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      Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging

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          Abstract

          Background

          Vultures have adapted the remarkable ability to feed on carcasses that may contain microorganisms that would be pathogenic to most other animals. The holobiont concept suggests that the genetic basis of such adaptation may not only lie within their genomes, but additionally in their associated microbes. To explore this, we generated shotgun DNA sequencing datasets of the facial skin and large intestine microbiomes of the black vulture ( Coragyps atratus) and the turkey vulture ( Cathartes aura). We characterized the functional potential and taxonomic diversity of their microbiomes, the potential pathogenic challenges confronted by vultures, and the microbial taxa and genes that could play a protective role on the facial skin and in the gut.

          Results

          We found microbial taxa and genes involved in diseases, such as dermatitis and pneumonia (more abundant on the facial skin), and gas gangrene and food poisoning (more abundant in the gut). Interestingly, we found taxa and functions with potential for playing beneficial roles, such as antilisterial bacteria in the gut, and genes for the production of antiparasitics and insecticides on the facial skin. Based on the identified phages, we suggest that phages aid in the control and possibly elimination, as in phage therapy, of microbes reported as pathogenic to a variety of species. Interestingly, we identified Adineta vaga in the gut, an invertebrate that feeds on dead bacteria and protozoans, suggesting a defensive predatory mechanism. Finally, we suggest a colonization resistance role through biofilm formation played by Fusobacteria and Clostridia in the gut.

          Conclusions

          Our results highlight the importance of complementing genomic analyses with metagenomics in order to obtain a clearer understanding of the host-microbial alliance and show the importance of microbiome-mediated health protection for adaptation to extreme diets, such as scavenging.

          Electronic supplementary material

          The online version of this article (10.1186/s13028-018-0415-3) contains supplementary material, which is available to authorized users.

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          Most cited references57

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          Microbiota-mediated colonization resistance against intestinal pathogens.

          Commensal bacteria inhabit mucosal and epidermal surfaces in mice and humans, and have effects on metabolic and immune pathways in their hosts. Recent studies indicate that the commensal microbiota can be manipulated to prevent and even to cure infections that are caused by pathogenic bacteria, particularly pathogens that are broadly resistant to antibiotics, such as vancomycin-resistant Enterococcus faecium, Gram-negative Enterobacteriaceae and Clostridium difficile. In this Review, we discuss how immune- mediated colonization resistance against antibiotic-resistant intestinal pathogens is influenced by the composition of the commensal microbiota. We also review recent advances characterizing the ability of different commensal bacterial families, genera and species to restore colonization resistance to intestinal pathogens in antibiotic-treated hosts.
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            The Universal Protein Resource (UniProt)

            The Universal Protein Resource (UniProt) provides a stable, comprehensive, freely accessible, central resource on protein sequences and functional annotation. The UniProt Consortium is a collaboration between the European Bioinformatics Institute (EBI), the Protein Information Resource (PIR) and the Swiss Institute of Bioinformatics (SIB). The core activities include manual curation of protein sequences assisted by computational analysis, sequence archiving, development of a user-friendly UniProt website, and the provision of additional value-added information through cross-references to other databases. UniProt is comprised of four major components, each optimized for different uses: the UniProt Knowledgebase, the UniProt Reference Clusters, the UniProt Archive and the UniProt Metagenomic and Environmental Sequences database. UniProt is updated and distributed every three weeks, and can be accessed online for searches or download at http://www.uniprot.org.
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              Human commensals producing a novel antibiotic impair pathogen colonization.

              The vast majority of systemic bacterial infections are caused by facultative, often antibiotic-resistant, pathogens colonizing human body surfaces. Nasal carriage of Staphylococcus aureus predisposes to invasive infection, but the mechanisms that permit or interfere with pathogen colonization are largely unknown. Whereas soil microbes are known to compete by production of antibiotics, such processes have rarely been reported for human microbiota. We show that nasal Staphylococcus lugdunensis strains produce lugdunin, a novel thiazolidine-containing cyclic peptide antibiotic that prohibits colonization by S. aureus, and a rare example of a non-ribosomally synthesized bioactive compound from human-associated bacteria. Lugdunin is bactericidal against major pathogens, effective in animal models, and not prone to causing development of resistance in S. aureus. Notably, human nasal colonization by S. lugdunensis was associated with a significantly reduced S. aureus carriage rate, suggesting that lugdunin or lugdunin-producing commensal bacteria could be valuable for preventing staphylococcal infections. Moreover, human microbiota should be considered as a source for new antibiotics.
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                Author and article information

                Contributors
                lisandracady@gmail.com
                miro@novozymes.com
                kmanzano97@gmail.com
                lhha@envs.au.dk
                brunak@bioinformatics.dtu.dk
                tgilbert@snm.ku.dk
                thomassp@snm.ku.dk
                Journal
                Acta Vet Scand
                Acta Vet. Scand
                Acta Veterinaria Scandinavica
                BioMed Central (London )
                0044-605X
                1751-0147
                11 October 2018
                11 October 2018
                2018
                : 60
                : 61
                Affiliations
                [1 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Centre for GeoGenetics, , Natural History Museum of Denmark, University of Copenhagen, ; Øster Voldgade 5-7, 1350 Copenhagen K, Denmark
                [2 ]ISNI 0000 0004 0373 0797, GRID grid.10582.3e, Department for Bioinformatics and Microbe Technology, , Novozymes A/S, ; 2880 Bagsværd, Denmark
                [3 ]ISNI 0000 0001 2159 0001, GRID grid.9486.3, Undergraduate Program on Genomic Sciences, Center for Genomic Sciences, , National Autonomous University of Mexico, ; Av. Universidad s/n Col. Chamilpa, 62210 Cuernavaca, Morelos Mexico
                [4 ]ISNI 0000 0001 1956 2722, GRID grid.7048.b, Section for Microbiology and Biotechnology, Department of Environmental Science, , Aarhus University, ; Frederiksborgvej 399, 4000 Roskilde, Denmark
                [5 ]ISNI 0000 0001 2181 8870, GRID grid.5170.3, Center for Biological Sequence Analysis, Department of Bio and Health Informatics, , Technical University of Denmark, ; Anker Engelunds Vej 1 Bygning 101A, 2800 Kgs. Lyngby, Denmark
                [6 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Novo Nordisk Foundation Center for Protein Research, Faculty of Health and Medical Sciences, , University of Copenhagen, ; Blegdamsvej 3, 2200 Copenhagen N, Denmark
                [7 ]ISNI 0000 0001 1516 2393, GRID grid.5947.f, Norwegian University of Science and Technology, University Museum, ; 7491 Trondheim, Norway
                [8 ]ISNI 0000 0004 0627 9137, GRID grid.444449.d, Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, , AIMST University, ; 08100 Bedong, Malaysia
                Author information
                http://orcid.org/0000-0002-1126-8219
                Article
                415
                10.1186/s13028-018-0415-3
                6182802
                30309375
                9611e578-796c-45bc-8655-06d591ab6ebd
                © The Author(s) 2018

                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.

                History
                : 27 April 2018
                : 3 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003554, Lundbeckfonden;
                Award ID: R52-A5062
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Veterinary medicine
                colonization resistance,diet specialization,metagenomics,microbiome,pathogens,scavenging,vulture

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