Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms

Circular RNAs (circRNAs), a novel class of ubiquitous and intriguing noncoding RNA, have been found in a number of eukaryotes but not yet basidiomycetes. In this study, we identified 73 circRNAs from 39.28 million filtered RNA reads from the basidiomycete Cryptococcus neoformans JEC21 using next-gen...

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Main Authors: Liang Huo, Ping Zhang, Chenxi Li, Kashif Rahim, Xiaoran Hao, Biyun Xiang, Xudong Zhu
Format: Article
Language:English
Published: MDPI AG 2018-02-01
Series:Genes
Subjects:
Online Access:http://www.mdpi.com/2073-4425/9/3/118
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spelling doaj-40737028ccba460589bb576fd26734e02020-11-24T22:45:23ZengMDPI AGGenes2073-44252018-02-019311810.3390/genes9030118genes9030118Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over KingdomsLiang Huo0Ping Zhang1Chenxi Li2Kashif Rahim3Xiaoran Hao4Biyun Xiang5Xudong Zhu6Beijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaBeijing Key Laboratory of Genetic Engineering Drug and Biotechnology, Institute of Biochemistry and Molecular Biology, College of Life Sciences, Beijing Normal University (CLS-BNU), Beijing 100875, ChinaCircular RNAs (circRNAs), a novel class of ubiquitous and intriguing noncoding RNA, have been found in a number of eukaryotes but not yet basidiomycetes. In this study, we identified 73 circRNAs from 39.28 million filtered RNA reads from the basidiomycete Cryptococcus neoformans JEC21 using next-generation sequencing (NGS) and the bioinformatics tool circular RNA identification (CIRI). Furthermore, mapping of newly found circRNAs to the genome showed that 73.97% of the circRNAs originated from exonic regions, whereas 20.55% were from intergenic regions and 5.48% were from intronic regions. Enrichment analysis of circRNA host genes was conducted based on the Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway databases. The results reveal that host genes are mainly responsible for primary metabolism and, interestingly, ribosomal protein production. Furthermore, we uncovered a high-level circRNA that was a transcript from the guanosine triphosphate (GTP)ase gene CNM01190 (gene ID: 3255052) in our yeast. Coincidentally, YPT5, CNM01190′s ortholog of the GTPase in Schizosaccharomyces pombe, protists, and humans, has already been proven to generate circRNAs. Additionally, overexpression of RNA debranching enzyme DBR1 had varied influence on the expression of circRNAs, indicating that multiple circRNA biosynthesis pathways exist in C. neoformans. Our study provides evidence for the existence of stable circRNAs in the opportunistic human pathogen C. neoformans and raises a question regarding their role related to pathogenesis in this yeast.http://www.mdpi.com/2073-4425/9/3/118Cryptococcus neoformansnext-generation sequencing (NGS)circRNAsRNA debranching enzymeGTPase-encoding gene
collection DOAJ
language English
format Article
sources DOAJ
author Liang Huo
Ping Zhang
Chenxi Li
Kashif Rahim
Xiaoran Hao
Biyun Xiang
Xudong Zhu
spellingShingle Liang Huo
Ping Zhang
Chenxi Li
Kashif Rahim
Xiaoran Hao
Biyun Xiang
Xudong Zhu
Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
Genes
Cryptococcus neoformans
next-generation sequencing (NGS)
circRNAs
RNA debranching enzyme
GTPase-encoding gene
author_facet Liang Huo
Ping Zhang
Chenxi Li
Kashif Rahim
Xiaoran Hao
Biyun Xiang
Xudong Zhu
author_sort Liang Huo
title Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
title_short Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
title_full Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
title_fullStr Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
title_full_unstemmed Genome-Wide Identification of circRNAs in Pathogenic Basidiomycetous Yeast Cryptococcus neoformans Suggests Conserved circRNA Host Genes over Kingdoms
title_sort genome-wide identification of circrnas in pathogenic basidiomycetous yeast cryptococcus neoformans suggests conserved circrna host genes over kingdoms
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2018-02-01
description Circular RNAs (circRNAs), a novel class of ubiquitous and intriguing noncoding RNA, have been found in a number of eukaryotes but not yet basidiomycetes. In this study, we identified 73 circRNAs from 39.28 million filtered RNA reads from the basidiomycete Cryptococcus neoformans JEC21 using next-generation sequencing (NGS) and the bioinformatics tool circular RNA identification (CIRI). Furthermore, mapping of newly found circRNAs to the genome showed that 73.97% of the circRNAs originated from exonic regions, whereas 20.55% were from intergenic regions and 5.48% were from intronic regions. Enrichment analysis of circRNA host genes was conducted based on the Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway databases. The results reveal that host genes are mainly responsible for primary metabolism and, interestingly, ribosomal protein production. Furthermore, we uncovered a high-level circRNA that was a transcript from the guanosine triphosphate (GTP)ase gene CNM01190 (gene ID: 3255052) in our yeast. Coincidentally, YPT5, CNM01190′s ortholog of the GTPase in Schizosaccharomyces pombe, protists, and humans, has already been proven to generate circRNAs. Additionally, overexpression of RNA debranching enzyme DBR1 had varied influence on the expression of circRNAs, indicating that multiple circRNA biosynthesis pathways exist in C. neoformans. Our study provides evidence for the existence of stable circRNAs in the opportunistic human pathogen C. neoformans and raises a question regarding their role related to pathogenesis in this yeast.
topic Cryptococcus neoformans
next-generation sequencing (NGS)
circRNAs
RNA debranching enzyme
GTPase-encoding gene
url http://www.mdpi.com/2073-4425/9/3/118
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AT pingzhang genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
AT chenxili genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
AT kashifrahim genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
AT xiaoranhao genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
AT biyunxiang genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
AT xudongzhu genomewideidentificationofcircrnasinpathogenicbasidiomycetousyeastcryptococcusneoformanssuggestsconservedcircrnahostgenesoverkingdoms
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