Gut microbial β-glucuronidases regulate host luminal proteases and are depleted in irritable bowel syndrome
Open accessAbstract
Intestinal proteases mediate digestion and immune signalling, while increased gut proteolytic activity disrupts the intestinal barrier and generates visceral hypersensitivity, which is common in irritable bowel syndrome (IBS). However, the mechanisms controlling protease function are unclear. Here we show that members of the gut microbiota suppress intestinal proteolytic activity through production of unconjugated bilirubin. This occurs via microbial β-glucuronidase-mediated conversion of bilirubin conjugates. Metagenomic analysis of faecal samples from patients with post-infection IBS (n = 52) revealed an altered gut microbiota composition, in particular a reduction in Alistipes taxa, and high gut proteolytic activity driven by specific host serine proteases compared with controls. Germ-free mice showed 10-fold higher proteolytic activity compared with conventional mice. Colonization with microbiota samples from high proteolytic activity IBS patients failed to suppress proteolytic activity in germ-free mice, but suppression of proteolytic activity was achieved with colonization using microbiota from healthy donors. High proteolytic activity mice had higher intestinal permeability, a higher relative abundance of Bacteroides and a reduction in Alistipes taxa compared with low proteolytic activity mice. High proteolytic activity IBS patients had lower fecal β-glucuronidase activity and end-products of bilirubin deconjugation. Mice treated with unconjugated bilirubin and β-glucuronidase-overexpressing E. coli significantly reduced proteolytic activity, while inhibitors of microbial β-glucuronidases increased proteolytic activity. Together, these data define a disease-relevant mechanism of host-microbial interaction that maintains protease homoeostasis in the gut.
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β-glucuronidases released by commensal microbes suppressed host proteolytic activity, thereby protecting the intestinal epithelium.
“The authors also showed that β-glucuronidases released by commensal microbes suppressed host PA, thereby protecting the intestinal epithelium and suggest that a decrease in microbial β-glucuronidase activity may contribute to IBS pathogenesis.57”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [57]
Metagenomic analysis of faecal samples from patients with post-infectious irritable bowel syndrome revealed an altered gut microbiota composition and high gut proteolytic activity driven by specific host serine proteases compared with controls.
“In a recent study, metagenomic analysis of faecal samples from patients with post-infectious IBS revealed an altered gut microbiota composition and high gut proteolytic activity driven by specific host serine proteases compared with controls.”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [57]
A decrease in microbial β-glucuronidase activity may contribute to irritable bowel syndrome pathogenesis.
“suggest that a decrease in microbial β-glucuronidase activity may contribute to IBS pathogenesis.57”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [57]
Studies in mice and humans have provided evidence that host- and bacterial-derived proteases may contribute to irritable bowel syndrome pathogenesis and symptom generation.
“Similar to IBD, studies in mice and humans have provided evidence that host- and bacterial-derived proteases may contribute to pathogenesis and symptom generation.7,13,57,58”
From The emerging roles of bacterial proteases in intestinal diseases (2023) · cites this paper as [57]
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Paracellular permeability and tight junction regulation in gut health and disease
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A gut microbiota-bile acid axis promotes intestinal homeostasis upon aspirin-mediated damage
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Vanuytsel, T., Berčík, P., & Boeckxstaens, G. E. (2023) · Gut · doi:10.1136/gutjnl-2020-320633 · Cited by 157 · see citing works
The emerging roles of bacterial proteases in intestinal diseases
Caminero, A., Guzman, M., Libertucci, J., & Lomax, A. E. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2181922 · Cited by 92 · see citing works
Chronic Visceral Pain: New Peripheral Mechanistic Insights and Resulting Treatments
Ford, A. C., Vanner, S. J., Kashyap, P., & Nasser, Y. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.01.045 · Cited by 79 · see citing works
Self-citationThe gut microbiome in disorders of gut–brain interaction
Kraïmi, N., Ross, T., Pujo, J., & Palma, G. D. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2360233 · Cited by 86 · see citing works
Simpson, J. B., Walker, M. E., Sekela, J. J., Ivey, S. M., Jariwala, P. B., Storch, C. M., Kowalewski, M. E., Graboski, A. L., Lietzan, A. D., Walton, W. G., et al. (2024) · Cell Host & Microbe · doi:10.1016/j.chom.2024.04.018 · Cited by 70 · see citing works
Self-citationZheng, C., Zhong, Y., Zhang, W., Wang, Z., Xiao, H., Zhang, W., Xie, J., Peng, X., Luo, J. F., & Xu, W. (2023) · Advanced Science · doi:10.1002/advs.202302798 · Cited by 67 · see citing works
Ameliorative effect of buckwheat polysaccharides on colitis via regulation of the gut microbiota
Yang, J.-Y., Chen, S.-Y., Wu, Y., Liao, Y.-L., & Yen, G. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.12.155 · Cited by 51 · see citing works
Feng, Y., Chen, S., Song, Y., Liu, S., Duan, Y., Cai, M., Kong, T., & Zhang, H. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.127835 · Cited by 46 · see citing works
Metagenome-guided culturomics for the targeted enrichment of gut microbes
Armetta, J., Li, S. S., Vaaben, T. H., Vazquez-Uribe, R., & Sommer, M. O. A. (2025) · Nature Communications · doi:10.1038/s41467-024-55668-y · Cited by 49 · see citing works
Gastrointestinal Biofilms: Endoscopic Detection, Disease Relevance, and Therapeutic Strategies
Jandl, B., Dighe, S. N., Baumgartner, M., Makristathis, A., Gasché, C., & Muttenthaler, M. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.04.032 · Cited by 46 · see citing works
Targeting the human gut microbiome with small-molecule inhibitors
Woo, A. Y. M., Aguilar Ramos, M. A., Narayan, R., Richards-Corke, K. C., Wang, M. L., Sandoval-Espinola, W. J., & Balskus, E. P. (2023) · Nature Reviews Chemistry · doi:10.1038/s41570-023-00471-4 · Cited by 42 · see citing works
Intestinal Permeability in Disorders of Gut–Brain Interaction: From Bench to Bedside
Grover, M., Vanuytsel, T., & Chang, L. (2024) · Gastroenterology · doi:10.1053/j.gastro.2024.08.033 · Cited by 43 · see citing works
Self-citationBenchmarking differential abundance analysis methods for correlated microbiome sequencing data
Yang, L., & Chen, J. (2022) · Briefings in Bioinformatics · doi:10.1093/bib/bbac607 · Cited by 39 · see citing works
Self-citationGut microbiota-mediated modulation of host amino acid availability and metabolism
Han, Z., Zhao, L., Hu, Q., Hung, I., Liu, C., Liu, S., Mei, X., Zeng, X., Bin, P., & Wang, J. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2552345 · Cited by 42 · see citing works
Shin, A., & Kashyap, P. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2195792 · Cited by 34 · see citing works
Self-citationChanges in signalling from faecal neuroactive metabolites following dietary modulation of IBS pain
Tuck, C. J., Omar, A. A., Palma, G. D., Osman, S., Jiménez-Vargas, N. N., Yu, Y., Bennet, S., López-López, C., Jaramillo-Polanco, J., Baker, C. C., et al. (2022) · Gut · doi:10.1136/gutjnl-2022-327260 · Cited by 31 · see citing works
Santiago, A., Hann, A., Constante, M., Rahmani, S., Libertucci, J., Jackson, K. J., Rueda, G. H., Rossi, L., Ramachandran, R., Ruf, W., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2205425 · Cited by 30 · see citing works
Gut microbiota interact with breast cancer therapeutics to modulate efficacy
Arnone, A. A., Ansley, K. C., Heeke, A. L., Howard-McNatt, M. M., & Cook, K. L. (2025) · EMBO Molecular Medicine · doi:10.1038/s44321-024-00185-0 · Cited by 36 · see citing works
A Galaxy of informatics resources for MS-based proteomics
Mehta, S., Bernt, M., Chambers, M., Fahrner, M., Föll, M. C., Gruening, B., Horro, C., Johnson, J. E., Loux, V., Rajczewski, A. T., et al. (2023) · Expert Review of Proteomics · doi:10.1080/14789450.2023.2265062 · Cited by 26 · see citing works
Self-citationThe Role of Gut Microbiome in Irritable Bowel Syndrome: Implications for Clinical Therapeutics
Zhao, Y., Zhu, S., Dong, Y., Xie, T., Chai, Z., Gao, X., Dai, Y., & Wang, X. (2024) · Biomolecules · doi:10.3390/biom14121643 · Cited by 30 · see citing works
Jadhav, A., Bajaj, A., Yang, X. J., Markandey, M., Ahuja, V., & Kashyap, P. (2023) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-061121-094908 · Cited by 27 · see citing works
Self-citationRecent advances in clinical practice: mastering the challenge—managing IBS symptoms in IBD
Wellens, J., Sabino, J., Vanuytsel, T., Tack, J. F., & Vermeire, S. (2024) · Gut · doi:10.1136/gutjnl-2024-333565 · Cited by 29 · see citing works
Microbial β-glucuronidases drive human periodontal disease etiology
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Self-citationMa, Y., Wei, X., Peng, J., Wei, F., Wen, Y., Liu, M., Song, B., Wang, Y., Zhang, Y., & Peng, T. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1414675 · Cited by 22 · see citing works
The role of the gut microbiome in disorders of gut–brain interaction
Gawey, B. J., Mars, R. A. T., & Kashyap, P. (2024) · FEBS Journal · doi:10.1111/febs.17200 · Cited by 28 · see citing works
Self-citationImpact of microbiota on breast cancer hormone therapy
Terrisse, S. A., Zitvogel, L., & Kroemer, G. (2023) · Cell Stress · doi:10.15698/cst2023.03.277 · Cited by 21 · see citing works
The proteolytic activity in inflammatory bowel disease: insight from gut microbiota
Hou, J., Ding, L., Yang, T., Yang, Y.-F., Jin, Y., Zhang, X., Ma, A.-H., & Qin, Y. (2024) · Microbial Pathogenesis · doi:10.1016/j.micpath.2024.106560 · Cited by 20 · see citing works
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Self-citationQuan, R., Decraecker, L., Appeltans, I., Cuende‐Estévez, M., Remoortel, S. V., Aguilera‐Lizarraga, J., Wang, Z., Hicks, G. A., Wykosky, J., McLean, P. G., et al. (2024) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000003042 · Cited by 16 · see citing works
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A New Fluorescent Probe Tool: ERNathG
Yu, Z., Zhang, J., Chen, J., Zhao, L., Yu, D., Liu, L., & Dong, S. (2023) · Analytical Chemistry · doi:10.1021/acs.analchem.3c00075 · Cited by 15 · see citing works
Self-citationFood supply toxicants and additives alter the gut microbiota and risk of metabolic disease
Barra, N. G., Fang, H., Bhatwa, A., Schmidt, A., Syed, S. A., Steinberg, G. R., Morrison, K. M., Surette, M. G., Wade, M. G., Holloway, A. C., et al. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00364.2024 · Cited by 13 · see citing works
Interaction between the breast tumor microenvironment and gut microbiome
Tang, G., Millar, E. K. A., Graham, P., & Beretov, J. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2514136 · Cited by 13 · see citing works
Gut microbial β-Glucuronidase: A key regulator of endobiotic homeostasis
Ning, L., & Hong, J. (2024) · Cell Host & Microbe · doi:10.1016/j.chom.2024.05.007 · Cited by 12 · see citing works
Nervous system in colorectal cancer
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Effects of gut microbiota in breast cancer
Kang, L., Chen, H., He, C., & Li, J. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1617410 · Cited by 11 · see citing works
Biodiversity Analysis of Metaproteomics Samples with Unipept: A Comprehensive Tutorial
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Rao, S. E., & Grover, M. (2023) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000972 · Cited by 10 · see citing works
Self-citationMaternal Diet Determines Milk Microbiome Composition and Offspring Gut Colonization in Wistar Rats
Martínez-Oca, P., Alba, C., Sánchez-Roncero, A., Fernández‐Marcelo, T., Martín, M. Á., Escrivá, F., Rodríguez, J. M., Álvarez, C., & Fernández‐Millán, E. (2023) · Nutrients · doi:10.3390/nu15204322 · Cited by 10 · see citing works
Dang, T., Fermin, A. S. R., & Machizawa, M. G. (2023) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2023.1266713 · Cited by 9 · see citing works
Yang, H. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1434582 · Cited by 8 · see citing works
Proteases in intestinal health and disease
Deraison, C., & Vergnolle, N. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01129-w · Cited by 9 · see citing works
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Diet, the Gut Microbiome, and Estrogen Physiology: A Review in Menopausal Health and Interventions
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Li, Y., Cheng, Y., Liu, W. J., Li, J., Li, S., Suriguga, Ma, T., Kwok, L., Cai, Z., & Sun, Z. (2026) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1722632 · Cited by 6 · see citing works
Serological and faecal markers of irritable bowel syndrome: a systematic review and meta-analysis
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Role of microbiota in pain: From bench to bedside
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The Intestinal Microenvironment and Disorders of Gut–Brain Interaction
Grover, M., Barbara, G., Chey, W. D., Chumpitazi, B. P., Feinle‐Bisset, C., Schellekens, H., & Quigley, E. M. M. (2026) · Gastroenterology · doi:10.1053/j.gastro.2026.02.015 · Cited by 10 · see citing works
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Pathophysiology of irritable bowel syndrome
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Insights on Wet and Dry Workflows for Human Gut Metaproteomics
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Microbial proteases as emerging anti-inflammatory therapeutics: a comprehensive review
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The role of the Alistipes genus in intestinal inflammation, cancer, and aging: a narrative review
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Editorial: Faecal microbiota transplantation in IBS —Moving closer or away from success?
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Self-citationRegulating protease homeostasis in irritable bowel syndrome
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Mammalian colonic contribution of amino acids to whole-body homeostasis
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Discovering microbiota functions via chemical probe incorporation for targeted sequencing
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Exploring a microbiota-targeted dietary strategy for irritable bowel syndrome
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mPower: a real data-based power analysis tool for microbiome study design
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Self-citationBarrier restoration as a therapeutic strategy for disorders of gut–brain interaction
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Self-citationFaecal proteases and immune signatures drive subtype-specific enteric neuronal activation in IBS
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Changes in the Gut Microbiota of Neonates with Hyperbilirubinemia Reaching Phototherapy Thresholds
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Di, J., & Zhang, X. (2025) · Advanced Chinese Medicine · doi:10.1002/acm4.70001
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Cheng, T., Wen, P., Yu, R., Zhang, F., Li, H., Xu, X., Zhao, D., Liu, F., Su, W., Zheng, Z., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26945604
- Authors
- Edwinson, A. L., Yang, L., Peters, S., Hanning, N., Jeraldo, P., Jagtap, P., Simpson, J. B., Yang, T.-Y., Kumar, P., Mehta, S., Nair, A., Breen-Lyles, M., Chikkamenahalli, L., Graham, R. P., De Winter, B., Patel, R., Dasari, S., Kashyap, P., Griffin, T., Chen, J., Farrugia, G., Redinbo, M. R., & Grover, M.
- Affiliations
- Mayo Clinic (US)
- University of Minnesota (US)
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Grover, Madhusudan
- ORCID
- Edwinson, Adam L.
- Yang, Lu
- Peters, Stephanie
- Hanning, Nikita
- Jeraldo, Patricio
- Jagtap, Pratik
- Simpson, Joshua B.
- Yang, Tzu-Yi
- Kumar, Praveen
- Mehta, Subina
- Graham, Rondell P.
- De Winter, Benedicte
- Patel, Robin
- Dasari, Surendra
- Kashyap, Purna
- Griffin, Timothy
- Chen, Jun
- Farrugia, Gianrico
- Redinbo, Matthew R.
- Grover, Madhusudan
- Venue
- Nature Microbiology
- Published
- 2022-04-28
- Volume
- 7
- Issue
- 5
- Pages
- 680-694
- ISSN
- 2058-5276 (ISSN-L)
- PMC
- PMC9081267
- OpenAlex
- W4225117821
- Cited by
- 105
- References
- 80
- Citations by year
- 2026: 30 · 2025: 25 · 2024: 28 · 2023: 18 · 2022: 4
- FWCI
- 7.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Microbiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Diabetes and Digestive and Kidney Diseases (DK127998, DK120745, DK103911)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Keywords
- irritable bowel syndrome, gut microbiota, beta-glucuronidase, intestinal proteases, serine protease, unconjugated bilirubin, Alistipes, Bacteroides, intestinal permeability, host-microbe interactions, post-infectious IBS, germ-free mice, microbial colonization, intestinal barrier
- MeSH terms
- Gastrointestinal Microbiome, Animals, Bilirubin, Escherichia coli, Glucuronidase, Humans, Endopeptidases, Irritable Bowel Syndrome, Mice, Serine Proteases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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