The Skin Microbiome in Healthy and Allergic Dogs
Publication Date
January 08, 2014
Journal
PLOS ONE
Authors
Aline Rodrigues Hoffmann, Adam P. Patterson, Alison Diesel, Sara D. Lawhon, et al
Volume
9
Issue
1
Pages
e83197
DOI
http://doi.org/10.1371/journal.pone.0083197
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0083197
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24421875
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3885435
Europe PMC
http://europepmc.org/abstract/MED/24421875
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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1342594"], "description"=>"<p>Principal coordinates analysis of unweighted Unifrac distances of 16S rRNA genes clusters samples based on similarities of bacterial molecular phylogenetic trees. (A) No clustering differences are observed in 3 healthy dogs with fleas compared to 9 healthy dogs without fleas, demonstrating that the presence of fleas does not appear to influence the microbial diversity. (B) Similarly, there were no clustering differences between male and female dogs. (C) Clustering differences were seen in the samples collected from mucosal surfaces or mucocutaneous junctions.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "coordinates"], "article_id"=>897349, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principal_coordinates_analysis_for_healthy_dogs_/897349", "title"=>"Principal coordinates analysis for healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342595"], "description"=>"<p>Alpha diversity measures at 1000 sequences per sample in the different sites of canine skin (<i>x</i> axis). The <i>y</i> axis represent the data points for the Chao1 index (species predictor estimator) (A), number of observed species (B) and Shannon diversity index (diversity index that accounts for species abundance and evenness) (C) data points (<i>y</i> axis) for each skin site. Error bars represent the standard deviations. A: Axilla; C: Conjunctiva; CP: Concave pinna, DL: Dorsal lumbar; DN: Dorsal Nose; DP: Dorsal Perianal; E: Ear; G: Groin; I: Interdigital 4&5; LP: Lip commissure; N: Nostril; PO: Periocular.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "sites"], "article_id"=>897350, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alpha_diversity_in_different_skin_sites_for_healthy_dogs_/897350", "title"=>"Alpha diversity in different skin sites for healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342598"], "description"=>"<p>Rarefaction curves of 16S rRNA gene sequences obtained from different skin sites from healthy dogs. The analysis was performed on a randomly selected subset of 1000 and 3000 sequences per sample. Haired skin shows higher Chao1 metric, more observed species, and higher Shannon index compared to the samples from mucosal surfaces, e.g. nostril and conjunctiva. Lines represent average of each skin site, whereas the error bars represent the standard deviations.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "curves", "sites"], "article_id"=>897353, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rarefaction_curves_from_different_skin_sites_from_healthy_dogs_/897353", "title"=>"Rarefaction curves from different skin sites from healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342602"], "description"=>"<p>Average of most common bacterial phyla and families identified in different sites in the skin of healthy dogs.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "phyla"], "article_id"=>897357, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_phyla_and_families_in_healthy_dogs_/897357", "title"=>"Bacterial phyla and families in healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342605"], "description"=>"<p>Principal coordinates analysis plot of unweighted Unifrac distances of 16S rRNA genes. No clustering differences are observed between allergic versus healthy dogs in the samples from the nostril, axilla, groin and interdigital skin.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "coordinates", "allergic"], "article_id"=>897360, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principal_coordinates_analysis_for_allergic_versus_healthy_dogs_/897360", "title"=>"Principal coordinates analysis for allergic versus healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342606"], "description"=>"<p>Rarefaction curve of 16S rRNA gene sequences obtained from axilla, groin, interdigital skin and nostril mucosa from allergic and healthy dogs. Lines represent average of each group, whereas the error bars represent the standard deviations. The analysis was performed on a randomly selected subset of 1000 sequences per sample.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "curves", "16s", "rrna", "allergic"], "article_id"=>897361, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rarefaction_curves_of_16S_rRNA_gene_from_allergic_versus_healthy_dogs_/897361", "title"=>"Rarefaction curves of 16S rRNA gene from allergic versus healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342607"], "description"=>"<p>Bacterial phyla and families in allergic versus healthy dogs Average of most common bacterial phyla and families identified in axilla, groin, interdigital skin and nostril in allergic and healthy dogs.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "phyla", "allergic", "dogs", "bacterial", "interdigital", "nostril"], "article_id"=>897362, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_phyla_and_families_in_allergic_versus_healthy_dogs_Average_of_most_common_bacterial_phyla_and_families_identified_in_axilla_groin_interdigital_skin_and_nostril_in_allergic_and_healthy_dogs_/897362", "title"=>"Bacterial phyla and families in allergic versus healthy dogs Average of most common bacterial phyla and families identified in axilla, groin, interdigital skin and nostril in allergic and healthy dogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342608"], "description"=>"<p>Pruritus associated with allergy, ear problems and presence of fleas were part of the clinical history of these canine patients, and not necessarily the clinical presentation at the time of sample collection. Lab: Labrador Retriver, Bos: Boston Terrier, Hee: Blue Heeler, Mix: Mixed breed, Pit: Pitbull, Ter: Terrier, Poo: Poodle, She: Shetland Sheepdog, Aus: Australian Shepherd, GR: Golden Retriever, NA: Not available, M: male, CM: castrated male, F: female, SF: spayed female, N: no, Y: yes, T: trees, G: grass, W: weeds, C: carpet, T: tile, L: leather, B: bedding, F: furniture, G: glucocorticoid, CsA: cyclosporine, ASIT: allergen-specific immunotherapy.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "allergic", "dogs", "enrolled"], "article_id"=>897363, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Physical_and_environmental_characteristics_of_healthy_and_allergic_dogs_enrolled_in_this_study_/897363", "title"=>"Physical and environmental characteristics of healthy and allergic dogs enrolled in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342609"], "description"=>"<p>R-values are shown for the healthy skin sites that showed significant differences. R- values closer zero to represent no difference between different sites, whereas values closer to 1 indicate that the most similar samples are within the same group.</p><p>Significance level p = 0.001.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "unweighted", "weighted", "unifrac"], "article_id"=>897364, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ANOSIM_analysis_of_unweighted_and_weighted_Unifrac_distances_/897364", "title"=>"ANOSIM analysis of unweighted and weighted Unifrac distances.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342610"], "description"=>"<p>Significant differences between skin sites were mainly observed when comparing mucosal surfaces with haired skin sites, e.g. conjunctiva versus axilla. The Chao 1 index estimates species richness at higher sequencing depth; the observed species represents the number of observed species in 1,000 sequences; the Shannon is a diversity index that takes into account abundance and evenness of species.</p><p>Superscripts represent sites that were significantly different when compared to the skin sites in the first column. A: Axilla; N: Nostril; CP: Concave pinna; DN: Dorsal nose; G: Groin.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "measures", "1000", "sequences", "sites"], "article_id"=>897365, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alpha_diversity_measures_at_1000_sequences_per_sample_in_the_different_sites_of_healthy_skin_/897365", "title"=>"Alpha diversity measures at 1000 sequences per sample in the different sites of healthy skin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342611"], "description"=>"<p>Significant differences between healthy versus allergic (<i>p</i><0.05).</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "nostril", "mucosa", "haired", "groin", "interdigital", "allergic"], "article_id"=>897366, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.t004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alpha_diversity_analysis_of_the_nostril_mucosa_and_haired_skin_including_axilla_groin_and_interdigital_area_of_healthy_vs_allergic_dogs_/897366", "title"=>"Alpha diversity analysis of the nostril mucosa and haired skin including axilla, groin and interdigital area of healthy vs allergic dogs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-08 04:26:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1342612", "https://ndownloader.figshare.com/files/1342613"], "description"=>"<div><p>Background</p><p>Changes in the microbial populations on the skin of animals have traditionally been evaluated using conventional microbiology techniques. The sequencing of bacterial 16S rRNA genes has revealed that the human skin is inhabited by a highly diverse and variable microbiome that had previously not been demonstrated by culture-based methods. The goals of this study were to describe the microbiome inhabiting different areas of the canine skin, and to compare the skin microbiome of healthy and allergic dogs.</p><p>Methodology/Principal Findings</p><p>DNA extracted from superficial skin swabs from healthy (n = 12) and allergic dogs (n = 6) from different regions of haired skin and mucosal surfaces were used for 454-pyrosequencing of the 16S rRNA gene. Principal coordinates analysis revealed clustering for the different skin sites across all dogs, with some mucosal sites and the perianal regions clustering separately from the haired skin sites. The rarefaction analysis revealed high individual variability between samples collected from healthy dogs and between the different skin sites. Higher species richness and microbial diversity were observed in the samples from haired skin when compared to mucosal surfaces or mucocutaneous junctions. In all examined regions, the most abundant phylum and family identified in the different regions of skin and mucosal surfaces were Proteobacteria and <i>Oxalobacteriaceae</i>. The skin of allergic dogs had lower species richness when compared to the healthy dogs. The allergic dogs had lower proportions of the Betaproteobacteria <i>Ralstonia</i> spp. when compared to the healthy dogs.</p><p>Conclusions/Significance</p><p>The study demonstrates that the skin of dogs is inhabited by much more rich and diverse microbial communities than previously thought using culture-based methods. Our sequence data reveal high individual variability between samples collected from different patients. Differences in species richness was also seen between healthy and allergic dogs, with allergic dogs having lower species richness when compared to healthy dogs.</p></div>", "links"=>[], "tags"=>["Computational biology", "genomics", "Sequence analysis", "microbiology", "bacteriology", "proteomics", "sequencing", "Veterinary diseases", "Veterinary bacteriology", "Veterinary epidemiology", "Veterinary informatics", "Veterinary medicine", "Small animal care", "Veterinary microbiology", "microbiome", "allergic"], "article_id"=>897367, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Aline Rodrigues Hoffmann", "Adam P. Patterson", "Alison Diesel", "Sara D. Lawhon", "Hoai Jaclyn Ly", "Christine Elkins Stephenson", "Joanne Mansell", "Jörg M. Steiner", "Scot E. Dowd", "Thierry Olivry", "Jan S. Suchodolski"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083197.s001", "https://dx.doi.org/10.1371/journal.pone.0083197.s002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Skin_Microbiome_in_Healthy_and_Allergic_Dogs_/897367", "title"=>"The Skin Microbiome in Healthy and Allergic Dogs", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-01-08 04:26:35"}

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