Multi-omics analysis reveals the effects of host-rumen microbiota interactions on growth performance in a goat model

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Abstract

The growth rate of young ruminants has been associated with production performance in later life, with recent studies highlighting the importance of rumen microbes in supporting the health and growth of ruminants. However, the specific role of rumen epithelium bacteria and microbiota-host interactions in influencing the early life growth rate of ruminants remains poorly understood. In this study, we investigated the rumen fermentation pattern, microbiota characteristics, and global gene expression profiles of the rumen epithelium in 6-month-old goats with varying growth rates. Our results showed that goats with high average daily gain (HADG) exhibited higher rumen propionate concentrations. Goats with low average daily gain (LADG) had the higher relative abundances of rumen epithelium bacteria genera U29-B03 and Quinella, while exhibiting a lower relative abundance of Lachnospiraceae UCG-009. In the rumen fluid, the relative abundances of bacteria genus Alloprevotella were lower and Desulfovibrio were higher in LADG goats compared to HADG goats. Additionally, the relative abundance of fungal genus Symmetrospora was lower in LADG goats compared to HADG goats. Transcriptome analysis showed that 415 genes were differentially expressed between LADG and HADG goats, which were enriched in functions related to cell junction and cell adhesion, etc. Correlation analysis revealed that rumen epithelium bacteria genera UCG-005 and Candidatus Saccharimonas were negatively associated, while Lachnospiraceae NK3A20 group and Oscillospiraceae NK4A214 group were positively associated with average daily gain (ADG) and genes related to barrier function. The rumen fluid bacteria genus Alloprevotella was positively correlated, while Desulfovibrio was negatively correlated with rumen propionate and ammoniacal nitrogen (NH ₃-N) concentrations, as well as genes related to barrier function and short chain fatty acids (SCFAs) transport. In summary, our study reveals that the higher ruminal fermentation efficiency, improved rumen epithelial barrier functions, and enhanced SCFAs transport in HADG goats could be attributed to the rumen microbiota, particularly the rumen epithelium bacteria, such as Lachnospiraceae and Oscillospiraceae NK4A214 group.

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Most cited references 43

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Methane emissions from cattle.

K A Johnson, D E Johnson (1995)

Increasing atmospheric concentrations of methane have led scientists to examine its sources of origin. Ruminant livestock can produce 250 to 500 L of methane per day. This level of production results in estimates of the contribution by cattle to global warming that may occur in the next 50 to 100 yr to be a little less than 2%. Many factors influence methane emissions from cattle and include the following: level of feed intake, type of carbohydrate in the diet, feed processing, addition of lipids or ionophores to the diet, and alterations in the ruminal microflora. Manipulation of these factors can reduce methane emissions from cattle. Many techniques exist to quantify methane emissions from individual or groups of animals. Enclosure techniques are precise but require trained animals and may limit animal movement. Isotopic and nonisotopic tracer techniques may also be used effectively. Prediction equations based on fermentation balance or feed characteristics have been used to estimate methane production. These equations are useful, but the assumptions and conditions that must be met for each equation limit their ability to accurately predict methane production. Methane production from groups of animals can be measured by mass balance, micrometeorological, or tracer methods. These techniques can measure methane emissions from animals in either indoor or outdoor enclosures. Use of these techniques and knowledge of the factors that impact methane production can result in the development of mitigation strategies to reduce methane losses by cattle. Implementation of these strategies should result in enhanced animal productivity and decreased contributions by cattle to the atmospheric methane budget.

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Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants

Sheerli Shabat, Goor Sasson, Adi Doron-Faigenboim … (2016)

Ruminants have the remarkable ability to convert human-indigestible plant biomass into human-digestible food products, due to a complex microbiome residing in the rumen compartment of their upper digestive tract. Here we report the discovery that rumen microbiome components are tightly linked to cows' ability to extract energy from their feed, termed feed efficiency. Feed efficiency was measured in 146 milking cows and analyses of the taxonomic composition, gene content, microbial activity and metabolomic composition was performed on the rumen microbiomes from the 78 most extreme animals. Lower richness of microbiome gene content and taxa was tightly linked to higher feed efficiency. Microbiome genes and species accurately predicted the animals' feed efficiency phenotype. Specific enrichment of microbes and metabolic pathways in each of these microbiome groups resulted in better energy and carbon channeling to the animal, while lowering methane emissions to the atmosphere. This ecological and mechanistic understanding of the rumen microbiome could lead to an increase in available food resources and environmentally friendly livestock agriculture.

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Taxonomic identification of commensal bacteria associated with the mucosa and digesta throughout the gastrointestinal tracts of preweaned calves.

Nilusha Malmuthuge, Philip Griebel, Le Luo Guan (2014)

Bacterial colonization in the gastrointestinal tracts (GIT) of preweaned calves is very important, since it can influence early development and postweaning performance and health. This study investigated the composition of the bacteria along the GIT (rumen, jejunum, ileum, cecum, and colon) of preweaned bull calves (3 weeks old) using pyrosequencing to understand the segregation of bacteria between the mucosal surface and digesta. Phylogenetic analysis revealed that a total of 83 genera belonging to 13 phyla were distributed throughout the GIT of preweaned calves, with the Firmicutes, Bacteroidetes, and Proteobacteria predominating. Quantitative PCR (qPCR) analysis of selected abundant bacterial genera (Prevotella, Bacteroides, Lactobacillus, and Faecalibacterium) revealed that their prevalence was significantly different among the GIT regions and between mucosa- and digesta-associated communities. Rumens contained the most diverse bacterial population, consisting of 47 genera, including 16 rumen-specific genera, followed by the large intestine and then the small intestine. Bacterial species richness was higher at the mucosal surface than in the local digesta, with the exception of the rumen. The majority of bacteria found on the rumen epithelial surface and within the small intestine could not be identified due to a lack of known genus-level information. Thus, future studies will be required to fully characterize the microbiome during the development of the rumens and the mucosal immune systems of newborn calves. This is the first study to analyze in depth the bacterial composition of the GIT microbiome in preweaned calves, which extends previous findings regarding early rumen colonization and bacterial segregation between mucosa- and digesta-associated microbial communities.

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Author and article information

Contributors

Juncai Chen: URI : https://loop.frontiersin.org/people/1456453/overviewRole: Role: Role: Role:

Xiaoli Zhang: Role: Role: Role:

Xuan Chang: Role: Role:

Bingni Wei: Role: Role:

Yan Fang: Role: Role: Role: Role:

Shanshan Song: Role: Role: Role:

Daxiang Gong: Role: Role: Role:

Deli Huang: Role: Role: Role:

Yawang Sun: URI : https://loop.frontiersin.org/people/1986230/overviewRole: Role: Role:

Xianwen Dong: URI : https://loop.frontiersin.org/people/1894349/overviewRole: Role: Role:

Yongju Zhao: URI : https://loop.frontiersin.org/people/1410642/overviewRole: Role: Role:

Zhongquan Zhao: Role: Role: Role:

Journal

Journal ID (nlm-ta): Front Microbiol

Journal ID (iso-abbrev): Front Microbiol

Journal ID (publisher-id): Front. Microbiol.

Title: Frontiers in Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-302X

Publication date (Electronic): 09 September 2024

Publication date Collection: 2024

Volume: 15

Electronic Location Identifier: 1445223

Affiliations

[1] ¹College of Animal Science and Technology, Chongqing Key Laboratory of Herbivore Science, Southwest University , Chongqing, China

[2] ²Tengda Animal Husbandry Co., Ltd. , Chongqing, China

[3] ³Chongqing Academy of Animal Science , Chongqing, China

Author notes

Edited by: Jie Yin, Hunan Agricultural University, China

Reviewed by: Limei Lin, Nanjing Agricultural University, China

Lifeng Dong, Chinese Academy of Agricultural Sciences, China

*Correspondence: Zhongquan Zhao, zhongquanzhao@ 123456126.com

Juncai Chen, juncai.chen@ 123456hotmail.com

^†These authors have contributed equally to this work

Article

DOI: 10.3389/fmicb.2024.1445223

PMC ID: 11417024

PubMed ID: 39314883

SO-VID: 53537244-ad99-4446-a127-cfe80d079eb5

License:

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.

History

Date received : 07 June 2024

Date accepted : 30 August 2024

Page count

Figures: 8, Tables: 1, Equations: 0, References: 43, Pages: 13, Words: 7033

Funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was supported by the National Natural Science Foundation of China (32202686), Key project of Chong Qing Natural Science Foundation (grant number. cstc2020jcyj-zdxmX0005), The Strategic Collaboration Project jointly funded by Chongqing Municipal People's Government and Chinese Academy of Agricultural Sciences, and Chongqing Municipal Training Program of Innovation and Entrepreneurship for Undergraduates (grant number X202310635055).

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section-at-acceptance Microbial Symbioses

ScienceOpen disciplines: Microbiology & Virology

Keywords: microbes,rumen epithelium,transcriptome,growth rate,goat

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ScienceOpen disciplines: Microbiology & Virology

Keywords: microbes, rumen epithelium, transcriptome, growth rate, goat

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Multi-omics analysis reveals the effects of host-rumen microbiota interactions on growth performance in a goat model

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Abstract

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Most cited references 43

Methane emissions from cattle.

Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants

Taxonomic identification of commensal bacteria associated with the mucosa and digesta throughout the gastrointestinal tracts of preweaned calves.

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