Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection
ABSTRACT This study compared intestinal DNA phage dynamics and gut microbiota changes observed at the onset of coronavirus disease 2019 (COVID-19). The study participants included 19 healthy individuals and 19 patients with severe acute respiratory syndrome coronavirus 2 infection. Significant diffe...
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American Society for Microbiology
2025-01-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00998-24 |
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| author | Aya Ishizaka Azumi Tamura Michiko Koga Taketoshi Mizutani Seiya Yamayoshi Kiyoko Iwatsuki-Horimoto Atsuhiro Yasuhara Shinya Yamamoto Hiroyuki Nagai Eisuke Adachi Yutaka Suzuki Yoshihiro Kawaoka Hiroshi Yotsuyanagi |
| author_facet | Aya Ishizaka Azumi Tamura Michiko Koga Taketoshi Mizutani Seiya Yamayoshi Kiyoko Iwatsuki-Horimoto Atsuhiro Yasuhara Shinya Yamamoto Hiroyuki Nagai Eisuke Adachi Yutaka Suzuki Yoshihiro Kawaoka Hiroshi Yotsuyanagi |
| author_sort | Aya Ishizaka |
| collection | DOAJ |
| description | ABSTRACT This study compared intestinal DNA phage dynamics and gut microbiota changes observed at the onset of coronavirus disease 2019 (COVID-19). The study participants included 19 healthy individuals and 19 patients with severe acute respiratory syndrome coronavirus 2 infection. Significant differences were observed in the diversity of the intestinal DNA virome after the onset of COVID-19 compared with that in healthy individuals. Classification by their tail morphology resulted in the order Caudovirales, a double-stranded DNA phage, accounting for >95% of all participants. In classifying phages based on host bacteria, a decreased number of phages infecting mainly the Clostridia class was observed immediately after the onset of COVID-19 and recovered over time. After the onset of COVID-19, two distinct movement patterns of intestinal phages and their host bacteria were observed: phage- and bacteria-predominant. The abundance of obligate anaerobes, such as Clostridium_sense_strict_1, Fusicatenibacter, and Romboutsia, and the phages hosting these bacteria decreased immediately after the onset of COVID-19, and faster phage recovery was observed compared with bacterial recovery. In contrast, the genus Staphylococcus, a facultative anaerobic bacterium, increased immediately after the onset of COVID-19, whereas the phages infecting Staphylococcus decreased. Furthermore, immediately after the onset of COVID-19, the percentage of lytic phages increased, whereas that of temperate phages decreased. These observations suggest that the gut microbiota dysbiosis observed immediately after the onset of COVID-19 may be linked to phage dynamics that control gut microbiota and may also affect the recovery from dysbiosis.IMPORTANCEBacteriophages infect and replicate with bacteria and archaea and are closely associated with intestinal bacteria. The symbiotic relationship between gut microbiota and bacteriophages is of interest, but it is challenging to study their dynamics in the human body over time. SARS-CoV-2 infection has been reported to alter the gut microbiota, which is involved in gut immune regulation and pathophysiology, although changes in the intestinal phages of patients with SARS-CoV-2 and their dynamic relationship with the gut microbiota remain unclear. SARS-CoV-2 infection, which follows a transient pathological course from disease onset to cure, may provide a reliable model to investigate these interactions in the gut environment. Therefore, this study aimed to elucidate the correlation between gut microbiota and intestinal DNA virome dynamics in COVID-19 pathogenesis. This study found that the dysbiosis observed in SARS-CoV-2 infection involves a growth strategy that depends on the phage or bacterial dominance. |
| format | Article |
| id | doaj-art-4d7bcd8cb93146fdb0dd0d5bba7be096 |
| institution | Kabale University |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-4d7bcd8cb93146fdb0dd0d5bba7be0962025-01-07T14:05:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.00998-24Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infectionAya Ishizaka0Azumi Tamura1Michiko Koga2Taketoshi Mizutani3Seiya Yamayoshi4Kiyoko Iwatsuki-Horimoto5Atsuhiro Yasuhara6Shinya Yamamoto7Hiroyuki Nagai8Eisuke Adachi9Yutaka Suzuki10Yoshihiro Kawaoka11Hiroshi Yotsuyanagi12Division of Infectious Diseases, Advanced Clinical Research Center, the Institute of Medical Science, the University of Tokyo, Tokyo, JapanDivision of Infectious Diseases, Advanced Clinical Research Center, the Institute of Medical Science, the University of Tokyo, Tokyo, JapanDivision of Infectious Diseases, Advanced Clinical Research Center, the Institute of Medical Science, the University of Tokyo, Tokyo, JapanCenter for Emergency Preparedness and Response, National Institute of Infectious Diseases, Tokyo, JapanDivision of Virology, Department of Microbiology and Immunology, Institute of Medical Science, the University of Tokyo, Tokyo, JapanDivision of Virology, Department of Microbiology and Immunology, Institute of Medical Science, the University of Tokyo, Tokyo, JapanDivision of Virology, Department of Microbiology and Immunology, Institute of Medical Science, the University of Tokyo, Tokyo, JapanDepartment of Infectious Diseases and Applied Immunology, IMSUT Hospital of Institute of Medical Science, the University of Tokyo, Tokyo, JapanDepartment of Infectious Diseases and Applied Immunology, IMSUT Hospital of Institute of Medical Science, the University of Tokyo, Tokyo, JapanDepartment of Infectious Diseases and Applied Immunology, IMSUT Hospital of Institute of Medical Science, the University of Tokyo, Tokyo, JapanDepartment of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, the University of Tokyo, Chiba, JapanDivision of Virology, Department of Microbiology and Immunology, Institute of Medical Science, the University of Tokyo, Tokyo, JapanDivision of Infectious Diseases, Advanced Clinical Research Center, the Institute of Medical Science, the University of Tokyo, Tokyo, JapanABSTRACT This study compared intestinal DNA phage dynamics and gut microbiota changes observed at the onset of coronavirus disease 2019 (COVID-19). The study participants included 19 healthy individuals and 19 patients with severe acute respiratory syndrome coronavirus 2 infection. Significant differences were observed in the diversity of the intestinal DNA virome after the onset of COVID-19 compared with that in healthy individuals. Classification by their tail morphology resulted in the order Caudovirales, a double-stranded DNA phage, accounting for >95% of all participants. In classifying phages based on host bacteria, a decreased number of phages infecting mainly the Clostridia class was observed immediately after the onset of COVID-19 and recovered over time. After the onset of COVID-19, two distinct movement patterns of intestinal phages and their host bacteria were observed: phage- and bacteria-predominant. The abundance of obligate anaerobes, such as Clostridium_sense_strict_1, Fusicatenibacter, and Romboutsia, and the phages hosting these bacteria decreased immediately after the onset of COVID-19, and faster phage recovery was observed compared with bacterial recovery. In contrast, the genus Staphylococcus, a facultative anaerobic bacterium, increased immediately after the onset of COVID-19, whereas the phages infecting Staphylococcus decreased. Furthermore, immediately after the onset of COVID-19, the percentage of lytic phages increased, whereas that of temperate phages decreased. These observations suggest that the gut microbiota dysbiosis observed immediately after the onset of COVID-19 may be linked to phage dynamics that control gut microbiota and may also affect the recovery from dysbiosis.IMPORTANCEBacteriophages infect and replicate with bacteria and archaea and are closely associated with intestinal bacteria. The symbiotic relationship between gut microbiota and bacteriophages is of interest, but it is challenging to study their dynamics in the human body over time. SARS-CoV-2 infection has been reported to alter the gut microbiota, which is involved in gut immune regulation and pathophysiology, although changes in the intestinal phages of patients with SARS-CoV-2 and their dynamic relationship with the gut microbiota remain unclear. SARS-CoV-2 infection, which follows a transient pathological course from disease onset to cure, may provide a reliable model to investigate these interactions in the gut environment. Therefore, this study aimed to elucidate the correlation between gut microbiota and intestinal DNA virome dynamics in COVID-19 pathogenesis. This study found that the dysbiosis observed in SARS-CoV-2 infection involves a growth strategy that depends on the phage or bacterial dominance.https://journals.asm.org/doi/10.1128/spectrum.00998-24COVID-19SARS-CoV-2gut microbiomebacteriophages |
| spellingShingle | Aya Ishizaka Azumi Tamura Michiko Koga Taketoshi Mizutani Seiya Yamayoshi Kiyoko Iwatsuki-Horimoto Atsuhiro Yasuhara Shinya Yamamoto Hiroyuki Nagai Eisuke Adachi Yutaka Suzuki Yoshihiro Kawaoka Hiroshi Yotsuyanagi Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection Microbiology Spectrum COVID-19 SARS-CoV-2 gut microbiome bacteriophages |
| title | Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection |
| title_full | Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection |
| title_fullStr | Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection |
| title_full_unstemmed | Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection |
| title_short | Dysbiosis of gut microbiota in COVID-19 is associated with intestinal DNA phage dynamics of lysogenic and lytic infection |
| title_sort | dysbiosis of gut microbiota in covid 19 is associated with intestinal dna phage dynamics of lysogenic and lytic infection |
| topic | COVID-19 SARS-CoV-2 gut microbiome bacteriophages |
| url | https://journals.asm.org/doi/10.1128/spectrum.00998-24 |
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