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      Captivity Shapes the Gut Microbiota of Andean Bears: Insights into Health Surveillance

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          Abstract

          The Andean bear is an endemic species of the tropical Andes who has an almost exclusively plant-based diet. Since herbivorous mammals do not carry enzymes for fiber degradation, the establishment of symbiosis with cellulolytic microorganisms in their gastrointestinal (GI) tract is necessary to help them fulfill their nutritional needs. Furthermore, as described for other mammals, a stable, diverse, and balanced gut microbial composition is an indicator of a healthy status of the host; under disturbances this balance can be lost, leading to potential diseases of the host. The goal of this study was to describe the gut microbiota of wild and captive Andean bears and determine how habitat status influences the composition and diversity of the gut symbiotic community. Fecal samples from wild ( n = 28) and captive ( n = 8) Andean bears were collected in “Reserva Pantano de Martos” and “Fundación Bioandina”, Colombia. Composition and diversity analyses were performed using amplicons from the V4 region of the 16S rDNA gene sequenced using the Ion PGM platform. PICRUSt algorithm was applied to predict the gene content of the gut microbiome of wild and captive Andean bears. A total of 5,411 and 838 OTUs were identified for wild and captive bears, respectively. Captive bears contained a lower number of bacterial phyla ( n = 7) compared to wild individuals ( n = 9). Proteobacteria (59.03%) and Firmicutes (14.03%) were the phyla that contributed the most to differences between wild and captive bears (overall dissimilarity = 87.72%). At family level, Enterobacteriaceae drove the main differences between the two groups (13.7%). PICRUSt metagenomics predictions suggested a similar pattern of relative abundance of gene families associated with the metabolism of carbohydrates across samples in wild individuals, despite the taxonomic differences of their gut microbiota. Captivity alters the availability and diversity of food resources, which likely reduces microbiota richness and diversity compared to wild individuals. Further considerations should be taken into account for nutritional schemes improving ex-situ conservation and its potential as a surveillance tool of endangered populations of wild Andean bears.

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          Most cited references36

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          QIIME allows analysis of high-throughput community sequencing data.

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            Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences

            Profiling phylogenetic marker genes, such as the 16S rRNA gene, is a key tool for studies of microbial communities but does not provide direct evidence of a community’s functional capabilities. Here we describe PICRUSt (Phylogenetic Investigation of Communities by Reconstruction of Unobserved States), a computational approach to predict the functional composition of a metagenome using marker gene data and a database of reference genomes. PICRUSt uses an extended ancestral-state reconstruction algorithm to predict which gene families are present and then combines gene families to estimate the composite metagenome. Using 16S information, PICRUSt recaptures key findings from the Human Microbiome Project and accurately predicts the abundance of gene families in host-associated and environmental communities, with quantifiable uncertainty. Our results demonstrate that phylogeny and function are sufficiently linked that this ‘predictive metagenomic’ approach should provide useful insights into the thousands of uncultivated microbial communities for which only marker gene surveys are currently available.
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              Energy contributions of volatile fatty acids from the gastrointestinal tract in various species.

              E BERGMAN (1990)
              The VFA, also known as short-chain fatty acids, are produced in the gastrointestinal tract by microbial fermentation of carbohydrates and endogenous substrates, such as mucus. This can be of great advantage to the animal, since no digestive enzymes exist for breaking down cellulose or other complex carbohydrates. The VFA are produced in the largest amounts in herbivorous animal species and especially in the forestomach of ruminants. The VFA, however, also are produced in the lower digestive tract of humans and all animal species, and intestinal fermentation resembles that occurring in the rumen. The principal VFA in either the rumen or large intestine are acetate, propionate, and butyrate and are produced in a ratio varying from approximately 75:15:10 to 40:40:20. Absorption of VFA at their site of production is rapid, and large quantities are metabolized by the ruminal or large intestinal epithelium before reaching the portal blood. Most of the butyrate is converted to ketone bodies or CO2 by the epithelial cells, and nearly all of the remainder is removed by the liver. Propionate is similarly removed by the liver but is largely converted to glucose. Although species differences exist, acetate is used principally by peripheral tissues, especially fat and muscle. Considerable energy is obtained from VFA in herbivorous species, and far more research has been conducted on ruminants than on other species. Significant VFA, however, are now known to be produced in omnivorous species, such as pigs and humans. Current estimates are that VFA contribute approximately 70% to the caloric requirements of ruminants, such as sheep and cattle, approximately 10% for humans, and approximately 20-30% for several other omnivorous or herbivorous animals. The amount of fiber in the diet undoubtedly affects the amount of VFA produced, and thus the contribution of VFA to the energy needs of the body could become considerably greater as the dietary fiber increases. Pigs and some species of monkey most closely resemble humans, and current research should be directed toward examining the fermentation processes and VFA metabolism in those species. In addition to the energetic or nutritional contributions of VFA to the body, the VFA may indirectly influence cholesterol synthesis and even help regulate insulin or glucagon secretion. In addition, VFA production and absorption have a very significant effect on epithelial cell growth, blood flow, and the normal secretory and absorptive functions of the large intestine, cecum, and rumen. The absorption of VFA and sodium, for example, seem to be interdependent, and release of bicarbonate usually occurs during VFA absorption.(ABSTRACT TRUNCATED AT 400 WORDS)
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                13 July 2017
                2017
                : 8
                : 1316
                Affiliations
                [1] 1Research Group on Computational Biology and Microbial Ecology, Department of Biological Sciences, Universidad de los Andes Bogotá, Colombia
                [2] 2Max Planck Tandem Group in Computational Biology, Universidad de los Andes Bogotá, Colombia
                [3] 3Laboratorio de Ecología Molecular de Vertebrados Acuáticos, Department of Biological Sciences, Universidad de los Andes Bogotá, Colombia
                [4] 4Center for Genome Sciences and Systems Biology, Washington University School of Medicine, Saint Louis MO, United States
                [5] 5Centro de Investigaciones Microbiológicas, Department of Biological Sciences, Universidad de los Andes Bogotá, Colombia
                Author notes

                Edited by: David Berry, University of Vienna, Austria

                Reviewed by: Robert W. Thacker, Stony Brook University, United States; Federico Rey, University of Wisconsin-Madison, United States; Katherine Amato, Northwestern University, United States

                *Correspondence: Andrea Borbón-García, ad.borbon174@ 123456uniandes.edu.co

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.01316
                5507997
                28751883
                46ee3fa1-9550-4ac5-955d-64cb428ef822
                Copyright © 2017 Borbón-García, Reyes, Vives-Flórez and Caballero.

                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) or licensor 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
                : 17 March 2017
                : 29 June 2017
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 60, Pages: 13, Words: 0
                Funding
                Funded by: Facultad de Ciencias, Universidad de los Andes 10.13039/501100006071
                Award ID: P16.160322.001/02-BIO04
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                16s rdna gene,andean bears conservation,gut microbiota,host–microbiota interactions,herbivory,feeding ecology,metagenomics,tremarctos ornatus

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