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      Longitudinal microbiome profiling reveals impermanence of probiotic bacteria in domestic pigeons

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          Abstract

          Probiotics are bacterial species or assemblages that are applied to animals and plants with the intention of altering the microbiome in a beneficial way. Probiotics have been linked to positive health effects such as faster disease recovery times in humans and increased weight gain in poultry. Pigeon fanciers often feed their show pigeons probiotics with the intention of increasing flight performance. The objective of our study was to determine the effect of two different probiotics, alone and in combination, on the fecal microbiome of Birmingham Roller pigeons. We sequenced fecal samples from 20 pigeons divided into three probiotic treatments, including prior to, during, and after treatment. Pre-treatment and control group samples were dominated by Actinobacteria, Firmicutes, Proteobacteria, and Cyanobacteria. Administration of a probiotic pellet containing Enterococcus faecium and Lactobacillus acidophilus resulted in increase in average relative abundance of Lactobacillus spp. from 4.7 ± 2.0% to 93.0 ± 5.3%. No significant effects of Enterococcus spp. were detected. Probiotic-induced shifts in the microbiome composition were temporary and disappeared within 2 days of probiotic cessation. Administration of a probiotic powder in drinking water that contained Enterococcus faecium and three Lactobacillus species had minimal effect on the microbiome. We conclude that supplementing Birmingham roller pigeons with the probiotic pellets, but not the probiotic powder, temporarily changed the microbiome composition. A next step is to experimentally test the effect of these changes in microbiome composition on host health and physical performance.

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          Most cited references37

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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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            Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications.

            Indigenous microbiota are an essential component in the modern concept of human health, but the composition and functional characteristics of a healthy microbiome remain to be precisely defined. Patterns of microbial colonization associated with disease states have been documented, but the health-associated microbial patterns and their functional characteristics are less clear. A healthy microbiome, considered in the context of body habitat or body site, could be described in terms of ecologic stability (i.e., ability to resist community structure change under stress or to rapidly return to baseline following a stress-related change), by an idealized (presumably health-associated) composition or by a desirable functional profile (including metabolic and trophic provisions to the host). Elucidation of the properties of healthy microbiota would provide a target for dietary interventions and/or microbial modifications aimed at sustaining health in generally healthy populations and improving the health of individuals exhibiting disrupted microbiota and associated diseases. Copyright © 2012 Elsevier Inc. All rights reserved.
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              Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature

              Probiotics are defined as live microorganisms, which when administered in adequate amounts, confer a health benefit on the host. Health benefits have mainly been demonstrated for specific probiotic strains of the following genera: Lactobacillus, Bifidobacterium, Saccharomyces, Enterococcus, Streptococcus, Pediococcus, Leuconostoc, Bacillus, Escherichia coli. The human microbiota is getting a lot of attention today and research has already demonstrated that alteration of this microbiota may have far-reaching consequences. One of the possible routes for correcting dysbiosis is by consuming probiotics. The credibility of specific health claims of probiotics and their safety must be established through science-based clinical studies. This overview summarizes the most commonly used probiotic microorganisms and their demonstrated health claims. As probiotic properties have been shown to be strain specific, accurate identification of particular strains is also very important. On the other hand, it is also demonstrated that the use of various probiotics for immunocompromised patients or patients with a leaky gut has also yielded infections, sepsis, fungemia, bacteraemia. Although the vast majority of probiotics that are used today are generally regarded as safe and beneficial for healthy individuals, caution in selecting and monitoring of probiotics for patients is needed and complete consideration of risk-benefit ratio before prescribing is recommended.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                17 June 2019
                2019
                : 14
                : 6
                : e0217804
                Affiliations
                [1 ] Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, United States of America
                [2 ] Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America
                [3 ] Department of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America
                [4 ] Independent Researcher: Sutton, Massachusetts, United States of America
                University of Illinois, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-6197-7139
                Article
                PONE-D-19-07064
                10.1371/journal.pone.0217804
                6578490
                31206549
                95e4c728-776b-43a9-90f5-2cfa408d3676
                © 2019 Grond et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 11 March 2019
                : 18 May 2019
                Page count
                Figures: 5, Tables: 2, Pages: 16
                Funding
                Funded by: Harvard University
                Award ID: Dean’s Competitive Fund for Promising Scholarship
                Award Recipient :
                Funded by: University of Connecticut
                Award ID: Start-up funding
                Award Recipient :
                Our study was funded by a Dean’s Competitive Fund for Promising Scholarship (Harvard University, Cambridge, MA) to CMC, and startup funds to SMH supplied by the University of Connecticut, Storrs, CT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Microbiology
                Probiotics
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Pigeons
                Biology and Life Sciences
                Organisms
                Bacteria
                Gut Bacteria
                Lactobacillus
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Animal Types
                Domestic Animals
                Biology and Life Sciences
                Zoology
                Animal Types
                Domestic Animals
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Shannon Index
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Shannon Index
                Custom metadata
                Sequences and metadata are available on Figshare at: Https://doi.org/10.6084/m9.figshare.7393037.v1.

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