Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)

ABSTRACT Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Protein-coding operons have not been reported in the Fungi even though they represent a very diverse kingdom of organisms. Here, we report a functional operon involved in the secondary me...

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Autores principales:	Qun Yue, Li Chen, Yan Li, Gerald F. Bills, Xinyu Zhang, Meichun Xiang, Shaojie Li, Yongsheng Che, Chengshu Wang, Xuemei Niu, Zhiqiang An, Xingzhong Liu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/63300983172d4693916710932bb617b8
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spelling	oai:doaj.org-article:63300983172d4693916710932bb617b82021-11-15T15:49:02ZFunctional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)10.1128/mBio.00703-152150-7511https://doaj.org/article/63300983172d4693916710932bb617b82015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00703-15https://doaj.org/toc/2150-7511ABSTRACT Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Protein-coding operons have not been reported in the Fungi even though they represent a very diverse kingdom of organisms. Here, we report a functional operon involved in the secondary metabolism of the fungus Glarea lozoyensis belonging to Leotiomycetes (Ascomycota). Two contiguous genes, glpks3 and glnrps7, encoding polyketide synthase and nonribosomal peptide synthetase, respectively, are cotranscribed into one dicistronic mRNA under the control of the same promoter, and the mRNA is then translated into two individual proteins, GLPKS3 and GLNRPS7. Heterologous expression in Aspergillus nidulans shows that the GLPKS3-GLNRPS7 enzyme complex catalyzes the biosynthesis of a novel pyrrolidinedione-containing compound, xenolozoyenone (compound 1), which indicates the operon is functional. Although it is structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus has a monophylogenic origin from fungi rather than having been horizontally transferred from prokaryotes. Moreover, two additional operons, glpks28-glnrps8 and glpks29-glnrps9, were verified at the transcriptional level in the same fungus. This is the first report of protein-coding operons in a member of the Fungi. IMPORTANCE Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Three operon-like gene structures for secondary metabolism that were discovered in the filamentous fungus Glarea lozoyensis are the first examples of protein-coding operons identified in a member of the Fungi. Among them, the glpks3-glnrps7 operon is responsible for the biosynthesis of xenolozoyenone, which is a novel tetramic acid-containing compound. Although structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus did not result from horizontal gene transfer from prokaryotes. In addition, operonlike structures have been predicted in silico to be common in other fungi. The common occurrence and operonlike structure in fungi provide evolutionary insight and essential data for eukaryotic gene transcription.Qun YueLi ChenYan LiGerald F. BillsXinyu ZhangMeichun XiangShaojie LiYongsheng CheChengshu WangXuemei NiuZhiqiang AnXingzhong LiuAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Qun Yue Li Chen Yan Li Gerald F. Bills Xinyu Zhang Meichun Xiang Shaojie Li Yongsheng Che Chengshu Wang Xuemei Niu Zhiqiang An Xingzhong Liu Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
description	ABSTRACT Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Protein-coding operons have not been reported in the Fungi even though they represent a very diverse kingdom of organisms. Here, we report a functional operon involved in the secondary metabolism of the fungus Glarea lozoyensis belonging to Leotiomycetes (Ascomycota). Two contiguous genes, glpks3 and glnrps7, encoding polyketide synthase and nonribosomal peptide synthetase, respectively, are cotranscribed into one dicistronic mRNA under the control of the same promoter, and the mRNA is then translated into two individual proteins, GLPKS3 and GLNRPS7. Heterologous expression in Aspergillus nidulans shows that the GLPKS3-GLNRPS7 enzyme complex catalyzes the biosynthesis of a novel pyrrolidinedione-containing compound, xenolozoyenone (compound 1), which indicates the operon is functional. Although it is structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus has a monophylogenic origin from fungi rather than having been horizontally transferred from prokaryotes. Moreover, two additional operons, glpks28-glnrps8 and glpks29-glnrps9, were verified at the transcriptional level in the same fungus. This is the first report of protein-coding operons in a member of the Fungi. IMPORTANCE Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Three operon-like gene structures for secondary metabolism that were discovered in the filamentous fungus Glarea lozoyensis are the first examples of protein-coding operons identified in a member of the Fungi. Among them, the glpks3-glnrps7 operon is responsible for the biosynthesis of xenolozoyenone, which is a novel tetramic acid-containing compound. Although structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus did not result from horizontal gene transfer from prokaryotes. In addition, operonlike structures have been predicted in silico to be common in other fungi. The common occurrence and operonlike structure in fungi provide evolutionary insight and essential data for eukaryotic gene transcription.
format	article
author	Qun Yue Li Chen Yan Li Gerald F. Bills Xinyu Zhang Meichun Xiang Shaojie Li Yongsheng Che Chengshu Wang Xuemei Niu Zhiqiang An Xingzhong Liu
author_facet	Qun Yue Li Chen Yan Li Gerald F. Bills Xinyu Zhang Meichun Xiang Shaojie Li Yongsheng Che Chengshu Wang Xuemei Niu Zhiqiang An Xingzhong Liu
author_sort	Qun Yue
title	Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
title_short	Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
title_full	Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
title_fullStr	Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
title_full_unstemmed	Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)
title_sort	functional operons in secondary metabolic gene clusters in <italic toggle="yes">glarea lozoyensis</italic> (fungi, ascomycota, leotiomycetes)
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/63300983172d4693916710932bb617b8
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Functional Operons in Secondary Metabolic Gene Clusters in <italic toggle="yes">Glarea lozoyensis</italic> (Fungi, Ascomycota, Leotiomycetes)

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