Steamed broccoli sprouts alleviate DSS-induced inflammation and retain gut microbial biogeography in mice

Author:

Holman Johanna M.1,Colucci Louisa2,Baudewyns Dorien3,Balkan Joe4,Hunt Timothy5,Hunt Benjamin5,Kinney Marissa1,Holcomb Lola6,Stratigakis Allesandra7,Chen Grace8,Moses Peter L.910,Mawe Gary M.9,Zhang Tao7,Li Yanyan1ORCID,Ishaq Suzanne L.1ORCID

Affiliation:

1. School of Food and Agriculture, University of Maine , Orono, Maine, USA

2. Department of Biology, Husson University , Bangor, Maine, USA

3. Department of Psychology, University of Maine , Orono, Maine, USA

4. Department of Chemical and Biological Engineering, Tufts University , Medford, Massachusetts, USA

5. Department of Biology, University of Maine , Orono, Maine, USA

6. Graduate School of Biomedical Sciences and Engineering, University of Maine , Orono, Maine, USA

7. School of Pharmacy and Pharmaceutical Sciences, SUNY Binghamton University , Johnson City, New York, USA

8. Department of Internal Medicine, University of Michigan Medical School , Ann Arbor, Michigan, USA

9. Departments of Neurological Sciences and of Medicine, Larner College of Medicine, University of Vermont , Burlington, Vermont, USA

10. Finch Therapeutics , Somerville, Massachusetts, USA

Abstract

ABSTRACT Inflammatory bowel diseases (IBDs) are devastating conditions of the gastrointestinal tract with limited treatments, and dietary intervention may be effective and affordable for managing symptoms. Glucosinolate compounds are highly concentrated in broccoli sprouts, especially glucoraphanin (GLR), and can be metabolized by certain mammalian gut bacteria into anti-inflammatory isothiocyanates, such as sulforaphane. Gut microbiota exhibit biogeographic patterns, but it is unknown if colitis alters these or whether the location of glucoraphanin-metabolizing bacteria affects anti-inflammatory benefits. We fed specific pathogen-free C57BL/6 mice either a control diet or a 10% steamed broccoli sprout diet and gave a three-cycle regimen of 2.5% dextran sodium sulfate (DSS) in drinking water over a 34-day experiment to simulate chronic, relapsing ulcerative colitis (UC). We monitored body weight, fecal characteristics, lipocalin, serum cytokines, and bacterial communities from the luminal- and mucosal-associated populations in the jejunum, cecum, and colon. Mice fed the broccoli sprout diet with DSS treatment performed better than mice fed the control diet with DSS, and had significantly more weight gain, lower Disease Activity Index scores, lower plasma lipocalin and proinflammatory cytokines, and higher bacterial richness in all gut locations. Bacterial communities were assorted by gut location but were more homogenous across locations in the control diet + DSS mice. Importantly, our results showed that broccoli sprout feeding abrogated the effects of DSS on gut microbiota, as bacterial richness and biogeography were similar between mice receiving broccoli sprouts with and without DSS. Collectively, these results support the protective effect of steamed broccoli sprouts against dysbiosis and colitis induced by DSS. IMPORTANCE Evaluating bacterial communities across different locations in the gut provides a greater insight than fecal samples alone and provides an additional metric by which to evaluate beneficial host-microbe interactions. Here, we show that 10% steamed broccoli sprouts in the diet protects mice from the negative effects of dextran sodium sulfate-induced colitis, that colitis erases biogeographic patterns of bacterial communities in the gut, and that the cecum is not likely to be a significant contributor to colonic bacteria of interest in the DSS mouse model of ulcerative colitis. Mice fed the broccoli sprout diet during colitis performed better than mice fed the control diet while receiving DSS. The identification of accessible dietary components and concentrations that help maintain and correct the gut microbiome may provide universal and equitable approaches to IBD prevention and recovery, and broccoli sprouts represent a promising strategy.

Funder

USDA | National Institute of Food and Agriculture

HHS | NIH | National Institute of Diabetes and Digestive and Kidney Diseases

Publisher

American Society for Microbiology

Subject

Computer Science Applications,Genetics,Molecular Biology,Modeling and Simulation,Ecology, Evolution, Behavior and Systematics,Biochemistry,Physiology,Microbiology

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