Individual Signatures Define Canine Skin Microbiota Composition and Variability

Dogs present almost all their skin sites covered by hair, but canine skin disorders are more common in certain skin sites and breeds. The goal of our study is to characterize the composition and variability of the skin microbiota in healthy dogs and to evaluate the effect of the breed, the skin site, and the individual. We have analyzed eight skin sites of nine healthy dogs from three different breeds by massive sequencing of 16S rRNA gene V1–V2 hypervariable regions. The main phyla inhabiting the skin microbiota in healthy dogs are Proteobacteria, Firmicutes, Fusobacteria, Actinobacteria, and Bacteroidetes. Our results suggest that skin microbiota composition pattern is individual specific, with some dogs presenting an even representation of the main phyla and other dogs with only a major phylum. The individual is the main force driving skin microbiota composition and diversity rather than the skin site or the breed. The individual is explaining 45% of the distances among samples, whereas skin site explains 19% and breed 9%. Moreover, analysis of similarities suggests a strong dissimilarity among individuals (R = 0.79, P = 0.001) that is mainly explained by low-abundant species in each dog. Skin site also plays a role: inner pinna presents the highest diversity value, whereas perianal region presents the lowest one and the most differentiated microbiota composition.

[1]  Jing Wu,et al.  The skin microbiome in allergen-induced canine atopic dermatitis. , 2016, Veterinary dermatology.

[2]  Charles W. Bradley,et al.  Longitudinal Evaluation of the Skin Microbiome and Association with Microenvironment and Treatment in Canine Atopic Dermatitis. , 2016, The Journal of investigative dermatology.

[3]  Allyson L. Byrd,et al.  Temporal Stability of the Human Skin Microbiome , 2016, Cell.

[4]  Geoffrey D. Hannigan,et al.  Skin Microbiome Surveys Are Strongly Influenced by Experimental Design. , 2016, The Journal of investigative dermatology.

[5]  Marcus J. Claesson,et al.  Comparing Apples and Oranges?: Next Generation Sequencing and Its Impact on Microbiome Analysis , 2016, PloS one.

[6]  K. Bittinger,et al.  A comparison of rumen microbial profiles in dairy cows as retrieved by 454 Roche and Ion Torrent (PGM) sequencing platforms , 2016, PeerJ.

[7]  Alison Diesel,et al.  What is living on your dog's skin? Characterization of the canine cutaneous mycobiota and fungal dysbiosis in canine allergic dermatitis , 2015, FEMS microbiology ecology.

[8]  J. Gilbert,et al.  The Influence of Age and Gender on Skin-Associated Microbial Communities in Urban and Rural Human Populations , 2015, PloS one.

[9]  M. Muto,et al.  Molecular characterization of the skin fungal microbiome in patients with psoriasis , 2015, The Journal of dermatology.

[10]  J. Steiner,et al.  Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease , 2015, Gut microbes.

[11]  Paul Turner,et al.  Reagent and laboratory contamination can critically impact sequence-based microbiome analyses , 2014, BMC Biology.

[12]  Elizabeth A. Grice,et al.  The Skin Microbiome: A Focus on Pathogens and Their Association with Skin Disease , 2014, PLoS pathogens.

[13]  Allyson L. Byrd,et al.  Biogeography and individuality shape function in the human skin metagenome , 2014, Nature.

[14]  D. Graham.  Muller and Kirk's Small Animal Dermatology , 2014 .

[15]  S. Dowd,et al.  The Skin Microbiome in Healthy and Allergic Dogs , 2014, PloS one.

[16]  F. Dewhirst,et al.  Host-associated bacterial taxa from Chlorobi, Chloroflexi, GN02, Synergistetes, SR1, TM7, and WPS-2 Phyla/candidate divisions , 2014, Journal of oral microbiology.

[17]  Ana I. Domingos,et al.  Hypothalamic melanin concentrating hormone neurons communicate the nutrient value of sugar , 2013, eLife.

[18]  Martin J Blaser,et al.  Community differentiation of the cutaneous microbiota in psoriasis , 2013, Microbiome.

[19]  Julia Oh,et al.  The altered landscape of the human skin microbiome in patients with primary immunodeficiencies , 2013, Genome research.

[20]  Jesse R. Zaneveld,et al.  Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences , 2013, Nature Biotechnology.

[21]  Se Jin Song,et al.  Cohabiting family members share microbiota with one another and with their dogs , 2013, eLife.

[22]  J. Weese,et al.  Metagenomic analysis of the canine oral cavity as revealed by high-throughput pyrosequencing of the 16S rRNA gene. , 2013, Veterinary microbiology.

[23]  J. Weese,et al.  The canine and feline skin microbiome in health and disease. , 2013, Veterinary dermatology.

[24]  H. Nakaminami,et al.  In vitro antiseptic susceptibilities for Staphylococcus pseudintermedius isolated from canine superficial pyoderma in Japan. , 2013, Veterinary dermatology.

[25]  David Elashoff,et al.  Propionibacterium acnes strain populations in the human skin microbiome associated with acne , 2013, The Journal of investigative dermatology.

[26]  C. Deming,et al.  Compartmentalized Control of Skin Immunity by Resident Commensals , 2012, Science.

[27]  Katherine H. Huang,et al.  Structure, Function and Diversity of the Healthy Human Microbiome , 2012, Nature.

[28]  Julia Oh,et al.  Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis , 2012, Genome research.

[29]  William A. Walters,et al.  Experimental and analytical tools for studying the human microbiome , 2011, Nature Reviews Genetics.

[30]  C. Huttenhower,et al.  Metagenomic biomarker discovery and explanation , 2011, Genome Biology.

[31]  B. Haas,et al.  Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. , 2011, Genome research.

[32]  K. Nelson,et al.  Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice , 2010, The ISME Journal.

[33]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[34]  B. White,et al.  Phylogenetic Characterization of Fecal Microbial Communities of Dogs Fed Diets with or without Supplemental Dietary Fiber Using 454 Pyrosequencing , 2010, PloS one.

[35]  R. Knight,et al.  Forensic identification using skin bacterial communities , 2010, Proceedings of the National Academy of Sciences.

[36]  R. Rosychuk,et al.  Breed and site predispositions of dogs with atopic dermatitis: a comparison of five locations in three continents. , 2010, Veterinary dermatology.

[37]  R. Knight,et al.  Bacterial Community Variation in Human Body Habitats Across Space and Time , 2009, Science.

[38]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[39]  Catherine André,et al.  Coat Variation in the Domestic Dog Is Governed by Variants in Three Genes , 2009, Science.

[40]  C. Deming,et al.  Topographical and Temporal Diversity of the Human Skin Microbiome , 2009, Science.

[41]  Gabriel Renaud,et al.  A diversity profile of the human skin microbiota. , 2008, Genome research.

[42]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[43]  Eoin L. Brodie,et al.  Greengenes: Chimera-checked 16S rRNA gene database and workbench compatible in ARB , 2006 .

[44]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[45]  J. Prescott,et al.  Virulence of Streptococcus canis from canine streptococcal toxic shock syndrome and necrotizing fasciitis. , 1999, Veterinary microbiology.

[46]  J. C. Reynolds,et al.  Spatial variations in the microbial community structure and diversity of the human foot is associated with the production of odorous volatiles. , 2015, FEMS microbiology ecology.

[47]  Rob Knight,et al.  Advancing our understanding of the human microbiome using QIIME. , 2013, Methods in enzymology.

[48]  M. Kanehisa,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[49]  Howard E. Evans,et al.  Miller's anatomy of the dog , 1979 .