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      Age-related variation in the oral microbiome of urban Cooper’s hawks ( Accipiter cooperii)

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          Abstract

          Background

          Bird species worldwide are affected by trichomoniasis caused by the protist Trichomonas gallinae. In avivorous raptors such as Cooper’s hawks ( Accipiter cooperii), nestlings are more susceptible than fledglings and adults. Previous research suggested a link between oral pH and susceptibility: the oral pH of fledgling and adult hawks is more than seven times more acidic than that of nestlings. We speculated that this age-specific difference in pH would correspond to age-specific differences in the oral microbiota of Cooper’s hawks. We examined the oral microbiomes of 31 healthy, wild Cooper’s hawks in Tucson, Arizona (USA). Individuals represented three age classes (nestlings, fledglings, and adults). We designed our study with multiple controls, replicated sampling, mock communities, and stringent quality-controls to address challenges that can limit the inferential quality of microbiome data sets.

          Results

          Richness of bacterial communities in oral cavities of Cooper’s hawks differed as a function of age but not as a function of sex, sampling date, or sampling location. Bacterial communities in oral cavities of nestlings differed from those of fledglings and adults, whereas communities in fledglings and adults did not differ from each other. Communities were similar in males and females and did not differ over the sampling season. Prevalence of acid-producing bacteria in fledgling and adults vs. nestlings is consistent with previous reports of age-specific variation in oral pH, but further research is needed to establish a causal link to pH levels or susceptibility to disease. Analyses of mock communities demonstrated high repeatability and showed that operon number and read abundance were highly correlated.

          Conclusions

          The oral microbiota of wild Cooper’s hawks differs between nestlings and older birds. Variation in the oral microbiome is consistent with differences in oral pH between nestlings and older individuals. Overall our study provides a first perspective on bacterial communities associated with oral cavities of a wild raptor.

          Electronic supplementary material

          The online version of this article (10.1186/s12866-019-1413-y) contains supplementary material, which is available to authorized users.

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          Most cited references31

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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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            Dialogue between skin microbiota and immunity.

            Human skin, the body's largest organ, functions as a physical barrier to bar the entry of foreign pathogens, while concomitantly providing a home to myriad commensals. Over a human's life span, keratinized skin cells, immune cells, and microbes all interact to integrate the processes of maintaining skin's physical and immune barrier under homeostatic healthy conditions and also under multiple stresses, such as wounding or infection. In this Review, we explore the intricate interactions of microbes and immune cells on the skin surface and within associated appendages to regulate this orchestrated maturation in the context of both host physiological changes and environmental challenges. Copyright © 2014, American Association for the Advancement of Science.
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              Comparative Gut Microbiota of 59 Neotropical Bird Species

              The gut microbiota of vertebrates are essential to host health. Most non-model vertebrates, however, lack even a basic description of natural gut microbiota biodiversity. Here, we sampled 116 intestines from 59 Neotropical bird species and used the V6 region of the 16S rRNA molecule as a microbial fingerprint (average coverage per bird ~80,000 reads). A core microbiota of Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria was identified, as well as several gut-associated genera. We tested 18 categorical variables associated with each bird for significant correlation to the gut microbiota; host taxonomic categories were most frequently significant and explained the most variation. Ecological variables (e.g., diet, foraging stratum) were also frequently significant but explained less variation. Little evidence was found for a significant influence of geographic space. Finally, we suggest that microbial sampling during field collection of organisms would propel biological understanding of evolutionary history and ecological significance of host-associated microbiota.
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                Author and article information

                Contributors
                Michaeljtaylor93@gmail.com
                mannan@ag.arizona.edu
                juren@email.arizona.edu
                npgarber@email.arizona.edu
                rgallery@email.arizona.edu
                arnold@ag.arizona.edu
                Journal
                BMC Microbiol
                BMC Microbiol
                BMC Microbiology
                BioMed Central (London )
                1471-2180
                21 February 2019
                21 February 2019
                2019
                : 19
                : 47
                Affiliations
                [1 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, School of Natural Resources and the Environment, , The University of Arizona, ; Tucson, USA
                [2 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, Department of Biosystems Engineering, , The University of Arizona, ; Tucson, USA
                [3 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, School of Plant Sciences, , The University of Arizona, ; Tucson, USA
                [4 ]ISNI 0000 0001 2168 186X, GRID grid.134563.6, Department of Ecology and Evolutionary Biology, , The University of Arizona, ; Tucson, USA
                Author information
                http://orcid.org/0000-0002-7013-4026
                Article
                1413
                10.1186/s12866-019-1413-y
                6385412
                30791867
                28ccf749-0222-4e49-9fd7-817faa562bcc
                © The Author(s). 2019

                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
                : 11 June 2018
                : 7 February 2019
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Microbiology & Virology
                16s rrna,accipitridae,bacteria,porphyromonas,ph,raptors,trichomonas
                Microbiology & Virology
                16s rrna, accipitridae, bacteria, porphyromonas, ph, raptors, trichomonas

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