Comparison of Gut Microbiota of 96 Healthy Dogs by Individual Traits: Breed, Age, and Body Condition Score

Simple Summary The gut microbial ecosystem is affected by various factors such as lifestyle, environment, and disease. Although gut microbiota is closely related to host health, an understanding of the gut microbiota of dogs is still lacking. Therefore, we investigated gut microbial composition in healthy dogs and divided them into groups according to their breed, age, or body condition score. From our results, age is the most crucial factor driving the gut microbial community of dogs compared to breed and body condition score (especially Fusobacterium perfoetens, which was much more abundant in the older group). We have revealed that even in healthy dogs without any diseases, there are differences in gut microbiota depending on individual traits. These results can be used as a basis for improving the quality of life by managing dogs’ gut microbiota. Abstract Since dogs are part of many peoples’ lives, research and industry related to their health and longevity are becoming a rising topic. Although gut microbiota (GM) is a key contributor to host health, limited information is available for canines. Therefore, this study characterized GM according to individual signatures (e.g., breed, age, and body condition score—BCS) of dogs living in the same environment. Fresh fecal samples from 96 healthy dogs were analyzed by sequencing the V3-V4 region of the 16S rRNA gene. The major microbial phyla were Firmicutes, Bacteroidetes, Fusobacteria, Proteobacteria, and Actinobacteria. In the comparison by breeds, relative abundance of Fusobacterium was significantly differed. Interestingly, Fusobacterium perfoetens abundance was positively correlated with age (p = 0.018), being significantly more enriched in the 6–10-year-old group (14.3%) than in the 0.5–1-year-old group (7.2%). Moreover, despite the healthy appearance of dogs in all age (0.5–10 years) and BCS (3–6) groups, the gut microbial environment may be disadvantageous in older dogs or in dogs with an abnormal BCS. These findings broaden our understanding of gut microbial ecology according to individual characteristics of dogs and may be used as a reference for providing customized-care to companion animals.

[1]  N. Bosco,et al.  The aging gut microbiome and its impact on host immunity , 2021, Genes and immunity.

[2]  J. Call,et al.  Breed differences in dog cognition associated with brain-expressed genes and neurological functions. , 2020, Integrative and comparative biology.

[3]  B. Stefanon,et al.  Gut Microbiome of Healthy and Arthritic Dogs , 2020, Veterinary sciences.

[4]  S. Gómez-Martínez,et al.  Microbiota and Lifestyle: A Special Focus on Diet , 2020, Nutrients.

[5]  E. L. Rosado,et al.  Profile of the gut microbiota of adults with obesity: a systematic review , 2020, European Journal of Clinical Nutrition.

[6]  J. Chun,et al.  Difference of gut microbiota composition based on the body condition scores in dogs , 2020, Journal of animal science and technology.

[7]  J. Jeong,et al.  Impact of breed on the fecal microbiome of dogs under the same dietary condition. , 2019, Journal of microbiology and biotechnology.

[8]  Peter D. Adams,et al.  Quantitative translation of dog-to-human aging by conserved remodeling of epigenetic networks , 2019, bioRxiv.

[9]  Paolo Manghi,et al.  The Prevotella copri Complex Comprises Four Distinct Clades Underrepresented in Westernized Populations , 2019, Cell host & microbe.

[10]  Hongyi Yang,et al.  Factors affecting the composition of the gut microbiota, and its modulation , 2019, PeerJ.

[11]  Weiqiang Huang,et al.  Oral Administration of Compound Probiotics Improved Canine Feed Intake, Weight Gain, Immunity and Intestinal Microbiota , 2019, Front. Immunol..

[12]  Edoardo Pasolli,et al.  Distinct Genetic and Functional Traits of Human Intestinal Prevotella copri Strains Are Associated with Different Habitual Diets. , 2019, Cell host & microbe.

[13]  Y. Luan,et al.  Effects of Codonopis bulleynana forest ex diels on Deferribacteres in constipation predominant intestine tumor: Differential analysis , 2018, Saudi journal of biological sciences.

[14]  J. Cryan,et al.  Targeting the gut microbiota to influence brain development and function in early life , 2018, Neuroscience & Biobehavioral Reviews.

[15]  P. Castelo,et al.  Childhood Obesity and Firmicutes/Bacteroidetes Ratio in the Gut Microbiota: A Systematic Review. , 2018, Childhood obesity.

[16]  L. Ferrucci,et al.  Commensal bacteria contribute to insulin resistance in aging by activating innate B1a cells , 2018, Science Translational Medicine.

[17]  R. Wu,et al.  Progress in characterizing the linkage between Fusobacterium nucleatum and gastrointestinal cancer , 2018, Journal of Gastroenterology.

[18]  Laurel A. Doherty,et al.  Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota , 2018, Front. Microbiol..

[19]  P. Cotter,et al.  Gut microbiota as a source of novel antimicrobials , 2018, Gut microbes.

[20]  T. Mizutani,et al.  Molecular diversity of the faecal microbiota of Toy Poodles in Japan , 2018, The Journal of veterinary medical science.

[21]  J. García-Mena,et al.  Gut microbiome production of short-chain fatty acids and obesity in children , 2018, European Journal of Clinical Microbiology & Infectious Diseases.

[22]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[23]  A. York Microbiome: Fusobacterium persistence in colorectal cancer , 2017, Nature Reviews Microbiology.

[24]  Luis Pedro Coelho,et al.  Subspecies in the global human gut microbiome , 2017, Molecular systems biology.

[25]  J. Lidbury,et al.  A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy , 2017, FEMS microbiology ecology.

[26]  Daniel J. O'Connell,et al.  Indoleacrylic Acid Produced by Commensal Peptostreptococcus Species Suppresses Inflammation. , 2017, Cell host & microbe.

[27]  G. Hansson,et al.  Bacteria Tell Us How to Protect Our Intestine. , 2017, Cell host & microbe.

[28]  C. Greenhill Obesity: Gut microbiome and serum metabolome changes , 2017, Nature Reviews Endocrinology.

[29]  B. Guard,et al.  Characterization of the fecal microbiome during neonatal and early pediatric development in puppies , 2017, PloS one.

[30]  I. Bautista-Castaño,et al.  Prevalence of Canine Obesity, Obesity-Related Metabolic Dysfunction, and Relationship with Owner Obesity in an Obesogenic Region of Spain , 2017, Front. Vet. Sci..

[31]  Rob Knight,et al.  Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson’s Disease , 2016, Cell.

[32]  N. Oezguen,et al.  GABA‐producing Bifidobacterium dentium modulates visceral sensitivity in the intestine , 2016, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[33]  R. Ley Gut microbiota in 2015: Prevotella in the gut: choose carefully , 2016, Nature Reviews Gastroenterology &Hepatology.

[34]  C. Chakraborti New-found link between microbiota and obesity. , 2015, World journal of gastrointestinal pathophysiology.

[35]  R. Gomis,et al.  Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice , 2015, Scientific Reports.

[36]  Knut Rudi,et al.  The composition of the gut microbiota throughout life, with an emphasis on early life , 2015, Microbial ecology in health and disease.

[37]  J. Steiner,et al.  Prevalence of Clostridium perfringens, Clostridium perfringens enterotoxin and dysbiosis in fecal samples of dogs with diarrhea. , 2014, Veterinary microbiology.

[38]  K. Swanson,et al.  Gut microbiota of humans, dogs and cats: current knowledge and future opportunities and challenges , 2014, British Journal of Nutrition.

[39]  E. Head,et al.  Prevention approaches in a preclinical canine model of Alzheimer’s disease: benefits and challenges , 2014, Front. Pharmacol..

[40]  M. Ebert,et al.  Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome , 2014, European Journal of Clinical Microbiology & Infectious Diseases.

[41]  L. Joseph,et al.  Obesity and C‐reactive protein in various populations: a systematic review and meta‐analysis , 2013, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[42]  John C. Wooley,et al.  Ultrafast clustering algorithms for metagenomic sequence analysis , 2012, Briefings Bioinform..

[43]  Kelly S Swanson,et al.  Current state of knowledge: the canine gastrointestinal microbiome , 2012, Animal Health Research Reviews.

[44]  H. Flint Obesity and the Gut Microbiota , 2011, Journal of clinical gastroenterology.

[45]  S. Salzberg,et al.  FLASH: fast length adjustment of short reads to improve genome assemblies , 2011, Bioinform..

[46]  D. Werling,et al.  Canine breeds at high risk of developing inflammatory bowel disease in the south-eastern UK , 2011, Veterinary Record.

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

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

[49]  A. Schwiertz,et al.  Microbiota and SCFA in Lean and Overweight Healthy Subjects , 2010, Obesity.

[50]  A. Masclee,et al.  Understanding the role of tryptophan and serotonin metabolism in gastrointestinal function , 2009, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[51]  G. Leroy,et al.  Genetic diversity of dog breeds: between-breed diversity, breed assignation and conservation approaches. , 2009, Animal genetics.

[52]  B. Roe,et al.  A core gut microbiome in obese and lean twins , 2008, Nature.

[53]  A. Pompei,et al.  Effect of a Lactobacillus animalis strain on composition and metabolism of the intestinal microflora in adult dogs. , 2007, Veterinary microbiology.

[54]  S. Holden,et al.  The WALTHAM International Nutritional Sciences Symposia A Simple , Reliable Tool for Owners to Assess the Body Condition of Their Dog or Cat 1 – 3 , 2006 .

[55]  E. Ostrander,et al.  The canine genome. , 2005, Genome research.

[56]  M. Chikindas,et al.  Mode of action of lactocin 160, a bacteriocin from vaginal Lactobacillus rhamnosus. , 2005, Infectious diseases in obstetrics and gynecology.

[57]  F. Bäckhed,et al.  Obesity alters gut microbial ecology. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Lukas Wagner,et al.  A Greedy Algorithm for Aligning DNA Sequences , 2000, J. Comput. Biol..

[59]  G. Macfarlane,et al.  Formation of Phenolic and Indolic Compounds by Anaerobic Bacteria in the Human Large Intestine , 1997, Microbial Ecology.

[60]  Philip H. Ramsey Nonparametric Statistical Methods , 1974, Technometrics.

[61]  D. Bauer Constructing Confidence Sets Using Rank Statistics , 1972 .

[62]  J. Serpell,et al.  Dog Breeds and Their Behavior , 2014 .

[63]  Elizabeth Head,et al.  The canine (dog) model of human aging and disease: dietary, environmental and immunotherapy approaches. , 2008, Journal of Alzheimer's disease : JAD.

[64]  D. Laflamme Development and validation of a body condition score system for dogs , 1997 .