Gluten-free diet affects fecal small non-coding RNA profiles and microbiome composition in celiac disease supporting a host-gut microbiota crosstalk

Francavilla, A.; Ferrero, Giulio; Pardini, Barbara; Tarallo, Sonia; Zanatto, Laura; Caviglia, Gian Paolo; Sieri, Sabina; Grioni, Sara; Francescato, Giulia; Stalla, Francesco; Guiotto, Cristina; Crocella, Lucia; Astegiano, Marco; Bruno, Mauro; Calvo, Pier Luigi; Víneis, Paolo; Ribaldone, Davide Giuseppe; Naccarati, Alessio

doi:10.1080/19490976.2023.2172955

Cited by 18 publications

(12 citation statements)

References 61 publications

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“…Multiple of the observed differences in bacterial abundance and/or prevalence between tCeD and controls (Table 2 and Table 3) are in accordance with earlier reports, such as the enrichment of H. parainfluenzae (28) , R. inulinivorans (28), E. coli (18,47), and Bacteroides species (18,27,28), as well as the decreased prevalence of R. bicirculans , C. eutactus (27), C. fastidiosus (28,48), Roseburia sp. CAG:309 (28), and several Bifidobacterium species (18,28,47). In addition, however, several novel species were identified in our analysis, including an increase in Clostridium sp.…”

Section: Resultssupporting

confidence: 91%

“…We aimed to compare taxonomic profiles at the species level with those of previous CeD microbiome studies. In summary, our data (Table 2 and Table 3) confirms previous findings in (treated) CeD patients, demonstrating an increase in several Bacteroides species, H. parainfluenzae, R. inulinivorans , and E. coli , along with a decrease of various bifidobacteria, R. bicirculans , C. eutactus, and C. fastidiosus (18,27,28,47). Despite a lower prevalence of the major butyrigenic bacterium Butyrivibrio crossotus (62) (Table 3), we observed novel associations with increased abundances of other butyrate-producing bacteria including Clostridium sp.…”

Section: Discussionsupporting

confidence: 90%

“…Moreover, given that the majority of the 13 tested species exhibit a positive correlation, these findings imply that GFD indeed plays a role in several species-level associations observed in this study. Notably, we were unable to replicate the adverse impact of the GFD on the abundance of H. parainfluenzae as seen in other research (28,57).…”

Section: Resultscontrasting

confidence: 77%

“…Furthermore, most studies do not provide informaXon on the funcXonality of the gut microbiota. Our results, in addiXon to confirming previous studies (27,28), revealed novel associaXons between tCeD and the microbiome, explored the contribuXon of a GFD to gut microbiome composiXon and reported a less uniform microbiome composiXon, as well as increased strainto-strain variaXon in paXents with tCeD. Upon taxonomic analyses, we found both tCeD and self-reported IBD to present a unique microbiome signature, with limited overlap among changes in microbial abundance.…”

Section: Introduc4onsupporting

confidence: 89%

“…Alpha diversity is decreased in self-reported IBS and IBD subjects, but not in CeD pa9ents on GFD Although contradicXng data can be found in literature, most ooen it is described that withinsample microbiome diversity (alpha diversity) in untreated CeD is higher than that in controls (27,42) and that adherence to a GFD restores alpha diversity to normal levels (27,28). Indeed, using the Shannon index for evenness of the microbiome, we did not observe a significant difference in alpha diversity on either genus or species level, when comparing tCeD (adhering to a GFD) paXents and matched controls (Table 2).…”

Section: Resultsmentioning

confidence: 98%

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High-resolution analysis of the treated coeliac disease microbiome reveals increased inter-individual variability

Slager,

Simpson,

Gacesa

et al. 2024

Preprint

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Background: Coeliac disease (CeD) is a prevalent immune-mediated disorder primarily affecting the small intestine, characterised by a breakdown of tolerance to dietary gluten. Its onset results from the multifaceted interplay of genetic and environmental factors. Recent data show that alterations in gut microbiome composition could play an important role in CeD. However, many current studies have been constrained by small sample sizes and limited resolution.Methods: To address these limitations, faecal gut microbiota from two Dutch patient cohorts, CeDNN (129 treated CeD patients; tCeD and 106 non-CeD controls) and the Lifelines Dutch Microbiome Project (24 self-reported treated CeD and 659 non-CeD controls), was analyzed using shotgun metagenomic sequencing. Controls were matched by age, sex, and sequencing depth. Self-reported IBS and IBD were used as comparative conditions of the gastrointestinal tract. Inter-individual variation among cases and controls was calculated for the whole microbiome and on the strain-level. Finally, species-specific gene repertoires were analysed in tCeD patients and controls.Results: Alpha diversity was decreased in patients with self-reported IBS and IBD, but not in tCeD. Each condition displayed a unique microbial pattern, with minimal overlap in differentially abundant species. In addition to confirming existing studies, we identified an increase in the abundance of previously unreported species, includingClostridium sp. CAG:253,Roseburia hominis, andClostridium lavalense. We demonstrate that changes in tCeD gut microbiome can be, at least partly, explained by adherence to a GFD and report an increased inter-individual variation in gut microbiome composition among tCeD patients. More detailed analyses revealed that a higher bacterial mutation frequency in CeD also leads to a higher inter-individual variation on the strain-level. In line with this, we found that the immotile European subspecies ofEubacterium rectale, with distinct carbohydrate metabolism potential, was nearly absent in tCeD patients.Conclusion: Our study sheds light on the complex interplay between the gut microbiome and CeD, revealing unique microbial patterns and increased inter-individual variation among tCeD patients. These findings expand our understanding of the role of the microbiome in intestinal health and disease.Highlights: Shotgun metagenomic sequencing of the largest coeliac disease (CeD) patient cohort to date provides insights into gut microbiome composition down to the strain level. Novel associations between tCeD (treated CeD; adhering to a gluten-free diet) were identified. tCeD patients have a less uniform microbiome structure. Bacteria display higher mutation frequency in tCeD, compared to controls. The European subspecies of Eubacterium rectale is almost absent in tCeD patients.

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