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      Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation

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          Abstract

          Background

          Heat stress (HS) jeopardizes intestinal barrier functions and augments intestinal permeability in pigs. However, whether HS-induced maternal microbial and metabolic changes in primiparous sows during late gestation remains elusive. We present here, a study investigating the fecal microbial and metabolic responses in late gestational primiparous sows when exposed to HS.

          Methods

          Twelve first-parity Landrace × Large White F1 sows were randomly assigned into two environmental treatments including the thermoneutral (TN) (18–22 °C; n = 6) and HS (28–32 °C; n = 6) conditions. Both treatments were applied from 85 d of gestation to farrowing. The serum and feces samples were collected on d 107 of gestation, for analyses including intestinal integrity biomarkers, high-throughput sequencing metagenomics, short-chain fatty acid (SCFA) profiles and nontargeted metabolomics.

          Results

          Our results show that HS group has higher serum Heat shock protein 70 (HSP70), lipopolysaccharide (LPS) and lipopolysaccharide-binding protein (LBP) levels. The gut microbial community can be altered upon HS by using β-diversity and taxon-based analysis. In particular, the relative abundance of genera and operational taxonomic units (OTUs) related to Clostridiales and Halomonas are higher in HS group, the relative abundance of genera and OTUs related to Bacteroidales and Streptococcus, however, are lower in HS group. Results of metabolic analysis reveal that HS lowers the concentrations of propionate, butyrate, total SCFA, succinate, fumarate, malate, lactate, aspartate, ethanolamine, β-alanine and niacin, whereas that of fructose and azelaic acid are higher in HS group. These metabolites mainly affect propanoate metabolism, alanine, aspartate and glutamate metabolism, phenylalanine metabolism, β-alanine metabolism, pantothenate and CoA biosynthesis, tricarboxylic acid cycle (TCA) and nicotinate and nicotinamide metabolism. Additionally, correlation analysis between significant microbes and metabolites indicated that the HS-induced microbiota shift is likely the cause of changes of intestinal metabolism.

          Conclusions

          Taken together, we reveal characteristic structural and metabolic changes in maternal gut microbiota as a result of late gestational HS, which could potentially provide the basis for further study on offspring gut microbiota and immune programming.

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          Most cited references 35

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          Commensal Clostridia: leading players in the maintenance of gut homeostasis

          The gastrointestinal tract is a complex and dynamic network where an intricate and mutualistic symbiosis modulates the relationship between the host and the microbiota in order to establish and ensure gut homeostasis. Commensal Clostridia consist of gram-positive, rod-shaped bacteria in the phylum Firmicutes and make up a substantial part of the total bacteria in the gut microbiota. They start to colonize the intestine of breastfed infants during the first month of life and populate a specific region in the intestinal mucosa in close relationship with intestinal cells. This position allows them to participate as crucial factors in modulating physiologic, metabolic and immune processes in the gut during the entire lifespan, by interacting with the other resident microbe populations, but also by providing specific and essential functions. This review focus on what is currently known regarding the role of commensal Clostridia in the maintenance of overall gut function, as well as touch on their potential contribution in the unfavorable alteration of microbiota composition (dysbiosis) that has been implicated in several gastrointestinal disorders. Commensal Clostridia are strongly involved in the maintenance of overall gut function. This leads to important translational implications in regard to the prevention and treatment of dysbiosis, to drug efficacy and toxicity, and to the development of therapies that may modulate the composition of the microflora, capitalizing on the key role of commensal Clostridia, with the end goal of promoting gut health.
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            Acetate utilization and butyryl coenzyme A (CoA):acetate-CoA transferase in butyrate-producing bacteria from the human large intestine.

            Seven strains of Roseburia sp., Faecalibacterium prausnitzii, and Coprococcus sp. from the human gut that produce high levels of butyric acid in vitro were studied with respect to key butyrate pathway enzymes and fermentation patterns. Strains of Roseburia sp. and F. prausnitzii possessed butyryl coenzyme A (CoA):acetate-CoA transferase and acetate kinase activities, but butyrate kinase activity was not detectable either in growing or in stationary-phase cultures. Although unable to use acetate as a sole source of energy, these strains showed net utilization of acetate during growth on glucose. In contrast, Coprococcus sp. strain L2-50 is a net producer of acetate and possessed detectable butyrate kinase, acetate kinase, and butyryl-CoA:acetate-CoA transferase activities. These results demonstrate that different functionally distinct groups of butyrate-producing bacteria are present in the human large intestine.
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              Bacteria, colonic fermentation, and gastrointestinal health.

              The colonic microbiota plays an important role in human digestive physiology and makes a significant contribution to homeostasis in the large bowel. The microbiome probably comprises thousands of different bacterial species. The principal metabolic activities of colonic microorganisms are associated with carbohydrate and protein digestion. Nutrients of dietary and host origin support the growth of intestinal organisms. Short-chain fatty acids (SCFAs), predominantly acetate, propionate, and butyrate, are the principal metabolites generated during the catabolism of carbohydrates and proteins. In contrast, protein digestion yields a greater diversity of end products, including SCFAs, amines, phenols, indoles, thiols, CO2, H2, and H2S, many of which have toxic properties. The majority of SCFAs are absorbed from the gut and metabolized in various body tissues, making a relatively small but significant contribution to the body's daily energy requirements. Carbohydrate fermentation is, for the most part, a beneficial process in the large gut, because the growth of saccharolytic bacteria stimulates their requirements for toxic products associated with putrefaction, for incorporation into cellular proteins, thereby protecting the host. However, as digestive materials move along the gut, carbohydrates become depleted, which may be linked to the increased prevalence of colonic disease in the distal bowel.
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                Author and article information

                Contributors
                2016205015@njau.edu.cn
                2017205024@njau.edu.cn
                zhengweijiang@njau.edu.cn
                yongqiangxue@126.com
                469458229@qq.com
                +86-25-84399830 , yaowen67jp@njau.edu.cn
                Journal
                J Anim Sci Biotechnol
                J Anim Sci Biotechnol
                Journal of Animal Science and Biotechnology
                BioMed Central (London )
                1674-9782
                2049-1891
                4 November 2019
                4 November 2019
                2019
                : 10
                Affiliations
                [1 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and Technology, , Nanjing Agricultural University, ; Nanjing, Jiangsu People’s Republic of China 210095
                [2 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, National Experimental Teaching Center for Animal Science, College of Animal Science and Technology, , Nanjing Agricultural University, ; Nanjing, Jiangsu People’s Republic of China 210095
                [3 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Key Laboratory of Animal Physiology and Biochemistry, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, , Nanjing Agricultural University, ; Nanjing, Jiangsu People’s Republic of China 210095
                Article
                391
                10.1186/s40104-019-0391-0
                6827230
                a2cc3771-a292-4c53-abd8-54deb9fac0bf
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Funding
                Funded by: National Key R&D Program of China (CN)
                Award ID: 2016YFD0500502
                Award Recipient :
                Funded by: Jiangsu Modern Agricultural (Swine) Industry Technology System (CN)
                Award ID: JATS[2018]287
                Award Recipient :
                Funded by: Postgraduate Research & Practice Innovation Program of Jiangsu Province
                Award ID: KYCX18_0698
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Animal science & Zoology

                heat stress, late gestation, metabolic profiles, microbial community, sow

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