Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism

Abstract MicroRNAs (miRNAs), as important post-transcriptional regulators, are ubiquitous in various tissues. The aim of this exploratory study was to determine the presence of miRNAs in rumen fluid, and to investigate the possibility of miRNA-mediated cross-talk within the ruminal ecosystem. Rumen...

Full description

Bibliographic Details
Main Authors: Sara Ricci, Renée M. Petri, Cátia Pacífico, Ezequias Castillo-Lopez, Raul Rivera-Chacon, Arife Sener-Aydemir, Nicole Reisinger, Qendrim Zebeli, Susanne Kreuzer-Redmer
Format: Article
Language:English
Published: Nature Portfolio 2022-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-17445-z
_version_ 1828150654144610304
author Sara Ricci
Renée M. Petri
Cátia Pacífico
Ezequias Castillo-Lopez
Raul Rivera-Chacon
Arife Sener-Aydemir
Nicole Reisinger
Qendrim Zebeli
Susanne Kreuzer-Redmer
author_facet Sara Ricci
Renée M. Petri
Cátia Pacífico
Ezequias Castillo-Lopez
Raul Rivera-Chacon
Arife Sener-Aydemir
Nicole Reisinger
Qendrim Zebeli
Susanne Kreuzer-Redmer
author_sort Sara Ricci
collection DOAJ
description Abstract MicroRNAs (miRNAs), as important post-transcriptional regulators, are ubiquitous in various tissues. The aim of this exploratory study was to determine the presence of miRNAs in rumen fluid, and to investigate the possibility of miRNA-mediated cross-talk within the ruminal ecosystem. Rumen fluid samples from four cannulated Holstein cows were collected during two feeding regimes (forage and high-grain diet) and DNA and RNA were extracted for amplicon and small RNA sequencing. Epithelial biopsies were simultaneously collected to investigate the co-expression of miRNAs in papillae and rumen fluid. We identified 377 miRNAs in rumen fluid and 638 in rumen papillae, of which 373 were shared. Analysis of microbiota revealed 20 genera to be differentially abundant between the two feeding regimes, whereas no difference in miRNAs expression was detected. Correlations with at least one genus were found for 170 miRNAs, of which, 39 were highly significant (r > |0.7| and P < 0.01). Both hierarchical clustering of the correlation matrix and WGCNA analysis identified two main miRNA groups. Putative target and functional prediction analysis for the two groups revealed shared pathways with the predicted metabolic activities of the microbiota. Hence, our study supports the hypothesis of a cross-talk within the rumen at least partly mediated by miRNAs.
first_indexed 2024-04-11T21:46:21Z
format Article
id doaj.art-f3d57ab0f4cb435b86c4853a1cba345c
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-04-11T21:46:21Z
publishDate 2022-08-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-f3d57ab0f4cb435b86c4853a1cba345c2022-12-22T04:01:24ZengNature PortfolioScientific Reports2045-23222022-08-0112111510.1038/s41598-022-17445-zCharacterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanismSara Ricci0Renée M. Petri1Cátia Pacífico2Ezequias Castillo-Lopez3Raul Rivera-Chacon4Arife Sener-Aydemir5Nicole Reisinger6Qendrim Zebeli7Susanne Kreuzer-Redmer8Christian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineAgriculture and Agri-Food Canada, Sherbrooke Research and Development CentreChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineDSM, BIOMIN Research CenterChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineChristian Doppler Laboratory for Innovative Gut Health Concepts of Livestock, Department for Farm Animals and Veterinary Public Health, Institute of Animal Nutrition and Functional Plant Compounds, University of Veterinary MedicineAbstract MicroRNAs (miRNAs), as important post-transcriptional regulators, are ubiquitous in various tissues. The aim of this exploratory study was to determine the presence of miRNAs in rumen fluid, and to investigate the possibility of miRNA-mediated cross-talk within the ruminal ecosystem. Rumen fluid samples from four cannulated Holstein cows were collected during two feeding regimes (forage and high-grain diet) and DNA and RNA were extracted for amplicon and small RNA sequencing. Epithelial biopsies were simultaneously collected to investigate the co-expression of miRNAs in papillae and rumen fluid. We identified 377 miRNAs in rumen fluid and 638 in rumen papillae, of which 373 were shared. Analysis of microbiota revealed 20 genera to be differentially abundant between the two feeding regimes, whereas no difference in miRNAs expression was detected. Correlations with at least one genus were found for 170 miRNAs, of which, 39 were highly significant (r > |0.7| and P < 0.01). Both hierarchical clustering of the correlation matrix and WGCNA analysis identified two main miRNA groups. Putative target and functional prediction analysis for the two groups revealed shared pathways with the predicted metabolic activities of the microbiota. Hence, our study supports the hypothesis of a cross-talk within the rumen at least partly mediated by miRNAs.https://doi.org/10.1038/s41598-022-17445-z
spellingShingle Sara Ricci
Renée M. Petri
Cátia Pacífico
Ezequias Castillo-Lopez
Raul Rivera-Chacon
Arife Sener-Aydemir
Nicole Reisinger
Qendrim Zebeli
Susanne Kreuzer-Redmer
Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
Scientific Reports
title Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
title_full Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
title_fullStr Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
title_full_unstemmed Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
title_short Characterization of presence and activity of microRNAs in the rumen of cattle hints at possible host-microbiota cross-talk mechanism
title_sort characterization of presence and activity of micrornas in the rumen of cattle hints at possible host microbiota cross talk mechanism
url https://doi.org/10.1038/s41598-022-17445-z
work_keys_str_mv AT sararicci characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT reneempetri characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT catiapacifico characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT ezequiascastillolopez characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT raulriverachacon characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT arifeseneraydemir characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT nicolereisinger characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT qendrimzebeli characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism
AT susannekreuzerredmer characterizationofpresenceandactivityofmicrornasintherumenofcattlehintsatpossiblehostmicrobiotacrosstalkmechanism