Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes

Abstract Background In ruminants, early rumen development is vital for efficient fermentation that converts plant materials to human edible food such as milk and meat. Here, we investigate the extent and functional basis of host-microbial interactions regulating rumen development during the first 6 ...

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Main Authors: Nilusha Malmuthuge, Guanxiang Liang, Le Luo Guan
Format: Article
Language:English
Published: BMC 2019-08-01
Series:Genome Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13059-019-1786-0
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spelling doaj-4f26f571b9db4522b853cb917d0407d72020-11-25T03:40:51ZengBMCGenome Biology1474-760X2019-08-0120111610.1186/s13059-019-1786-0Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomesNilusha Malmuthuge0Guanxiang Liang1Le Luo Guan2Department of Agricultural, Food and Nutritional Science, University of AlbertaDepartment of Agricultural, Food and Nutritional Science, University of AlbertaDepartment of Agricultural, Food and Nutritional Science, University of AlbertaAbstract Background In ruminants, early rumen development is vital for efficient fermentation that converts plant materials to human edible food such as milk and meat. Here, we investigate the extent and functional basis of host-microbial interactions regulating rumen development during the first 6 weeks of life. Results The use of microbial metagenomics, together with quantification of volatile fatty acids (VFAs) and qPCR, reveals the colonization of an active bacterial community in the rumen at birth. Colonization of active complex carbohydrate fermenters and archaea with methyl-coenzyme M reductase activity was also observed from the first week of life in the absence of a solid diet. Integrating microbial metagenomics and host transcriptomics reveals only 26.3% of mRNA transcripts, and 46.4% of miRNAs were responsive to VFAs, while others were ontogenic. Among these, one host gene module was positively associated with VFAs, while two other host gene modules and one miRNA module were negatively associated with VFAs. Eight host genes and five miRNAs involved in zinc ion binding-related transcriptional regulation were associated with a rumen bacterial cluster consisting of Prevotella, Bacteroides, and Ruminococcus. Conclusion This three-way interaction suggests a potential role of bacteria-driven transcriptional regulation in early rumen development via miRNAs. Our results reveal a highly active early microbiome that regulates rumen development of neonatal calves at the cellular level, and miRNAs may coordinate these host-microbial interactions.http://link.springer.com/article/10.1186/s13059-019-1786-0NeonatesRumen developmentMetagenomeHost transcriptomeHost microRNAomeHost-microbial interactions
collection DOAJ
language English
format Article
sources DOAJ
author Nilusha Malmuthuge
Guanxiang Liang
Le Luo Guan
spellingShingle Nilusha Malmuthuge
Guanxiang Liang
Le Luo Guan
Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
Genome Biology
Neonates
Rumen development
Metagenome
Host transcriptome
Host microRNAome
Host-microbial interactions
author_facet Nilusha Malmuthuge
Guanxiang Liang
Le Luo Guan
author_sort Nilusha Malmuthuge
title Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
title_short Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
title_full Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
title_fullStr Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
title_full_unstemmed Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
title_sort regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes
publisher BMC
series Genome Biology
issn 1474-760X
publishDate 2019-08-01
description Abstract Background In ruminants, early rumen development is vital for efficient fermentation that converts plant materials to human edible food such as milk and meat. Here, we investigate the extent and functional basis of host-microbial interactions regulating rumen development during the first 6 weeks of life. Results The use of microbial metagenomics, together with quantification of volatile fatty acids (VFAs) and qPCR, reveals the colonization of an active bacterial community in the rumen at birth. Colonization of active complex carbohydrate fermenters and archaea with methyl-coenzyme M reductase activity was also observed from the first week of life in the absence of a solid diet. Integrating microbial metagenomics and host transcriptomics reveals only 26.3% of mRNA transcripts, and 46.4% of miRNAs were responsive to VFAs, while others were ontogenic. Among these, one host gene module was positively associated with VFAs, while two other host gene modules and one miRNA module were negatively associated with VFAs. Eight host genes and five miRNAs involved in zinc ion binding-related transcriptional regulation were associated with a rumen bacterial cluster consisting of Prevotella, Bacteroides, and Ruminococcus. Conclusion This three-way interaction suggests a potential role of bacteria-driven transcriptional regulation in early rumen development via miRNAs. Our results reveal a highly active early microbiome that regulates rumen development of neonatal calves at the cellular level, and miRNAs may coordinate these host-microbial interactions.
topic Neonates
Rumen development
Metagenome
Host transcriptome
Host microRNAome
Host-microbial interactions
url http://link.springer.com/article/10.1186/s13059-019-1786-0
work_keys_str_mv AT nilushamalmuthuge regulationofrumendevelopmentinneonatalruminantsthroughmicrobialmetagenomesandhosttranscriptomes
AT guanxiangliang regulationofrumendevelopmentinneonatalruminantsthroughmicrobialmetagenomesandhosttranscriptomes
AT leluoguan regulationofrumendevelopmentinneonatalruminantsthroughmicrobialmetagenomesandhosttranscriptomes
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