Dataset Information

Colonization with two different Blastocystis subtypes in DSS-induced colitis mice is associated with strikingly different microbiome and pathological features.

ABSTRACT: Rationale: The gut microbiota plays a significant role in the pathogenesis of inflammatory bowel disease (IBD). However, the role of Blastocystis infection and Blastocystis-altered gut microbiota in the development of inflammatory diseases and their underlying mechanisms are not well understood. Methods: We investigated the effect of Blastocystis ST4 and ST7 infection on the intestinal microbiota, metabolism, and host immune responses, and then explored the role of Blastocystis-altered gut microbiome in the development of dextran sulfate sodium (DSS)-induced colitis in mice. Results: This study showed that prior colonization with ST4 conferred protection from DSS-induced colitis through elevating the abundance of beneficial bacteria, short-chain fatty acid (SCFA) production and the proportion of Foxp3⁺ and IL-10-producing CD4⁺ T cells. Conversely, prior ST7 infection exacerbated the severity of colitis by increasing the proportion of pathogenic bacteria and inducing pro-inflammatory IL-17A and TNF-α-producing CD4⁺ T cells. Furthermore, transplantation of ST4- and ST7-altered microbiota resulted in similar phenotypes. Conclusions: Our data showed that ST4 and ST7 infection exert strikingly differential effects on the gut microbiota, and these could influence the susceptibility to colitis. ST4 colonization prevented DSS-induced colitis in mice and may be considered as a novel therapeutic strategy against immunological diseases in the future, while ST7 infection is a potential risk factor for the development of experimentally induced colitis that warrants attention.

SUBMITTER: Deng L

PROVIDER: S-EPMC9925320 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Colonization with two different Blastocystis subtypes in DSS-induced colitis mice is associated with strikingly different microbiome and pathological features.

Deng Lei L Wojciech Lukasz L Png Chin Wen CW Kioh Dorinda Yan Qin DYQ Gu Yuxiang Y Aung Thet Tun TT Malleret Benoit B Chan Eric Chun Yong ECY Peng Guangneng G Zhang Yongliang Y Gascoigne Nicholas Robert John NRJ Tan Kevin Shyong Wei KSW

Theranostics 20230205 3

Rationale: The gut microbiota plays a significant role in the pathogenesis of inflammatory bowel disease (IBD). However, the role of Blastocystis infection and Blastocystis-altered gut microbiota in the development of inflammatory diseases and their underlying mechanisms are not well understood. Methods: We investigated the effect of Blastocystis ST4 and ST7 infection on the intestinal microbiota, metabolism, and host immune responses, and then explored the rol ...[more]

PMID: 36793854

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Project description:Protists are a normal component of mammalian intestinal ecosystems that live alongside, and interact with, bacterial microbiota. Blastocystis, one of the most common intestinal eukaryotes, is reported as a pathogen that causes inflammation and disease, though health consequences likely vary depending on host health, the gut ecosystem, and genetic diversity. Accumulating evidence suggests that Blastocystis is by and large commensal. Blastocystis is more common in healthy individuals than those with immune mediated diseases such as Inflammatory Bowel Diseases (IBD). Blastocystis presence is also associated with altered composition and higher richness of the bacterial gut microbiota. It is not clear whether Blastocystis directly promotes a healthy gut and microbiome or is more likely to colonize and persist in a healthy gut environment. We test this hypothesis by measuring the effect of Blastocystis ST3 colonization on the health and microbiota in a rat experimental model of intestinal inflammation using the haptenizing agent dinitrobenzene sulfonic acid (DNBS). We experimentally colonized rats with Blastocystis ST3 obtained from a healthy, asymptomatic human donor and then induced colitis after 3 weeks (short term exposure experiment) or after 13 weeks (long term exposure experiment) and compared these colonized rats to a colitis-only control group. Across experiments Blastocystis ST3 colonization alters microbiome composition, but not richness, and induces only mild gut inflammation but no clinical symptoms. Our results showed no effect of short-term exposure to Blastocystis ST3 on gut inflammation following colitis induction. In contrast, long-term Blastocystis exposure appears to promote a faster recovery from colitis. There was a significant reduction in inflammatory markers, pathology 2 days after colitis induction in the colonized group, and clinical scores also improved in this group. Blastocystis colonization resulted in a significant reduction in tumor necrosis factor alpha (TNFα) and IL-1β relative gene expression, while expression of IFNγ and IL17re/17C were elevated. We obtained similar results in a previous pilot study. We further found that bacterial richness rebounded in rats colonized by Blastocystis ST3. These results suggest that Blastocystis sp. may alter the gut ecosystem in a protective manner and promote faster recovery from disturbance.

Project description:Blastocystis is the most prevalent protist of the human intestine, colonizing approximately 20% of the North American population and up to 100% in some nonindustrialized settings. Blastocystis is associated with gastrointestinal and systemic disease but can also be an asymptomatic colonizer in large populations. While recent findings in humans have shown bacterial microbiota changes associated with this protist, it is unknown whether these occur due to the presence of Blastocystis or as a result of inflammation. To explore this, we evaluated the fecal bacterial and eukaryotic microbiota in 156 asymptomatic adult subjects from a rural population in Xoxocotla, Mexico. Colonization with Blastocystis was strongly associated with an increase in bacterial alpha diversity and broad changes in beta diversity and with more discrete changes to the microbial eukaryome. More than 230 operational taxonomic units (OTUs), including those of dominant species Prevotella copri and Ruminococcus bromii, were differentially abundant in Blastocystis-colonized individuals. Large functional changes accompanied these observations, with differential abundances of 202 (out of 266) predicted metabolic pathways (PICRUSt), as well as lower fecal concentrations of acetate, butyrate, and propionate in colonized individuals. Fecal calprotectin was markedly decreased in association with Blastocystis colonization, suggesting that this ecological shift induces subclinical immune consequences to the asymptomatic host. This work is the first to show a direct association between the presence of Blastocystis and shifts in the gut bacterial and eukaryotic microbiome in the absence of gastrointestinal disease or inflammation. These results prompt further investigation of the role Blastocystis and other eukaryotes play within the human microbiome. IMPORTANCE Given the results of our study and other reports of the effects of the most common human gut protist on the diversity and composition of the bacterial microbiome, Blastocystis and, possibly, other gut protists should be studied as ecosystem engineers that drive community diversity and composition.

Dataset Information

Colonization with two different Blastocystis subtypes in DSS-induced colitis mice is associated with strikingly different microbiome and pathological features.

Publications

Colonization with two different <i>Blastocystis</i> subtypes in DSS-induced colitis mice is associated with strikingly different microbiome and pathological features.

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