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      Transcriptomics analysis of host liver and meta-transcriptome analysis of rumen epimural microbial community in young calves treated with artificial dosing of rumen content from adult donor cow

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          Abstract

          In mammals, microbial colonization of the digestive tract (GIT) occurs right after birth by several bacterial phyla. Numerous human and mouse studies have reported the importance of early gut microbial inhabitants on host health. However, few attempts have been undertaken to directly interrogate the role of early gut/rumen microbial colonization on GIT development or host health in neonatal ruminants through artificial manipulation of the rumen microbiome. Thus, the molecular changes associated with bacterial colonization are largely unknown in cattle. In this study, we dosed young calves with exogenous rumen fluid obtained from an adult donor cow, starting at birth, and repeated every other week until six weeks of age. Eight Holstein bull calves were included in this study and were separated into two groups of four: the first group was treated with rumen content freshly extracted from an adult cow, and the second group was treated with sterilized rumen content. Using whole-transcriptome RNA-sequencing, we investigated the transcriptional changes in the host liver, which is a major metabolic organ and vital to the calf’s growth performance. Additionally, the comparison of rumen epimural microbial communities between the treatment groups was performed using the rRNA reads generated by sequencing. Liver transcriptome changes were enriched with genes involved in cell signaling and protein phosphorylation. Specifically, up-regulation of SGPL1 suggests a potential increase in the metabolism of sphingolipids, an essential molecular signal for bacterial survival in digestive tracts. Notably, eight genera, belonging to four phyla, had significant increases in abundance in treated calves. Our study provides insight into host liver transcriptome changes associated with early colonization of the microbial communities in neonatal calves. Such knowledge provides a foundation for future probiotics-based research in microbial organism mediated rumen development and nutrition in ruminants.

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          Most cited references40

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          DAVID: Database for Annotation, Visualization, and Integrated Discovery.

          Functional annotation of differentially expressed genes is a necessary and critical step in the analysis of microarray data. The distributed nature of biological knowledge frequently requires researchers to navigate through numerous web-accessible databases gathering information one gene at a time. A more judicious approach is to provide query-based access to an integrated database that disseminates biologically rich information across large datasets and displays graphic summaries of functional information. Database for Annotation, Visualization, and Integrated Discovery (DAVID; http://www.david.niaid.nih.gov) addresses this need via four web-based analysis modules: 1) Annotation Tool - rapidly appends descriptive data from several public databases to lists of genes; 2) GoCharts - assigns genes to Gene Ontology functional categories based on user selected classifications and term specificity level; 3) KeggCharts - assigns genes to KEGG metabolic processes and enables users to view genes in the context of biochemical pathway maps; and 4) DomainCharts - groups genes according to PFAM conserved protein domains. Analysis results and graphical displays remain dynamically linked to primary data and external data repositories, thereby furnishing in-depth as well as broad-based data coverage. The functionality provided by DAVID accelerates the analysis of genome-scale datasets by facilitating the transition from data collection to biological meaning.
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            A microbial symbiosis factor prevents intestinal inflammatory disease.

            Humans are colonized by multitudes of commensal organisms representing members of five of the six kingdoms of life; however, our gastrointestinal tract provides residence to both beneficial and potentially pathogenic microorganisms. Imbalances in the composition of the bacterial microbiota, known as dysbiosis, are postulated to be a major factor in human disorders such as inflammatory bowel disease. We report here that the prominent human symbiont Bacteroides fragilis protects animals from experimental colitis induced by Helicobacter hepaticus, a commensal bacterium with pathogenic potential. This beneficial activity requires a single microbial molecule (polysaccharide A, PSA). In animals harbouring B. fragilis not expressing PSA, H. hepaticus colonization leads to disease and pro-inflammatory cytokine production in colonic tissues. Purified PSA administered to animals is required to suppress pro-inflammatory interleukin-17 production by intestinal immune cells and also inhibits in vitro reactions in cell cultures. Furthermore, PSA protects from inflammatory disease through a functional requirement for interleukin-10-producing CD4+ T cells. These results show that molecules of the bacterial microbiota can mediate the critical balance between health and disease. Harnessing the immunomodulatory capacity of symbiosis factors such as PSA might potentially provide therapeutics for human inflammatory disorders on the basis of entirely novel biological principles.
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              Bioactive sphingolipids: metabolism and function.

              Sphingolipids (SLs) are essential constituents of eukaryotic cells. Besides playing structural roles in cellular membranes, some metabolites, including ceramide, sphingosine, and sphingosine-1-phosphate, have drawn attention as bioactive signaling molecules involved in the regulation of cell growth, differentiation, senescence, and apoptosis. Understanding the many cell regulatory functions of SL metabolites requires an advanced knowledge of how and where in the cell they are generated, converted, or degraded. This review will provide a short overview of the metabolism, localization, and compartmentalization of SLs. Also, a discussion on bioactive members of the SL family and inducers of SL enzymes that lead to ceramide generation will be presented.
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                Author and article information

                Contributors
                wenli.li@ars.usda.gov
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                28 January 2019
                28 January 2019
                2019
                : 9
                : 790
                Affiliations
                [1 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, The Cell Wall Utilization and Biology Laboratory, , US Dairy Forage Research Center, USDA ARS, ; Madison, WI 53706 USA
                [2 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Biology, , University of Wisconsin-Madison, ; Madison, WI 53706 USA
                [3 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Genetics, , University of Wisconsin-Madison, ; Madison, WI 53706 USA
                [4 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Microbiology, , University of Wisconsin-Madison, ; Madison, WI 53706 USA
                [5 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Medical Sciences, School of Veterinary Medicine, , University of Wisconsin-Madison, ; Madison, WI 53706 USA
                [6 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, Cereal Crops Research Unit – USDA, 502 Walnut Street Madison, ; Madison, WI 53726 USA
                Author information
                http://orcid.org/0000-0002-0946-5061
                http://orcid.org/0000-0001-7897-6896
                http://orcid.org/0000-0003-2223-9285
                Article
                37033
                10.1038/s41598-018-37033-4
                6349911
                30692556
                034fd9d4-93e5-420b-a44d-a17f7d72aba1
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 19 July 2018
                : 25 November 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/100007917, United States Department of Agriculture | Agricultural Research Service (USDA Agricultural Research Service);
                Award ID: 5090-31000-026-00D
                Award ID: 5090-31000-026-00D
                Award Recipient :
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