. Thus far, only A . palloides and A. bisporigera from North America and A . exitialis and A. rimosa from Asia have been studied based on transcriptome analysis. However, the MSDIN and POP genes of many amanitin-producing mushrooms in China remain unstudied; hence, the transcriptomes of these speices deserve to be analysed. Results: In this study, the MSDIN and POP genes from ten Amanita species, two Galerina species and Lepiota venenata were studied and the phylogenetic relationships of their MSDIN and POP genes were analysed. Through transcriptome sequencing and PCR cloning, 19 POP genes and 151 MSDIN gened to encode 98 non-duplicated cyclopeptides, including α- amanitin, β-amanitin, phallacidin, phalloidin and 94 unknown peptides, were found in these species. Phylogenetic analysis showed that (1) MSDIN genes generally clustered depending on the taxonomy of the genus, while Amanita MSDIN genes clustered depending on the chemical substance; and (2) the POPA genes of Amanita , Galerina and Lepiota clustered and were separated into three different groups, but the POPB genes of the three distinct genera were clustered in a highly supported monophyletic group. Conclusions: These results indicate that lethal Amanita species have the genetic capacity to produce numerous cyclopeptides, most of which are unknown, while lethal Galerina and Lepiota species seem to only have the genetic capacity to produce α-amanitin. Additionally, the POPB phylogeny of Amanita , Galerina and Lepiota conflicts with the taxonomic status of the three genera, suggesting that underlying horizontal gene transfer has occurred among these three genera.

“…Additionally, α-AMA of Lepiota brunneoincarnata, which is an amanitin-containing mushroom of the genus Lepiota, has been successfully cloned [8]. The genome sequencing of L. venenata, another newly reported amanitincontaining species, has been completed, and it has been shown to harbour α-AMA genes [9]. Precursor peptide sequence alignment of α-AMA sequences from Amanita, Galerina and Lepiota shows high divergence except in the toxin region.…”

Section: Introductionmentioning

confidence: 99%

Diversity of MSDIN family members in amanitin-producing mushrooms and the phylogeny of the MSDIN and prolyl oligopeptidase genes

et al. 2020

BMC Genomics

Background: Amanitin-producing mushrooms, mainly distributed in the genera Amanita, Galerina and Lepiota, possess MSDIN gene family for the biosynthesis of many cyclopeptides catalysed by prolyl oligopeptidase (POP). Recently, transcriptome sequencing has proven to be an efficient way to mine MSDIN and POP genes in these lethal mushrooms. Thus far, only A. palloides and A. bisporigera from North America and A. exitialis and A. rimosa from Asia have been studied based on transcriptome analysis. However, the MSDIN and POP genes of many amanitin-producing mushrooms in China remain unstudied; hence, the transcriptomes of these speices deserve to be analysed. Results: In this study, the MSDIN and POP genes from ten Amanita species, two Galerina species and Lepiota venenata were studied and the phylogenetic relationships of their MSDIN and POP genes were analysed. Through transcriptome sequencing and PCR cloning, 19 POP genes and 151 MSDIN genes predicted to encode 98 nonduplicated cyclopeptides, including α-amanitin, β-amanitin, phallacidin, phalloidin and 94 unknown peptides, were found in these species. Phylogenetic analysis showed that (1) MSDIN genes generally clustered depending on the taxonomy of the genus, while Amanita MSDIN genes clustered depending on the chemical substance; and (2) the POPA genes of Amanita, Galerina and Lepiota clustered and were separated into three different groups, but the POPB genes of the three distinct genera were clustered in a highly supported monophyletic group. Conclusions: These results indicate that lethal Amanita species have the genetic capacity to produce numerous cyclopeptides, most of which are unknown, while lethal Galerina and Lepiota species seem to only have the genetic capacity to produce α-amanitin. Additionally, the POPB phylogeny of Amanita, Galerina and Lepiota conflicts with the taxonomic status of the three genera, suggesting that underlying horizontal gene transfer has occurred among these three genera.