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Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach

Most species in the genus Amanita are ectomycorrhizal fungi comprising both edible and poisonous mushrooms. Some species produce potent cyclic peptide toxins, such as α-amanitin, which places them among the deadliest organisms known to mankind. These toxins and related cyclic peptides are encoded by...

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Autores principales: Zhou, Shengwen, Li, Xincan, Lüli, Yunjiao, Li, Xuan, Chen, Zuo H., Yuan, Pengcheng, Yang, Zhu L., Li, Guohong, Luo, Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7998459/
https://www.ncbi.nlm.nih.gov/pubmed/33799506
http://dx.doi.org/10.3390/jof7030204
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author Zhou, Shengwen
Li, Xincan
Lüli, Yunjiao
Li, Xuan
Chen, Zuo H.
Yuan, Pengcheng
Yang, Zhu L.
Li, Guohong
Luo, Hong
author_facet Zhou, Shengwen
Li, Xincan
Lüli, Yunjiao
Li, Xuan
Chen, Zuo H.
Yuan, Pengcheng
Yang, Zhu L.
Li, Guohong
Luo, Hong
author_sort Zhou, Shengwen
collection PubMed
description Most species in the genus Amanita are ectomycorrhizal fungi comprising both edible and poisonous mushrooms. Some species produce potent cyclic peptide toxins, such as α-amanitin, which places them among the deadliest organisms known to mankind. These toxins and related cyclic peptides are encoded by genes of the “MSDIN” family (named after the first five amino acid residues of the precursor peptides), and it is largely unknown to what extent these genes are expressed in the basidiocarps. In the present study, Amanita rimosa and Amanita exitialis were sequenced through the PacBio and Illumina techniques. Together with our two previously sequenced genomes, Amanita subjunquillea and Amanita pallidorosea, in total, 46 previously unknown MSDIN genes were discovered. The expression of over 80% of the MSDIN genes was demonstrated in A. subjunquillea. Through a combination of genomics and mass spectrometry, 12 MSDIN genes were shown to produce novel cyclic peptides. To further confirm the results, three of the cyclic peptides were chemically synthesized. The tandem mass spectrometry (MS/MS) spectra of the natural and the synthetic peptides shared a majority of the fragment ions, demonstrating an identical structure between each peptide pair. Collectively, the results suggested that the genome-guided approach is reliable for identifying novel cyclic peptides in Amanita species and that there is a large peptide reservoir in these mushrooms.
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spelling pubmed-79984592021-03-28 Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach Zhou, Shengwen Li, Xincan Lüli, Yunjiao Li, Xuan Chen, Zuo H. Yuan, Pengcheng Yang, Zhu L. Li, Guohong Luo, Hong J Fungi (Basel) Article Most species in the genus Amanita are ectomycorrhizal fungi comprising both edible and poisonous mushrooms. Some species produce potent cyclic peptide toxins, such as α-amanitin, which places them among the deadliest organisms known to mankind. These toxins and related cyclic peptides are encoded by genes of the “MSDIN” family (named after the first five amino acid residues of the precursor peptides), and it is largely unknown to what extent these genes are expressed in the basidiocarps. In the present study, Amanita rimosa and Amanita exitialis were sequenced through the PacBio and Illumina techniques. Together with our two previously sequenced genomes, Amanita subjunquillea and Amanita pallidorosea, in total, 46 previously unknown MSDIN genes were discovered. The expression of over 80% of the MSDIN genes was demonstrated in A. subjunquillea. Through a combination of genomics and mass spectrometry, 12 MSDIN genes were shown to produce novel cyclic peptides. To further confirm the results, three of the cyclic peptides were chemically synthesized. The tandem mass spectrometry (MS/MS) spectra of the natural and the synthetic peptides shared a majority of the fragment ions, demonstrating an identical structure between each peptide pair. Collectively, the results suggested that the genome-guided approach is reliable for identifying novel cyclic peptides in Amanita species and that there is a large peptide reservoir in these mushrooms. MDPI 2021-03-11 /pmc/articles/PMC7998459/ /pubmed/33799506 http://dx.doi.org/10.3390/jof7030204 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ).
spellingShingle Article
Zhou, Shengwen
Li, Xincan
Lüli, Yunjiao
Li, Xuan
Chen, Zuo H.
Yuan, Pengcheng
Yang, Zhu L.
Li, Guohong
Luo, Hong
Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title_full Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title_fullStr Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title_full_unstemmed Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title_short Novel Cyclic Peptides from Lethal Amanita Mushrooms through a Genome-Guided Approach
title_sort novel cyclic peptides from lethal amanita mushrooms through a genome-guided approach
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7998459/
https://www.ncbi.nlm.nih.gov/pubmed/33799506
http://dx.doi.org/10.3390/jof7030204
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