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Exploring the Rumen and Cecum Microbial Community from Fetus to Adulthood in Goat.

ABSTRACT: The present study aimed to investigate the colonization process of epithelial bacteria attached to the rumen and intestinal tract tissue during the development of goats after birth. However, this process from fetus to adulthood was very limited. In goats, the rumen and cecum are two important fermentation organs, and it is important to study the acquisition and development of the neonatal microbiome, as well as the difference between these two organs. To characterize the microbial establishment and dynamic changes in the rumen and cecum from fetus to adulthood, we performed 16S rRNA gene sequencing for 106 samples from 47 individuals of nine pregnant mother-fetus pairs and 16 kids from birth up to 6 months. The diversity, structure and composition of the microbial communities were distinct between the rumen and cecum after birth, while they were similar in the fetal period. The study showed a rapid loss and influx of microbes at birth, followed by slight selection after drinking colostrum, and then a strong selection after weaning, suggesting that the establishment and dynamic fluctuations of the gut microbiome undergoes three distinct phases of microbiome progression in life: a conserved phase (during late pregnancy in the fetus), a transitional phase (newborn until weaning), and a stable phase (from weaning to adulthood). The results supported the view that microbes exist in the fetus, and revealed the establishment and dynamic fluctuations of the gut microbiome from fetus to adulthood in goats.

SUBMITTER: Zou X

PROVIDER: S-EPMC7552217 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Exploring the Rumen and Cecum Microbial Community from Fetus to Adulthood in Goat.

Zou Xian X Liu Guangbin G Meng Fanming F Hong Linjun L Li Yaokun Y Lian Zhiquan Z Yang Zhenwei Z Luo Chenglong C Liu Dewu D

Animals : an open access journal from MDPI 20200911 9

The present study aimed to investigate the colonization process of epithelial bacteria attached to the rumen and intestinal tract tissue during the development of goats after birth. However, this process from fetus to adulthood was very limited. In goats, the rumen and cecum are two important fermentation organs, and it is important to study the acquisition and development of the neonatal microbiome, as well as the difference between these two organs. To characterize the microbial establishment ...[more]

PMID: 32932976

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Project description:BackgroundGoat rumen microbial communities are perceived as one of the most potential biochemical reservoirs of multi-functional enzymes, which are applicable to enhance wide array of bioprocesses such as the hydrolysis of cellulose and hemi-cellulose into fermentable sugar for biofuel and other value-added biochemical production. Even though, the limited understanding of rumen microbial genetic diversity and the absence of effective screening culture methods have impeded the full utilization of these potential enzymes. In this study, we applied culture independent metagenomics sequencing approach to isolate, and identify microbial communities in goat rumen, meanwhile, clone and functionally characterize novel cellulase and xylanase genes in goat rumen bacterial communities.ResultsBacterial DNA samples were extracted from goat rumen fluid. Three genomic libraries were sequenced using Illumina HiSeq 2000 for paired-end 100-bp (PE100) and Illumina HiSeq 2500 for paired-end 125-bp (PE125). A total of 435gb raw reads were generated. Taxonomic analysis using Graphlan revealed that Fibrobacter, Prevotella, and Ruminococcus are the most abundant genera of bacteria in goat rumen. SPAdes assembly and prodigal annotation were performed. The contigs were also annotated using the DOE-JGI pipeline. In total, 117,502 CAZymes, comprising endoglucanases, exoglucanases, beta-glucosidases, xylosidases, and xylanases, were detected in all three samples. Two genes with predicted cellulolytic/xylanolytic activities were cloned and expressed in E. coli BL21(DE3). The endoglucanases and xylanase enzymatic activities of the recombinant proteins were confirmed using substrate plate assay and dinitrosalicylic acid (DNS) analysis. The 3D structures of endoglucanase A and endo-1,4-beta xylanase was predicted using the Swiss Model. Based on the 3D structure analysis, the two enzymes isolated from goat's rumen metagenome are unique with only 56-59% similarities to those homologous proteins in protein data bank (PDB) meanwhile, the structures of the enzymes also displayed greater stability, and higher catalytic activity.ConclusionsIn summary, this study provided the database resources of bacterial metagenomes from goat's rumen fluid, including gene sequences with annotated functions and methods for gene isolation and over-expression of cellulolytic enzymes; and a wealth of genes in the metabolic pathways affecting food and nutrition of ruminant animals.

Project description:BackgroundThe rumen is an ecosystem with a complex microbial microflora in which microbes initiate biofilm formation by attaching to plant surfaces for plant degradation and are capable of converting feed to nutrients and energy via microbial processes. Quorum sensing (QS) is a cell-to-cell communication mechanism that allows microbes to synchronize the expression of multiple genes in the group to perform social behaviors such as chemotaxis and biofilm formation using self-synthesized QS signaling molecules. Whereas QS has been extensively studied in model microorganisms under pure culture conditions, QS mechanisms are poorly understood in complex bacterial communities, such as the rumen microflora, in which cell-to-cell communication may be common.ResultsHere, we analyzed 981 rumens bacterial and archaeal genomes from the Joint Genome Institute (JGI) and GenBank databases and identified 15 types of known QS signaling molecule-related genes. The analysis of the prevalence and abundance of genes involved in QS showed that 767 microbial genomes appeared to possess QS-related genes, including 680 bacterial genomes containing autoinducer-2 (AI-2) synthase- or receptor-encoding genes. Prevotella, Butyivibrio, Ruminococcus, Oribacterium, Selenomonas, and Treponema, known abundant bacterial genera in the rumen, possessed the greatest numbers of AI-2-related genes; these genes were highly expressed within the metatranscriptome dataset, suggesting that intra- and interspecies communication mediated by AI-2 among rumen microbes was universal in the rumen. The QS processes mediated by the dCache_1-containing AI-2 receptors (CahRs) with various functional modules may be essential for degrading plants, digesting food, and providing energy and nutrients to the host. Additionally, a universal natural network based on QS revealed how rumen microbes coordinate social behaviors via the AI-2-mediated QS system, most of which may potentially function via AI-2 binding to the extracellular sensor dCache_1 domain to activate corresponding receptors involved in different signal transduction pathways, such as methyl-accepting chemotaxis proteins, histidine kinases, serine phosphatases, c-di-GMP synthases and phosphodiesterases, and serine/threonine kinases in the rumen.ConclusionsThe exploration of AI-2-related genes, especially CahR-type AI-2 receptors, greatly increased our insight into AI-2 as a potentially "universal" signal mediating social behaviors and will help us better understand microbial communication networks and the function of QS in plant-microbe interactions in complex microecosystems. Video Abstract.

Project description:Recently, the relationship between the goat host and its gastrointestinal microbiome has emerged as a hallmark of host-microbiota symbiosis, which was indispensable for the proper physiological function that convert the plant biomass to livestock products. However, little integrative information about the establishment of gastrointestinal microflora in goats exists. Herein, we characterized the colonizing process of the bacterial community in the digesta and mucosa of the rumen, cecum, and colon of the cashmere goat from birth to adulthood to compare its spatiotemporal difference via 16S rRNA gene sequencing. A total of 1,003 genera belonging to 43 phyla were identified. Principal coordinate analysis unveiled the similarity of microbial community between or within each age group increased and gradually developed toward mature whatever in digesta or mucosa. In the rumen, the composition of the bacterial community in digesta differed significantly from in mucosa across age groups; whereas in the hindgut, there was a high similarity of bacterial composition between the in digesta and mucosa in each age group before weaning, while the bacterial community structure differed markedly between these two types of samples after weaning. Taxonomic analysis indicated that 25 and 21 core genera coexisted in digesta and mucosa of the rumen and hindgut, respectively; but their abundances differed considerably by GIT region and/or age. In digesta, as goats aged, a lower abundance of Bacillus was observed with higher abundances of Prevotella 1 and Rikenellaceae RC9 in the rumen; while in the hindgut, the genera Escherichia-Shigella, Variovorax, and Stenotrophomonas decreased and Ruminococcaceae UCG-005, Ruminococcaceae UCG-010, and Alistipes increased with age increased. In mucosa, the rumen showed microbial dynamics with increases of Butyrivibrio 2 and Prevotellaceae UCG-001 and decreases of unclassified_f_Pasteurellaceae; while the genera Treponema 2 and Ruminococcaceae UCG-010 increased and Escherichia-Shigella decreased in the hindgut as goats aged. These results shed light on the colonization process of microbiota in the rumen and hindgut, which mainly include the initial, transit, and mature phases. Furthermore, there is a significant difference in the microbial composition between in digesta and mucosa, and both these exhibit a considerable spatiotemporal specificity.

Dataset Information

Exploring the Rumen and Cecum Microbial Community from Fetus to Adulthood in Goat.

Publications

Exploring the Rumen and Cecum Microbial Community from Fetus to Adulthood in Goat.

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