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Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas

Ruminants digest plant biomass more efficiently than monogastric animals due to their symbiotic relationship with a complex microbiota residing in the rumen environment. What remains unclear is the relationship between the rumen microbial taxonomic and functional composition and feed efficiency (FE)...

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Autores principales: Fregulia, Priscila, Campos, Mariana Magalhães, Dias, Roberto Júnio Pedroso, Liu, Junhong, Guo, Wei, Pereira, Luiz Gustavo Ribeiro, Machado, Marco Antônio, Faza, Daniele Ribeiro de Lima Reis, Guan, Le Luo, Garnsworthy, Phil C., Neves, André Luis Alves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9745175/
https://www.ncbi.nlm.nih.gov/pubmed/36523842
http://dx.doi.org/10.3389/fmicb.2022.1025173
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author Fregulia, Priscila
Campos, Mariana Magalhães
Dias, Roberto Júnio Pedroso
Liu, Junhong
Guo, Wei
Pereira, Luiz Gustavo Ribeiro
Machado, Marco Antônio
Faza, Daniele Ribeiro de Lima Reis
Guan, Le Luo
Garnsworthy, Phil C.
Neves, André Luis Alves
author_facet Fregulia, Priscila
Campos, Mariana Magalhães
Dias, Roberto Júnio Pedroso
Liu, Junhong
Guo, Wei
Pereira, Luiz Gustavo Ribeiro
Machado, Marco Antônio
Faza, Daniele Ribeiro de Lima Reis
Guan, Le Luo
Garnsworthy, Phil C.
Neves, André Luis Alves
author_sort Fregulia, Priscila
collection PubMed
description Ruminants digest plant biomass more efficiently than monogastric animals due to their symbiotic relationship with a complex microbiota residing in the rumen environment. What remains unclear is the relationship between the rumen microbial taxonomic and functional composition and feed efficiency (FE), especially in crossbred dairy cattle (Holstein x Gyr) raised under tropical conditions. In this study, we selected twenty-two F1 Holstein x Gyr heifers and grouped them according to their residual feed intake (RFI) ranking, high efficiency (HE) (n = 11) and low efficiency (LE) (n = 11), to investigate the effect of FE on the rumen microbial taxa and their functions. Rumen fluids were collected using a stomach tube apparatus and analyzed using amplicon sequencing targeting the 16S (bacteria and archaea) and 18S (protozoa) rRNA genes. Alpha-diversity and beta-diversity analysis revealed no significant difference in the rumen microbiota between the HE and LE animals. Multivariate analysis (sPLS-DA) showed a clear separation of two clusters in bacterial taxonomic profiles related to each FE group, but in archaeal and protozoal profiles, the clusters overlapped. The sPLS-DA also revealed a clear separation in functional profiles for bacteria, archaea, and protozoa between the HE and LE animals. Microbial taxa were differently related to HE (e.g., Howardella and Shuttleworthia) and LE animals (e.g., Eremoplastron and Methanobrevibacter), and predicted functions were significatively different for each FE group (e.g., K03395—signaling and cellular process was strongly related to HE animals, and K13643—genetic information processing was related to LE animals). This study demonstrates that differences in the rumen microbiome relative to FE ranking are not directly observed from diversity indices (Faith’s Phylogenetic Diversity, Pielou’s Evenness, Shannon’s diversity, weighted UniFrac distance, Jaccard index, and Bray–Curtis dissimilarity), but from targeted identification of specific taxa and microbial functions characterizing each FE group. These results shed light on the role of rumen microbial taxonomic and functional profiles in crossbred Holstein × Gyr dairy cattle raised in tropical conditions, creating the possibility of using the microbial signature of the HE group as a biological tool for the development of biomarkers that improve FE in ruminants.
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spelling pubmed-97451752022-12-14 Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas Fregulia, Priscila Campos, Mariana Magalhães Dias, Roberto Júnio Pedroso Liu, Junhong Guo, Wei Pereira, Luiz Gustavo Ribeiro Machado, Marco Antônio Faza, Daniele Ribeiro de Lima Reis Guan, Le Luo Garnsworthy, Phil C. Neves, André Luis Alves Front Microbiol Microbiology Ruminants digest plant biomass more efficiently than monogastric animals due to their symbiotic relationship with a complex microbiota residing in the rumen environment. What remains unclear is the relationship between the rumen microbial taxonomic and functional composition and feed efficiency (FE), especially in crossbred dairy cattle (Holstein x Gyr) raised under tropical conditions. In this study, we selected twenty-two F1 Holstein x Gyr heifers and grouped them according to their residual feed intake (RFI) ranking, high efficiency (HE) (n = 11) and low efficiency (LE) (n = 11), to investigate the effect of FE on the rumen microbial taxa and their functions. Rumen fluids were collected using a stomach tube apparatus and analyzed using amplicon sequencing targeting the 16S (bacteria and archaea) and 18S (protozoa) rRNA genes. Alpha-diversity and beta-diversity analysis revealed no significant difference in the rumen microbiota between the HE and LE animals. Multivariate analysis (sPLS-DA) showed a clear separation of two clusters in bacterial taxonomic profiles related to each FE group, but in archaeal and protozoal profiles, the clusters overlapped. The sPLS-DA also revealed a clear separation in functional profiles for bacteria, archaea, and protozoa between the HE and LE animals. Microbial taxa were differently related to HE (e.g., Howardella and Shuttleworthia) and LE animals (e.g., Eremoplastron and Methanobrevibacter), and predicted functions were significatively different for each FE group (e.g., K03395—signaling and cellular process was strongly related to HE animals, and K13643—genetic information processing was related to LE animals). This study demonstrates that differences in the rumen microbiome relative to FE ranking are not directly observed from diversity indices (Faith’s Phylogenetic Diversity, Pielou’s Evenness, Shannon’s diversity, weighted UniFrac distance, Jaccard index, and Bray–Curtis dissimilarity), but from targeted identification of specific taxa and microbial functions characterizing each FE group. These results shed light on the role of rumen microbial taxonomic and functional profiles in crossbred Holstein × Gyr dairy cattle raised in tropical conditions, creating the possibility of using the microbial signature of the HE group as a biological tool for the development of biomarkers that improve FE in ruminants. Frontiers Media S.A. 2022-11-29 /pmc/articles/PMC9745175/ /pubmed/36523842 http://dx.doi.org/10.3389/fmicb.2022.1025173 Text en Copyright © 2022 Fregulia, Campos, Dias, Liu, Guo, Pereira, Machado, Faza, Guan, Garnsworthy and Neves. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Fregulia, Priscila
Campos, Mariana Magalhães
Dias, Roberto Júnio Pedroso
Liu, Junhong
Guo, Wei
Pereira, Luiz Gustavo Ribeiro
Machado, Marco Antônio
Faza, Daniele Ribeiro de Lima Reis
Guan, Le Luo
Garnsworthy, Phil C.
Neves, André Luis Alves
Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title_full Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title_fullStr Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title_full_unstemmed Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title_short Taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
title_sort taxonomic and predicted functional signatures reveal linkages between the rumen microbiota and feed efficiency in dairy cattle raised in tropical areas
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9745175/
https://www.ncbi.nlm.nih.gov/pubmed/36523842
http://dx.doi.org/10.3389/fmicb.2022.1025173
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