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      Responses of Intestinal Microbiota and Immunity to Increasing Dietary Levels of Iron Using a Piglet Model

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          Abstract

          Iron is an essential metal for both animals and microbiota. In general, neonates and infants of humans and animals are at the risk of iron insufficiency. However, excess dietary iron usually causes negative impacts on the host and microbiota. This study aimed to investigate overloaded dietary iron supplementation on growth performance, the distribution pattern of iron in the gut lumen and the host, intestinal microbiota, and intestine transcript profile of piglets. Sixty healthy weaning piglets were randomly assigned to six groups: fed on diets supplemented with ferrous sulfate monohydrate at the dose of 50 ppm (Fe50 group), 100 ppm (Fe100 group), 200 ppm (Fe200 group), 500 ppm (Fe500 group), and 800 ppm (Fe800), separately, for 3 weeks. The results indicated that increasing iron had no significant effects on growth performance, but increased diarrheal risk and iron deposition in intestinal digesta, tissues of intestine and liver, and serum. High iron also reduced serum iron-binding capacity, apolipoprotein, and immunoglobin A. The RNA-sequencing analysis revealed that iron changed colonic transcript profile, such as interferon gamma-signal transducer and activator of transcription two-based anti-infection gene network. Increasing iron also shifted colonic and cecal microbiota, such as reducing alpha diversity and the relative abundance of Clostridiales and Lactobacillus reuteri and increasing the relative abundance of Lactobacillus and Lactobacillus amylovorus. Collectively, this study demonstrated that high dietary iron increased diarrheal incidence, changed intestinal immune response-associated gene expression, and shifted gut microbiota. The results would enhance our knowledge of iron effects on the gut and microbiome in piglets and further contribute to understanding these aspects in humans.

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          Most cited references52

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          Interaction between microbiota and immunity in health and disease

          The interplay between the commensal microbiota and the mammalian immune system development and function includes multifold interactions in homeostasis and disease. The microbiome plays critical roles in the training and development of major components of the host’s innate and adaptive immune system, while the immune system orchestrates the maintenance of key features of host-microbe symbiosis. In a genetically susceptible host, imbalances in microbiota-immunity interactions under defined environmental contexts are believed to contribute to the pathogenesis of a multitude of immune-mediated disorders. Here, we review features of microbiome-immunity crosstalk and their roles in health and disease, while providing examples of molecular mechanisms orchestrating these interactions in the intestine and extra-intestinal organs. We highlight aspects of the current knowledge, challenges and limitations in achieving causal understanding of host immune-microbiome interactions, as well as their impact on immune-mediated diseases, and discuss how these insights may translate towards future development of microbiome-targeted therapeutic interventions.
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            Iron in infection and immunity.

            Iron is an essential nutrient for both humans and pathogenic microbes. Because of its ability to exist in one of two oxidation states, iron is an ideal redox catalyst for diverse cellular processes including respiration and DNA replication. However, the redox potential of iron also contributes to its toxicity; thus, iron concentration and distribution must be carefully controlled. Given the absolute requirement for iron by virtually all human pathogens, an important facet of the innate immune system is to limit iron availability to invading microbes in a process termed nutritional immunity. Successful human pathogens must therefore possess mechanisms to circumvent nutritional immunity in order to cause disease. In this review, we discuss regulation of iron metabolism in the setting of infection and delineate strategies used by human pathogens to overcome iron-withholding defenses. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Metal homeostasis and resistance in bacteria

              In this Review, Chandrangsu et al. discuss recent insights into metalloregulatory systems that are used by bacteria and how they respond to metal limitation and intoxication, as well as how these systems influence host–pathogen interactions.
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                Author and article information

                Contributors
                Journal
                Front Cell Dev Biol
                Front Cell Dev Biol
                Front. Cell Dev. Biol.
                Frontiers in Cell and Developmental Biology
                Frontiers Media S.A.
                2296-634X
                17 December 2020
                2020
                : 8
                : 603392
                Affiliations
                [1] 1National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Key Laboratory of Agro-Ecology, Institute of Subtropical Agriculture, Chinese Academy of Sciences , Changsha, China
                [2] 2University of the Chinese Academy of Sciences , Beijing, China
                [3] 3College of Animal Science and Technology, Hunan Agriculture University, Hunan Co-Innovation Center of Animal Production Safety , Changsha, China
                [4] 4Animal Nutrition and Human Health Laboratory, School of Life Sciences, Hunan Normal University , Changsha, China
                [5] 5Yiyang Vocational Technical College , Yiyang, China
                [6] 6State Key Laboratory of Microbial Technology, Shandong University , Qingdao, China
                Author notes

                Edited by: Jun Fang, Hunan Agricultural University, China

                Reviewed by: Ruqing Zhong, Institute of Animal Science, Chinese Academy of Agricultural Sciences, China; Xiangbing Mao, Institute of Animal Nutrition, Sichuan Agricultural University, China

                *Correspondence: Huansheng Yang, yhs@ 123456hunnu.edu.cn

                These authors have contributed equally to this work

                This article was submitted to Molecular Medicine, a section of the journal Frontiers in Cell and Developmental Biology

                Article
                10.3389/fcell.2020.603392
                7773786
                33392192
                b6ec1af5-8ddc-423f-bb89-42fd68399586
                Copyright © 2020 Chen, Wu, Wang, Shao, Tu, Yang, Yin and Yin.

                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
                : 06 September 2020
                : 05 October 2020
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 52, Pages: 13, Words: 0
                Categories
                Cell and Developmental Biology
                Original Research

                iron overload,pig,diarrhea,immunity,microbiota,lactobacillus
                iron overload, pig, diarrhea, immunity, microbiota, lactobacillus

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