Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis
ABSTRACT The gut microbiota plays an essential role in the regulation of the immune system and the etiology of human autoimmune diseases. However, a holistic understanding of the gut bacteriome, mycobiome, and virome in patients with osteoarthritis (OA) remains lacking. Here, we explored the gut mic...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01711-22 |
| _version_ | 1811164382181195776 |
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| author | Changming Chen Yue Zhang Xueming Yao Shenghui Li Guangyang Wang Ying Huang Yutao Yang Aiqin Zhang Can Liu Dan Zhu Hufan Li Qiulong Yan Wukai Ma |
| author_facet | Changming Chen Yue Zhang Xueming Yao Shenghui Li Guangyang Wang Ying Huang Yutao Yang Aiqin Zhang Can Liu Dan Zhu Hufan Li Qiulong Yan Wukai Ma |
| author_sort | Changming Chen |
| collection | DOAJ |
| description | ABSTRACT The gut microbiota plays an essential role in the regulation of the immune system and the etiology of human autoimmune diseases. However, a holistic understanding of the gut bacteriome, mycobiome, and virome in patients with osteoarthritis (OA) remains lacking. Here, we explored the gut microbiotas of 44 OA patients and 46 healthy volunteers via deep whole-metagenome shotgun sequencing of their fecal samples. The gut bacteriome and mycobiome were analyzed using a reference-based strategy. Gut viruses were identified from the metagenomic assembled contigs, and the gut virome was profiled based on 6,567 nonredundant viral operational taxonomic units (vOTUs). We revealed that the gut microbiome (including bacteriome, mycobiome, and virome) of OA patients is fundamentally altered, characterized by a panel of 279 differentially abundant bacterial species, 10 fungal species, and 627 vOTUs. The representative OA-enriched bacteria included Anaerostipes hadrus (GENOME147149), Prevotella sp900313215 (GENOME08259), Eubacterium_E hallii (GENOME000299), and Blautia A (GENOME001004), while Bacteroides plebeius A (GENOME239725), Roseburia inulinivorans (GENOME 001770), Dialister sp900343095 (GENOME075103), Phascolarctobacterium faecium (GENOME233517), and several members of Faecalibacterium and Prevotella were depleted in OA patients. Fungi such as Debaryomyces fabryi (GenBank accession no. GCA_003708665), Candida parapsilosis (GCA_000182765), and Apophysomyces trapeziformis (GCA_000696975) were enriched in the OA gut microbiota, and Malassezia restricta (GCA_003290485), Aspergillus fumigatus (GCA_003069565), and Mucor circinelloides (GCA_010203745) were depleted. The OA-depleted viruses spanned Siphoviridae (95 vOTUs), Myoviridae (70 vOTUs), and Microviridae (5 vOTUs), while 30 Siphoviridae vOTUs were enriched in OA patients. Functional analysis of the gut bacteriome and virome also uncovered their functional signatures in relation to OA. Moreover, we demonstrated that the OA-associated gut bacterial and viral signatures are tightly interconnected, suggesting that they may impact disease together. Finally, we showed that the multikingdom signatures are effective in discriminating the OA patients from healthy controls, suggesting the potential of gut microbiota for the prediction of OA and related diseases. Our results delineated the fecal bacteriome, mycobiome, and virome landscapes of the OA microbiota and provided biomarkers that will aid in future mechanistic and clinical intervention studies. IMPORTANCE The gut microbiome of OA patients was completely altered compared to that in healthy individuals, including 279 differentially abundant bacterial species, 10 fungal species and 627 viral operational taxonomic units (vOTUs). Functional analysis of the gut bacteriome and virome also revealed their functional signatures in relation to OA. We found that OA-associated gut bacterial and viral signatures were tightly interconnected, indicating that they may affect the disease together. The OA patients can be discriminated effectively from healthy controls using the multikingdom signatures, suggesting the potential of gut microbiota for the prediction of OA and related diseases. |
| first_indexed | 2024-04-10T15:20:38Z |
| format | Article |
| id | doaj.art-91572f320ae242c9a2604f0df23c7af3 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-10T15:20:38Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-91572f320ae242c9a2604f0df23c7af32023-02-14T14:15:51ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.01711-22Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with OsteoarthritisChangming Chen0Yue Zhang1Xueming Yao2Shenghui Li3Guangyang Wang4Ying Huang5Yutao Yang6Aiqin Zhang7Can Liu8Dan Zhu9Hufan Li10Qiulong Yan11Wukai Ma12Department of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaPuensum Genetech Institute, Wuhan, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaPuensum Genetech Institute, Wuhan, ChinaDepartment of Microbiology, College of Basic Medical Sciences, Dalian Medical University, Dalian, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaPuensum Genetech Institute, Wuhan, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaDepartment of Microbiology, College of Basic Medical Sciences, Dalian Medical University, Dalian, ChinaDepartment of Rheumatology and Immunology, The Second Affiliated Hospital of Guizhou University of Traditional Chinese Medicine, Guiyang, ChinaABSTRACT The gut microbiota plays an essential role in the regulation of the immune system and the etiology of human autoimmune diseases. However, a holistic understanding of the gut bacteriome, mycobiome, and virome in patients with osteoarthritis (OA) remains lacking. Here, we explored the gut microbiotas of 44 OA patients and 46 healthy volunteers via deep whole-metagenome shotgun sequencing of their fecal samples. The gut bacteriome and mycobiome were analyzed using a reference-based strategy. Gut viruses were identified from the metagenomic assembled contigs, and the gut virome was profiled based on 6,567 nonredundant viral operational taxonomic units (vOTUs). We revealed that the gut microbiome (including bacteriome, mycobiome, and virome) of OA patients is fundamentally altered, characterized by a panel of 279 differentially abundant bacterial species, 10 fungal species, and 627 vOTUs. The representative OA-enriched bacteria included Anaerostipes hadrus (GENOME147149), Prevotella sp900313215 (GENOME08259), Eubacterium_E hallii (GENOME000299), and Blautia A (GENOME001004), while Bacteroides plebeius A (GENOME239725), Roseburia inulinivorans (GENOME 001770), Dialister sp900343095 (GENOME075103), Phascolarctobacterium faecium (GENOME233517), and several members of Faecalibacterium and Prevotella were depleted in OA patients. Fungi such as Debaryomyces fabryi (GenBank accession no. GCA_003708665), Candida parapsilosis (GCA_000182765), and Apophysomyces trapeziformis (GCA_000696975) were enriched in the OA gut microbiota, and Malassezia restricta (GCA_003290485), Aspergillus fumigatus (GCA_003069565), and Mucor circinelloides (GCA_010203745) were depleted. The OA-depleted viruses spanned Siphoviridae (95 vOTUs), Myoviridae (70 vOTUs), and Microviridae (5 vOTUs), while 30 Siphoviridae vOTUs were enriched in OA patients. Functional analysis of the gut bacteriome and virome also uncovered their functional signatures in relation to OA. Moreover, we demonstrated that the OA-associated gut bacterial and viral signatures are tightly interconnected, suggesting that they may impact disease together. Finally, we showed that the multikingdom signatures are effective in discriminating the OA patients from healthy controls, suggesting the potential of gut microbiota for the prediction of OA and related diseases. Our results delineated the fecal bacteriome, mycobiome, and virome landscapes of the OA microbiota and provided biomarkers that will aid in future mechanistic and clinical intervention studies. IMPORTANCE The gut microbiome of OA patients was completely altered compared to that in healthy individuals, including 279 differentially abundant bacterial species, 10 fungal species and 627 viral operational taxonomic units (vOTUs). Functional analysis of the gut bacteriome and virome also revealed their functional signatures in relation to OA. We found that OA-associated gut bacterial and viral signatures were tightly interconnected, indicating that they may affect the disease together. The OA patients can be discriminated effectively from healthy controls using the multikingdom signatures, suggesting the potential of gut microbiota for the prediction of OA and related diseases.https://journals.asm.org/doi/10.1128/spectrum.01711-22osteoarthritiswhole-metagenome shotgun sequencinggut bacteriomegut mycobiomegut viromemicrobiota dysbiosis |
| spellingShingle | Changming Chen Yue Zhang Xueming Yao Shenghui Li Guangyang Wang Ying Huang Yutao Yang Aiqin Zhang Can Liu Dan Zhu Hufan Li Qiulong Yan Wukai Ma Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis Microbiology Spectrum osteoarthritis whole-metagenome shotgun sequencing gut bacteriome gut mycobiome gut virome microbiota dysbiosis |
| title | Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis |
| title_full | Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis |
| title_fullStr | Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis |
| title_full_unstemmed | Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis |
| title_short | Characterizations of the Gut Bacteriome, Mycobiome, and Virome in Patients with Osteoarthritis |
| title_sort | characterizations of the gut bacteriome mycobiome and virome in patients with osteoarthritis |
| topic | osteoarthritis whole-metagenome shotgun sequencing gut bacteriome gut mycobiome gut virome microbiota dysbiosis |
| url | https://journals.asm.org/doi/10.1128/spectrum.01711-22 |
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