Multi-kingdom microbiota analysis reveals bacteria-viral interplay in IBS with depression and anxiety.

Journal: NPJ biofilms and microbiomes
Published Date:

Abstract

Irritable Bowel Syndrome (IBS) is a common gastrointestinal disorder frequently accompanied by psychological symptoms. Bacterial microbiota plays a critical role in mediating local and systemic immunity, and alterations in these microbial communities have been linked to IBS. Emerging data indicate that other intestinal organisms, including bacteriophages, are closely interlinked with the bacterial microbiota and their host, yet their collective role remains to be elucidated. Here, we analyze the gut multi-kingdom microbiota of 360 IBS patients from a prospective cohort study in Hong Kong, with participants phenotyped through psychological assessment. Our findings reveal significantly lower intra-community correlations in IBS patients compared to healthy controls and highlight unique taxa patterns associated with IBS and mental disorders. Utilizing multi-omic data alongside machine learning techniques, we successfully predicted psychiatric comorbidities in IBS, achieving an average AUC of 0.78. Notably, gut viruses emerged as significant contributors to our predictive model, indicating a vital role for bacteriophages in the gut microbiome of IBS patients. We found that lysogenic phages in IBS displayed a broader host range, with Bilophia containing the most abundant prophages. Our analysis further indicates that IBS patients with depression exhibited a higher prevalence of viral-encoded auxiliary metabolic genes, specifically those involved in the sulfur metabolic pathway related to ubiquinone biosynthesis. The gut virome is increasingly reported to play an important role in the pathogenesis of many diseases. The study provides a systematic characterization of the drivers of the gut viral community and further expands our knowledge of the distinct interaction of gut viruses with their prokaryotic hosts, which is critical for understanding the viral-bacterial environment in IBS.

Authors

  • Qin Liu
    School of Public Health and Management, Research Center for Medicine and Social Development, Innovation Center for Social risk Governance in Health, Chongqing Medical University, Chongqing 400016, China.
  • Wenyu Fang
    Centre for Chinese Herbal Medicine Drug Development, Hong Kong Baptist University, Hong Kong SAR, China.
  • Ping Zheng
    Department of Key Laboratory, Shanghai Pudong New Area People's Hospital, Shanghai, China.
  • Shicai Xie
    Centre for Chinese Herbal Medicine Drug Development, Hong Kong Baptist University, Hong Kong SAR, China.
  • Xuanting Jiang
    Centre for Chinese Herbal Medicine Drug Development, Hong Kong Baptist University, Hong Kong SAR, China.
  • Wen Luo
    College of Mathematics and Systems Science, Guangdong Polytechnic Normal University, Guangzhou, Guangdong 510665, China.
  • Lijuan Han
    Department of Scientific Research, Kangmeihuada GeneTech Co. Ltd. (KMHD), Shenzhen, China.
  • Ling Zhao
    School of Acu-Mox and Tuina, Chengdu University of Traditional Chinese Medicine, Chengdu, China.
  • Lin Lu
    School of Economics and Management, Guangxi Normal University, Guilin, China.
  • Lixiang Zhai
    Centre for Chinese Herbal Medicine Drug Development, Hong Kong Baptist University, Hong Kong SAR, China.
  • Danny J Yu
    Vincent V.C. Woo Chinese Medicine Clinical Research Institute, School of Chinese Medicine, Hong Kong Baptist University, Hong Kong SAR, China.
  • Wei Yang
    Key Laboratory of Structure-Based Drug Design and Discovery (Shenyang Pharmaceutical University), Ministry of Education, School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Wenhua Road 103, Shenyang 110016, PR China. Electronic address: 421063202@qq.com.
  • Chengyuan Lin
    Centre for Chinese Herbal Medicine Drug Development, Hong Kong Baptist University, Hong Kong SAR, China.
  • Xiaodong Fang
    BGI Research, Sanya, China.
  • Zhaoxiang Bian
    School of Chinese Medicine, Vincent V.C. Woo Chinese Medicine Clinical Research Institute, Hong Kong Baptist University, Hong Kong, China.