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      Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

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          Abstract

          Host ecological factors and external environmental factors are known to influence the structure of gut microbial communities, but few studies have examined the impacts of environmental changes on microbiotas in free‐ranging animals. Rapid land‐use change has the potential to shift gut microbial communities in wildlife through exposure to novel bacteria and/or by changing the availability or quality of local food resources. The consequences of such changes to host health and fitness remain unknown and may have important implications for pathogen spillover between humans and wildlife. To better understand the consequences of land‐use change on wildlife microbiotas, we analyzed long‐term dietary trends, gut microbiota composition, and innate immune function in common vampire bats ( Desmodus rotundus) in two nearby sites in Belize that vary in landscape structure. We found that vampire bats living in a small forest fragment had more homogenous diets indicative of feeding on livestock and shifts in microbiota heterogeneity, but not overall composition, compared to those living in an intact forest reserve. We also found that irrespective of sampling site, vampire bats which consumed relatively more livestock showed shifts in some core bacteria compared with vampire bats which consumed relatively less livestock. The relative abundance of some core microbiota members was associated with innate immune function, suggesting that future research should consider the role of the host microbiota in immune defense and its relationship to zoonotic infection dynamics. We suggest that subsequent homogenization of diet and habitat loss through livestock rearing in the Neotropics may lead to disruption to the microbiota that could have downstream impacts on host immunity and cross‐species pathogen transmission.

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          Most cited references55

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            The microbiome and innate immunity.

            The intestinal microbiome is a signalling hub that integrates environmental inputs, such as diet, with genetic and immune signals to affect the host's metabolism, immunity and response to infection. The haematopoietic and non-haematopoietic cells of the innate immune system are located strategically at the host-microbiome interface. These cells have the ability to sense microorganisms or their metabolic products and to translate the signals into host physiological responses and the regulation of microbial ecology. Aberrations in the communication between the innate immune system and the gut microbiota might contribute to complex diseases.
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              Microbiota regulates immune defense against respiratory tract influenza A virus infection.

              Although commensal bacteria are crucial in maintaining immune homeostasis of the intestine, the role of commensal bacteria in immune responses at other mucosal surfaces remains less clear. Here, we show that commensal microbiota composition critically regulates the generation of virus-specific CD4 and CD8 T cells and antibody responses following respiratory influenza virus infection. By using various antibiotic treatments, we found that neomycin-sensitive bacteria are associated with the induction of productive immune responses in the lung. Local or distal injection of Toll-like receptor (TLR) ligands could rescue the immune impairment in the antibiotic-treated mice. Intact microbiota provided signals leading to the expression of mRNA for pro-IL-1β and pro-IL-18 at steady state. Following influenza virus infection, inflammasome activation led to migration of dendritic cells (DCs) from the lung to the draining lymph node and T-cell priming. Our results reveal the importance of commensal microbiota in regulating immunity in the respiratory mucosa through the proper activation of inflammasomes.
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                Author and article information

                Contributors
                ingala.melissar@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                09 May 2019
                June 2019
                : 9
                : 11 ( doiID: 10.1002/ece3.2019.9.issue-11 )
                : 6508-6523
                Affiliations
                [ 1 ] Richard Gilder Graduate School American Museum of Natural History New York New York
                [ 2 ] Division of Vertebrate Zoology, Department of Mammalogy American Museum of Natural History New York New York
                [ 3 ] Odum School of Ecology University of Georgia Athens Georgia
                [ 4 ] Center for the Ecology of Infectious Disease University of Georgia Athens Georgia
                [ 5 ] Department of Biology Indiana University Bloomington Indiana
                [ 6 ] Department of Biology University of Copenhagen Copenhagen Denmark
                [ 7 ] Clinical‐Microbiomics Copenhagen Denmark
                [ 8 ] BGI Shenzhen China
                Author notes
                [*] [* ] Correspondence

                Melissa R. Ingala, Richard Gilder Graduate School at the American Museum of Natural History, 79th Street at Central Park West, New York, NY 10024.

                Email: ingala.melissar@ 123456gmail.com

                Author information
                https://orcid.org/0000-0002-9866-5646
                https://orcid.org/0000-0003-4315-8628
                Article
                ECE35228
                10.1002/ece3.5228
                6580296
                31236240
                671bd289-48ad-432b-8cdd-e29817c458f5
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 December 2018
                : 12 April 2019
                : 15 April 2019
                Page count
                Figures: 9, Tables: 2, Pages: 16, Words: 10926
                Funding
                Funded by: Explorers Club
                Award ID: Research Grant
                Funded by: American Museum of Natural History
                Award ID: Graduate Research Fellowship
                Funded by: Achievement Rewards for College Scientists Foundation
                Funded by: Danish National Science Research Council
                Funded by: Carlsbergfondet
                Funded by: National Science Foundation
                Award ID: Graduate Research Fellowship
                Funded by: ARCS Foundation
                Funded by: Sigma Xi
                Award ID: Grant-in-Aid
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece35228
                June 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.4 mode:remove_FC converted:18.06.2019

                Evolutionary Biology
                desmodus rotundus,diet homogenization,land‐use change,livestock,microbiota,resource provisioning

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