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The phageome of patients with ulcerative colitis treated with donor fecal microbiota reveals markers associated with disease remission

Author

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  • Marwan E. Majzoub

    (UNSW)

  • Sudarshan Paramsothy

    (University of Sydney
    Concord Repatriation General Hospital)

  • Craig Haifer

    (UNSW
    St Vincent’s Hospital)

  • Rohit Parthasarathy

    (UNSW)

  • Thomas J. Borody

    (Centre for Digestive Diseases)

  • Rupert W. Leong

    (University of Sydney
    Concord Repatriation General Hospital)

  • Michael A. Kamm

    (St Vincent’s Hospital
    University of Melbourne)

  • Nadeem O. Kaakoush

    (UNSW)

Abstract

Bacteriophages are influential within the human gut microbiota, yet they remain understudied relative to bacteria. This is a limitation of studies on fecal microbiota transplantation (FMT) where bacteriophages likely influence outcome. Here, using metagenomics, we profile phage populations - the phageome - in individuals recruited into two double-blind randomized trials of FMT in ulcerative colitis. We leverage the trial designs to observe that phage populations behave similarly to bacterial populations, showing temporal stability in health, dysbiosis in active disease, modulation by antibiotic treatment and by FMT. We identify a donor bacteriophage putatively associated with disease remission, which on genomic analysis was found integrated in a bacterium classified to Oscillospiraceae, previously isolated from a centenarian and predicted to produce vitamin B complex except B12. Our study provides an in-depth assessment of phage populations during different states and suggests that bacteriophage tracking has utility in identifying determinants of disease activity and resolution.

Suggested Citation

  • Marwan E. Majzoub & Sudarshan Paramsothy & Craig Haifer & Rohit Parthasarathy & Thomas J. Borody & Rupert W. Leong & Michael A. Kamm & Nadeem O. Kaakoush, 2024. "The phageome of patients with ulcerative colitis treated with donor fecal microbiota reveals markers associated with disease remission," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53454-4
    DOI: 10.1038/s41467-024-53454-4
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    References listed on IDEAS

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    1. Lingling Wang & Haobin Yao & Daniel C. Morgan & Kam Shing Lau & Suet Yi Leung & Joshua W. K. Ho & Wai K. Leung, 2023. "Altered human gut virome in patients undergoing antibiotics therapy for Helicobacter pylori," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Yuko Sato & Koji Atarashi & Damian R. Plichta & Yasumichi Arai & Satoshi Sasajima & Sean M. Kearney & Wataru Suda & Kozue Takeshita & Takahiro Sasaki & Shoki Okamoto & Ashwin N. Skelly & Yuki Okamura , 2021. "Novel bile acid biosynthetic pathways are enriched in the microbiome of centenarians," Nature, Nature, vol. 599(7885), pages 458-464, November.
    3. Alejandro Reyes & Matthew Haynes & Nicole Hanson & Florent E. Angly & Andrew C. Heath & Forest Rohwer & Jeffrey I. Gordon, 2010. "Viruses in the faecal microbiota of monozygotic twins and their mothers," Nature, Nature, vol. 466(7304), pages 334-338, July.
    4. Koen Wortelboer & Patrick A. Jonge & Torsten P. M. Scheithauer & Ilias Attaye & E. Marleen Kemper & Max Nieuwdorp & Hilde Herrema, 2023. "Phage-microbe dynamics after sterile faecal filtrate transplantation in individuals with metabolic syndrome: a double-blind, randomised, placebo-controlled clinical trial assessing efficacy and safety," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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