Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika
ABSTRACT Rarely has the vast diversity of bacteria on Earth been profiled, particularly on inaccessible plateaus. These uncultured microbes, which are also known as “microbial dark matter,” may play crucial roles in maintaining the ecosystem and are linked to human health, regarding pathogenicity an...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03495-22 |
| _version_ | 1827925138241224704 |
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| author | Ji Pu Jing Yang Shan Lu Dong Jin Xuelian Luo Yanwen Xiong Xiangning Bai Wentao Zhu Yuyuan Huang Shusheng Wu Lina Niu Liyun Liu Jianguo Xu |
| author_facet | Ji Pu Jing Yang Shan Lu Dong Jin Xuelian Luo Yanwen Xiong Xiangning Bai Wentao Zhu Yuyuan Huang Shusheng Wu Lina Niu Liyun Liu Jianguo Xu |
| author_sort | Ji Pu |
| collection | DOAJ |
| description | ABSTRACT Rarely has the vast diversity of bacteria on Earth been profiled, particularly on inaccessible plateaus. These uncultured microbes, which are also known as “microbial dark matter,” may play crucial roles in maintaining the ecosystem and are linked to human health, regarding pathogenicity and prebioticity. The plateau pika (Ochotona curzoniae) is a small burrowing steppe lagomorph that is endemic to the Qinghai-Tibetan Plateau and is a keystone species in the maintenance of ecological balance. We used a combination of full-length 16S rRNA amplicon sequencing, shotgun metagenomics, and metabolomics to elucidate the species-level community structure and the metabolic potential of the gut microbiota of the plateau pika. Using a full-length 16S rRNA metataxonomic approach, we clustered 618 (166 ± 35 per sample) operational phylogenetic units (OPUs) from 105 plateau pika samples and assigned them to 215 known species, 226 potentially new species, and 177 higher hierarchical taxa. Notably, 39 abundant OPUs (over 60% total relative abundance) are found in over 90% of the samples, thereby representing a “core microbiota.” They are all classified as novel microbial lineages, from the class to the species level. Using metagenomic reads, we independently assembled and binned 109 high-quality, species-level genome bins (SGBs). Then, a precise taxonomic assignment was performed to clarify the phylogenetic consistency of the SGBs and the 16S rRNA amplicons. Thus, the majority of the core microbes possess their genomes. SGBs belonging to the genus Treponema, the families Muribaculaceae, Lachnospiraceae, and Oscillospiraceae, and the order Eubacteriales are abundant in the metagenomic samples. In addition, multiple CAZymes are detected in these SGBs, indicating their efficient utilization of plant biomass. As the most widely connected metabolite with the core microbiota, tryptophan may relate to host environmental adaptation. Our investigation allows for a greater comprehension of the composition and functional capacity of the gut microbiota of the plateau pika. IMPORTANCE The great majority of microbial species remain uncultured, severely limiting their taxonomic characterization and biological understanding. The plateau pika (Ochotona curzoniae) is a small burrowing steppe lagomorph that is endemic to the Qinghai-Tibetan Plateau and is considered to be the keystone species in the maintenance of ecological stability. We comprehensively investigated the gut microbiota of the plateau pika via a multiomics endeavor. Combining full-length 16S rRNA metataxonomics, shotgun metagenomics, and metabolomics, we elucidated the species-level taxonomic assignment of the core uncultured intestinal microbiota of the plateau pika and revealed their correlation to host nutritional metabolism and adaptation. Our findings provide insights into the microbial diversity and biological significance of alpine animals. |
| first_indexed | 2024-03-13T05:20:56Z |
| format | Article |
| id | doaj.art-1b90a4c811d24aee821c7359c6caf0b8 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:20:56Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-1b90a4c811d24aee821c7359c6caf0b82023-06-15T13:18:31ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.03495-22Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau PikaJi Pu0Jing Yang1Shan Lu2Dong Jin3Xuelian Luo4Yanwen Xiong5Xiangning Bai6Wentao Zhu7Yuyuan Huang8Shusheng Wu9Lina Niu10Liyun Liu11Jianguo Xu12State Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaYushu Prefecture Center for Disease Control and Prevention, Yushu, ChinaKey Laboratory of Tropical Translational Medicine of Ministry of Education, Hainan Medical University, Haikou, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaState Key Laboratory of Infectious Disease Prevention and Control and National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, ChinaABSTRACT Rarely has the vast diversity of bacteria on Earth been profiled, particularly on inaccessible plateaus. These uncultured microbes, which are also known as “microbial dark matter,” may play crucial roles in maintaining the ecosystem and are linked to human health, regarding pathogenicity and prebioticity. The plateau pika (Ochotona curzoniae) is a small burrowing steppe lagomorph that is endemic to the Qinghai-Tibetan Plateau and is a keystone species in the maintenance of ecological balance. We used a combination of full-length 16S rRNA amplicon sequencing, shotgun metagenomics, and metabolomics to elucidate the species-level community structure and the metabolic potential of the gut microbiota of the plateau pika. Using a full-length 16S rRNA metataxonomic approach, we clustered 618 (166 ± 35 per sample) operational phylogenetic units (OPUs) from 105 plateau pika samples and assigned them to 215 known species, 226 potentially new species, and 177 higher hierarchical taxa. Notably, 39 abundant OPUs (over 60% total relative abundance) are found in over 90% of the samples, thereby representing a “core microbiota.” They are all classified as novel microbial lineages, from the class to the species level. Using metagenomic reads, we independently assembled and binned 109 high-quality, species-level genome bins (SGBs). Then, a precise taxonomic assignment was performed to clarify the phylogenetic consistency of the SGBs and the 16S rRNA amplicons. Thus, the majority of the core microbes possess their genomes. SGBs belonging to the genus Treponema, the families Muribaculaceae, Lachnospiraceae, and Oscillospiraceae, and the order Eubacteriales are abundant in the metagenomic samples. In addition, multiple CAZymes are detected in these SGBs, indicating their efficient utilization of plant biomass. As the most widely connected metabolite with the core microbiota, tryptophan may relate to host environmental adaptation. Our investigation allows for a greater comprehension of the composition and functional capacity of the gut microbiota of the plateau pika. IMPORTANCE The great majority of microbial species remain uncultured, severely limiting their taxonomic characterization and biological understanding. The plateau pika (Ochotona curzoniae) is a small burrowing steppe lagomorph that is endemic to the Qinghai-Tibetan Plateau and is considered to be the keystone species in the maintenance of ecological stability. We comprehensively investigated the gut microbiota of the plateau pika via a multiomics endeavor. Combining full-length 16S rRNA metataxonomics, shotgun metagenomics, and metabolomics, we elucidated the species-level taxonomic assignment of the core uncultured intestinal microbiota of the plateau pika and revealed their correlation to host nutritional metabolism and adaptation. Our findings provide insights into the microbial diversity and biological significance of alpine animals.https://journals.asm.org/doi/10.1128/spectrum.03495-2216S rRNAOchotona curzoniaespecies-levelmetabolomicsmetagenomicsmetataxonomics |
| spellingShingle | Ji Pu Jing Yang Shan Lu Dong Jin Xuelian Luo Yanwen Xiong Xiangning Bai Wentao Zhu Yuyuan Huang Shusheng Wu Lina Niu Liyun Liu Jianguo Xu Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika Microbiology Spectrum 16S rRNA Ochotona curzoniae species-level metabolomics metagenomics metataxonomics |
| title | Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika |
| title_full | Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika |
| title_fullStr | Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika |
| title_full_unstemmed | Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika |
| title_short | Species-Level Taxonomic Characterization of Uncultured Core Gut Microbiota of Plateau Pika |
| title_sort | species level taxonomic characterization of uncultured core gut microbiota of plateau pika |
| topic | 16S rRNA Ochotona curzoniae species-level metabolomics metagenomics metataxonomics |
| url | https://journals.asm.org/doi/10.1128/spectrum.03495-22 |
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