Nanopore sequencing of full rRNA operon improves resolution in mycobiome analysis and reveals high diversity in both human gut and environments
High‐throughput sequencing has substantially improved our understanding of fungal diversity. However, the short read (
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| Veröffentlicht in: | Molecular ecology 2023-12, Vol.32 (23), p.6330-6344 |
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| container_title | Molecular ecology |
| container_volume | 32 |
| creator | Lu, Jingjing Zhang, Xudong Zhang, Xuan Wang, Linqi Zhao, Ruilin Liu, Xiao Yong Liu, Xinzhan Zhuang, Wenying Chen, Liang Cai, Lei Wang, Jun |
| description | High‐throughput sequencing has substantially improved our understanding of fungal diversity. However, the short read ( |
| doi_str_mv | 10.1111/mec.16534 |
| format | Article |
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However, the short read (<500 bp) length of current second‐generation sequencing approaches provides limited taxonomic and phylogenetic resolution for species discrimination. Longer sequences containing more information are highly desired to provide greater taxonomic resolution. Here, we amplified full‐length rRNA operons (~5.5 kb) and established a corresponding fungal rRNA operon database for ONT sequences (FRODO), which contains ONT sequences representing eight phyla, 41 classes, 109 orders, 256 families, 524 genera and 1116 species. We also benchmarked the optimal method for sequence classification and determined that the RDP classifier based on our FRODO database was capable of improving the classification of ONT reads, with an average of 98%–99% reads correctly classified at the genus or species level. We investigated the applicability of our approach in three representative mycobiomes, namely, the soil, marine and human gut mycobiomes, and found that the gut contains the largest number of unknown species (over 90%), followed by the marine (42%) and soil (33.8%) mycobiomes. We also observed a distinct difference in the composition of the marine and soil mycobiomes, with the highest richness and diversity detected in soils. Overall, our study provides a systematic approach for mycobiome studies and revealed that the previous methods might have underestimated the diversity of mycobiome species. Future application of this method will lead to a better understanding of the taxonomic and functional diversity of fungi in environmental and health‐related mycobiomes.</description><identifier>ISSN: 0962-1083</identifier><identifier>ISSN: 1365-294X</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.16534</identifier><identifier>PMID: 35593386</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Classification ; FRODO database ; full‐length rRNA operons ; fungal metabarcoding ; Fungi ; Fungi - genetics ; Genera ; High-Throughput Nucleotide Sequencing - methods ; Humans ; Mycobiome - genetics ; Nanopore Sequencing ; Operons ; Oxford nanopore technology ; Phylogeny ; rRNA ; rRNA Operon ; Soil ; Soils ; Species ; Species diversity ; Taxonomy</subject><ispartof>Molecular ecology, 2023-12, Vol.32 (23), p.6330-6344</ispartof><rights>2022 John Wiley & Sons Ltd.</rights><rights>Copyright © 2023 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3534-9afb7cde1e5b8f6c9442d7aeba333beafd424405b3007e24ebcb731a393d76683</citedby><cites>FETCH-LOGICAL-c3534-9afb7cde1e5b8f6c9442d7aeba333beafd424405b3007e24ebcb731a393d76683</cites><orcidid>0000-0002-6527-9829 ; 0000-0002-8131-7274</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.16534$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.16534$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35593386$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lu, Jingjing</creatorcontrib><creatorcontrib>Zhang, Xudong</creatorcontrib><creatorcontrib>Zhang, Xuan</creatorcontrib><creatorcontrib>Wang, Linqi</creatorcontrib><creatorcontrib>Zhao, Ruilin</creatorcontrib><creatorcontrib>Liu, Xiao Yong</creatorcontrib><creatorcontrib>Liu, Xinzhan</creatorcontrib><creatorcontrib>Zhuang, Wenying</creatorcontrib><creatorcontrib>Chen, Liang</creatorcontrib><creatorcontrib>Cai, Lei</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><title>Nanopore sequencing of full rRNA operon improves resolution in mycobiome analysis and reveals high diversity in both human gut and environments</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>High‐throughput sequencing has substantially improved our understanding of fungal diversity. However, the short read (<500 bp) length of current second‐generation sequencing approaches provides limited taxonomic and phylogenetic resolution for species discrimination. Longer sequences containing more information are highly desired to provide greater taxonomic resolution. Here, we amplified full‐length rRNA operons (~5.5 kb) and established a corresponding fungal rRNA operon database for ONT sequences (FRODO), which contains ONT sequences representing eight phyla, 41 classes, 109 orders, 256 families, 524 genera and 1116 species. We also benchmarked the optimal method for sequence classification and determined that the RDP classifier based on our FRODO database was capable of improving the classification of ONT reads, with an average of 98%–99% reads correctly classified at the genus or species level. We investigated the applicability of our approach in three representative mycobiomes, namely, the soil, marine and human gut mycobiomes, and found that the gut contains the largest number of unknown species (over 90%), followed by the marine (42%) and soil (33.8%) mycobiomes. We also observed a distinct difference in the composition of the marine and soil mycobiomes, with the highest richness and diversity detected in soils. Overall, our study provides a systematic approach for mycobiome studies and revealed that the previous methods might have underestimated the diversity of mycobiome species. Future application of this method will lead to a better understanding of the taxonomic and functional diversity of fungi in environmental and health‐related mycobiomes.</description><subject>Classification</subject><subject>FRODO database</subject><subject>full‐length rRNA operons</subject><subject>fungal metabarcoding</subject><subject>Fungi</subject><subject>Fungi - genetics</subject><subject>Genera</subject><subject>High-Throughput Nucleotide Sequencing - methods</subject><subject>Humans</subject><subject>Mycobiome - genetics</subject><subject>Nanopore Sequencing</subject><subject>Operons</subject><subject>Oxford nanopore technology</subject><subject>Phylogeny</subject><subject>rRNA</subject><subject>rRNA Operon</subject><subject>Soil</subject><subject>Soils</subject><subject>Species</subject><subject>Species diversity</subject><subject>Taxonomy</subject><issn>0962-1083</issn><issn>1365-294X</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9q3DAQxkVpabZpD32BIuilPTiRLEuyjmFJ_0CaQGihNyPJ410FS9pK9hY_RV852myaQ6FzmWH4zTd8fAi9peSMljr3YM-o4Kx5hlaUCV7Vqvn5HK2IEnVFSctO0Kuc7wihrOb8JTphnCvGWrFCf651iLuYAGf4NUOwLmxwHPAwjyNOt9cXOO4gxYCd36W4h4wT5DjOkzvsAvaLjcZFD1gHPS7Z5TL0BdqDHjPeus0W924PKbtpORyYOG3xdvY64M08PcAQ9q688BCm_Bq9GMohvHnsp-jHp8vv6y_V1c3nr-uLq8qy4rNSejDS9kCBm3YQVjVN3UsNRjPGDOihb-qmIdwwQiTUDRhrJKOaKdZLIVp2ij4cdYur4jtPnXfZwjjqAHHOXS2ElK1qpSzo-3_Quzin4rZQraoVJ7JWhfp4pGyKOScYul1yXqelo6Q7pNSVlLqHlAr77lFxNh76J_JvLAU4PwK_3QjL_5W6b5fro-Q97QKe0A</recordid><startdate>202312</startdate><enddate>202312</enddate><creator>Lu, Jingjing</creator><creator>Zhang, Xudong</creator><creator>Zhang, Xuan</creator><creator>Wang, Linqi</creator><creator>Zhao, Ruilin</creator><creator>Liu, Xiao Yong</creator><creator>Liu, Xinzhan</creator><creator>Zhuang, Wenying</creator><creator>Chen, Liang</creator><creator>Cai, Lei</creator><creator>Wang, Jun</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-6527-9829</orcidid><orcidid>https://orcid.org/0000-0002-8131-7274</orcidid></search><sort><creationdate>202312</creationdate><title>Nanopore sequencing of full rRNA operon improves resolution in mycobiome analysis and reveals high diversity in both human gut and environments</title><author>Lu, Jingjing ; Zhang, Xudong ; Zhang, Xuan ; Wang, Linqi ; Zhao, Ruilin ; Liu, Xiao Yong ; Liu, Xinzhan ; Zhuang, Wenying ; Chen, Liang ; Cai, Lei ; Wang, Jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3534-9afb7cde1e5b8f6c9442d7aeba333beafd424405b3007e24ebcb731a393d76683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Classification</topic><topic>FRODO database</topic><topic>full‐length rRNA operons</topic><topic>fungal metabarcoding</topic><topic>Fungi</topic><topic>Fungi - genetics</topic><topic>Genera</topic><topic>High-Throughput Nucleotide Sequencing - methods</topic><topic>Humans</topic><topic>Mycobiome - genetics</topic><topic>Nanopore Sequencing</topic><topic>Operons</topic><topic>Oxford nanopore technology</topic><topic>Phylogeny</topic><topic>rRNA</topic><topic>rRNA Operon</topic><topic>Soil</topic><topic>Soils</topic><topic>Species</topic><topic>Species diversity</topic><topic>Taxonomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lu, Jingjing</creatorcontrib><creatorcontrib>Zhang, Xudong</creatorcontrib><creatorcontrib>Zhang, Xuan</creatorcontrib><creatorcontrib>Wang, Linqi</creatorcontrib><creatorcontrib>Zhao, Ruilin</creatorcontrib><creatorcontrib>Liu, Xiao Yong</creatorcontrib><creatorcontrib>Liu, Xinzhan</creatorcontrib><creatorcontrib>Zhuang, Wenying</creatorcontrib><creatorcontrib>Chen, Liang</creatorcontrib><creatorcontrib>Cai, Lei</creatorcontrib><creatorcontrib>Wang, Jun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lu, Jingjing</au><au>Zhang, Xudong</au><au>Zhang, Xuan</au><au>Wang, Linqi</au><au>Zhao, Ruilin</au><au>Liu, Xiao Yong</au><au>Liu, Xinzhan</au><au>Zhuang, Wenying</au><au>Chen, Liang</au><au>Cai, Lei</au><au>Wang, Jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nanopore sequencing of full rRNA operon improves resolution in mycobiome analysis and reveals high diversity in both human gut and environments</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2023-12</date><risdate>2023</risdate><volume>32</volume><issue>23</issue><spage>6330</spage><epage>6344</epage><pages>6330-6344</pages><issn>0962-1083</issn><issn>1365-294X</issn><eissn>1365-294X</eissn><abstract>High‐throughput sequencing has substantially improved our understanding of fungal diversity. However, the short read (<500 bp) length of current second‐generation sequencing approaches provides limited taxonomic and phylogenetic resolution for species discrimination. Longer sequences containing more information are highly desired to provide greater taxonomic resolution. Here, we amplified full‐length rRNA operons (~5.5 kb) and established a corresponding fungal rRNA operon database for ONT sequences (FRODO), which contains ONT sequences representing eight phyla, 41 classes, 109 orders, 256 families, 524 genera and 1116 species. We also benchmarked the optimal method for sequence classification and determined that the RDP classifier based on our FRODO database was capable of improving the classification of ONT reads, with an average of 98%–99% reads correctly classified at the genus or species level. We investigated the applicability of our approach in three representative mycobiomes, namely, the soil, marine and human gut mycobiomes, and found that the gut contains the largest number of unknown species (over 90%), followed by the marine (42%) and soil (33.8%) mycobiomes. We also observed a distinct difference in the composition of the marine and soil mycobiomes, with the highest richness and diversity detected in soils. Overall, our study provides a systematic approach for mycobiome studies and revealed that the previous methods might have underestimated the diversity of mycobiome species. Future application of this method will lead to a better understanding of the taxonomic and functional diversity of fungi in environmental and health‐related mycobiomes.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>35593386</pmid><doi>10.1111/mec.16534</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-6527-9829</orcidid><orcidid>https://orcid.org/0000-0002-8131-7274</orcidid></addata></record> |
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| ispartof | Molecular ecology, 2023-12, Vol.32 (23), p.6330-6344 |
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| source | MEDLINE; Access via Wiley Online Library |
| subjects | Classification FRODO database full‐length rRNA operons fungal metabarcoding Fungi Fungi - genetics Genera High-Throughput Nucleotide Sequencing - methods Humans Mycobiome - genetics Nanopore Sequencing Operons Oxford nanopore technology Phylogeny rRNA rRNA Operon Soil Soils Species Species diversity Taxonomy |
| title | Nanopore sequencing of full rRNA operon improves resolution in mycobiome analysis and reveals high diversity in both human gut and environments |
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