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

Priscila Fregulia; Mariana Magalhães Campos; Roberto Júnio Pedroso Dias; Junhong Liu; Wei Guo; Luiz Gustavo Ribeiro Pereira; Marco Antônio Machado; Daniele Ribeiro de Lima Reis Faza; Le Luo Guan; Phil C Garnsworthy; André Luis Alves Neves

doi:10.3389/fmicb.2022.1025173

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

Front Microbiol. 2022 Nov 29:13:1025173. doi: 10.3389/fmicb.2022.1025173. eCollection 2022.

Affiliations

¹ Laboratório de Protozoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, Brazil.
² Programa de Pós-Graduação em Biodiversidade e Conservação da Natureza, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, Brazil.
³ Brazilian Agricultural Research Corporation (Empresa Brasileira de Pesquisa Agropecuária, EMBRAPA), National Center for Research on Dairy Cattle, Juiz de Fora, Minas Gerais, Brazil.
⁴ Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada.
⁵ Key Laboratory of Animal Genetics, Breeding and Reproduction in the Plateau Mountainous Region, Ministry of Education, Guizhou University, Guiyang, China.
⁶ School of Biosciences, University of Nottingham, Loughborough, United Kingdom.
⁷ Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg, Denmark.

Abstract

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.

Keywords: RFI; SSU rRNA; functional microbial composition; rumen microbiome; taxonomic microbial composition.

Grants and funding

All funding support was received from EMBRAPA, http://www.embrapa.br/, Project number: 02.13.05.007.00.00, title: “Development and integration of feed efficiency metrics for dairy cattle,” and from Future Food Beacon of Excellence—University Nottingham/Embrapa, Project 20500.20/0037-1, title “Rumen microbiome and its association with feed efficiency and methane emissions in dairy cattle under tropical conditions,” Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (APQ-02929-18). CNPq provided the research grant to RD (Bolsa de Produtividade PQ) and CAPES provided a grant to PF.