Article Text

Original research
Stool microRNA profiles reflect different dietary and gut microbiome patterns in healthy individuals
  1. Sonia Tarallo1,2,
  2. Giulio Ferrero3,4,
  3. Francesca De Filippis5,6,
  4. Antonio Francavilla1,2,
  5. Edoardo Pasolli5,6,
  6. Valentina Panero1,
  7. Francesca Cordero3,
  8. Nicola Segata7,
  9. Sara Grioni8,
  10. Ruggero Gaetano Pensa3,
  11. Barbara Pardini1,2,
  12. Danilo Ercolini5,6,
  13. Alessio Naccarati1,2
  1. 1 Italian Institute for Genomic Medicine (IIGM), c/o IRCCS Candiolo, Torino, Italy
  2. 2 Candiolo Cancer Institute - FPO IRCCS, Candiolo, Torino, Italy
  3. 3 Department of Computer Science, University of Torino, Torino, Italy
  4. 4 Department of Clinical and Biological Sciences, University of Torino, Torino, Italy
  5. 5 Department Agricultural Sciences, University of Naples Federico II, Portici, Napoli, Italy
  6. 6 Task Force on Microbiome Studies, University of Naples Federico II, Napoli, Italy
  7. 7 Centre for Integrative Biology, University of Trento, Trento, Italy
  8. 8 Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy
  1. Correspondence to Dr Alessio Naccarati, Molecular Epidemiology and Exposomics Unit, IIGM, Torino, Piemonte, Italy; alessio.naccarati{at}iigm.it; Professor Danilo Ercolini; ercolini{at}unina.it

Abstract

Objectives MicroRNA (miRNA) profiles have been evaluated in several biospecimens in relation to common diseases for which diet may have a considerable impact. We aimed at characterising how specific diets are associated with the miRNome in stool of vegans, vegetarians and omnivores and how this is reflected in the gut microbial composition, as this is still poorly explored.

Design We performed small RNA and shotgun metagenomic sequencing in faecal samples and dietary recording from 120 healthy volunteers, equally distributed for the different diets and matched for sex and age.

Results We found 49 miRNAs differentially expressed among vegans, vegetarians and omnivores (adj. p <0.05) and confirmed trends of expression levels of such miRNAs in vegans and vegetarians compared with an independent cohort of 45 omnivores. Two miRNAs related to lipid metabolism, miR-636 and miR-4739, were inversely correlated to the non-omnivorous diet duration, independently of subject age. Seventeen miRNAs correlated (|rho|>0.22, adj. p <0.05) with the estimated intake of nutrients, particularly animal proteins, phosphorus and, interestingly, lipids. In omnivores, higher Prevotella and Roseburia and lower Bacteroides abundances than in vegans and vegetarians were observed. Lipid metabolism-related miR-425-3p and miR-638 expression levels were associated with increased abundances of microbial species, such as Roseburia sp. CAG 182 and Akkermansia muciniphila, specific of different diets. An integrated analysis identified 25 miRNAs, 25 taxa and 7 dietary nutrients that clearly discriminated (area under the receiver operating characteristic curve=0.89) the three diets.

Conclusion Stool miRNA profiles are associated with specific diets and support the role of lipids as a driver of epigenetic changes and host-microbial molecular interactions in the gut.

  • diet
  • molecular genetics
  • colonic microflora

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Raw data are available upon request to the corresponding author.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

Statistics from Altmetric.com

Request Permissions

If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

Data availability statement

All data relevant to the study are included in the article or uploaded as supplementary information. Raw data are available upon request to the corresponding author.

View Full Text

Supplementary materials

Footnotes

  • ST, GF and FDF are joint first authors.

  • Twitter @nsegata, @rupensa, @BarbaraPardini1

  • BP, DE and AN contributed equally.

  • Contributors BP, ST and AN contributed to concept and design; BP, GF, RGP, SG, ST, VP and AN to collection and assembly of the data; BP, GF, ST, AF, FC and AN to small RNA-Seq data analyses and interpretation; DE, FDF, EP and NS to metagenomic data analyses and interpretation; ST, BP, GF, FC, DE, FDF and AN to manuscript writing; all authors gave final approval of the version.

  • Funding This work was supported by Fondazione Umberto Veronesi postdoctoral fellowships 2017 and 2018 (recipients, ST and BP), Compagnia di San Paolo Torino, Italy (to BP, AN, ST), Lega Italiana per La Lotta contro i Tumori (to FC, BP and AN), Fondazione CRT (grant number 2019-0450 to RGP) the European H2020 research project Oncobiome (Grant number 825410), and the COST action TRANSCOLONCAN (CA17118). DE laboratory received funding from the JPI HDHL-INTIMIC - Knowledge Platform of Food, Diet, Intestinal Microbiomics and Human Health (ID 790) grant and the PRIN2017 (20174FHBWR_005) grant by the Italian Ministry of University and Research.

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

Linked Articles