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http://dx.doi.org/10.4014/jmb.1901.01047

Intestinal Microbial Dysbiosis in Beagles Naturally Infected with Canine Parvovirus  

Park, Jun Seok (College of Veterinary Medicine, Chungnam National University)
Guevarra, Robin B. (Department of Animal Resources Science, Dankook University)
Kim, Bo-Ra (Department of Animal Resources Science, Dankook University)
Lee, Jun Hyung (Department of Animal Resources Science, Dankook University)
Lee, Sun Hee (Department of Animal Resources Science, Dankook University)
Cho, Jae Hyoung (Department of Animal Resources Science, Dankook University)
Kim, Hyeri (Department of Animal Resources Science, Dankook University)
Cho, Jin Ho (Division of Food and Animal Sciences, Chungbuk National University)
Song, Minho (Division of Animal and Dairy Science, Chungnam National University)
Lee, Ju-Hoon (Department of Food Science and Biotechnology, Institute of Life Science and Resources, Kyung Hee University)
Isaacson, Richard E. (Department of Veterinary and Biomedical Sciences, University of Minnesota)
Song, Kun Ho (College of Veterinary Medicine, Chungnam National University)
Kim, Hyeun Bum (Department of Animal Resources Science, Dankook University)
Publication Information
Journal of Microbiology and Biotechnology / v.29, no.9, 2019 , pp. 1391-1400 More about this Journal
Abstract
Canine parvoviral enteritis (PVE) is an important intestinal disease of the puppies; however, the potential impact of the canine parvovirus (CPV) on the gut microbiota has not been investigated. Therefore, the aim of this study was to evaluate the gut microbial shifts in puppies naturally infected with CPV. Fecal samples were collected from healthy dogs and those diagnosed with PVE at 4, 6, 8, and 12 weeks of age. The distal gut microbiota of dogs was characterized using Illumina MiSeq sequencing of the bacterial 16S rRNA genes. The sequence data were analyzed using QIIME with an Operational Taxonomic Unit definition at a similarity cutoff of 97%. Our results showed that the CPV was associated with significant microbial dysbiosis of the intestinal microbiota. Alpha diversity and species richness and evenness in dogs with PVE decreased compared to those of healthy dogs. At the phylum level, the proportion of Proteobacteria was significantly enriched in dogs with PVE while Bacteroidetes was significantly more abundant in healthy dogs (p < 0.05). In dogs with PVE, Enterobacteriaceae was the most abundant bacterial family accounting for 36.44% of the total bacterial population compared to only 0.21% in healthy puppies. The two most abundant genera in healthy dogs were Prevotella and Lactobacillus and their abundance was significantly higher compared to that of dogs with PVE (p < 0.05). These observations suggest that disturbances of gut microbial communities were associated with PVE in young dogs. Evaluation of the roles of these bacterial groups in the pathophysiology of PVE warrants further studies.
Keywords
Gut microbiota; canine parvovirus; dogs; 16S rRNA;
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1 Vazquez-Baeza Y, Hyde ER, Suchodolski JS, Knight R. 2016. Dog and human inflammatory bowel disease rely on overlapping yet distinct dysbiosis networks. Nat. Microbiol. 1: 16177.   DOI
2 Choi S, Hwang YJ, Shin MJ, Yi H. 2017. Difference in the Gut Microbiome between Ovariectomy-Induced Obesity and Diet-Induced Obesity. J. Microbiol. Biotechnol. 27: 2228-2236.   DOI
3 Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl. Environ. Microbiol. 75: 7537-7541.   DOI
4 Kim D, Hong S, Kim YT, Ryu S, Kim HB, Lee JH. 2018. Metagenomic Approach to Identifying Foodborne Pathogens on Chinese Cabbage. J. Microbiol. Biotechnol. 28: 227-235.   DOI
5 Kim D, Hong S, Na H, Chun J, Guevarra RB, Kim YT, et al. 2018. Analysis of Microbiota in Bellflower Root, Platycodon grandiflorum, Obtained from South Korea. J. Microbiol. Biotechnol. 28: 551-560.   DOI
6 Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.   DOI
7 Parks DH, Tyson GW, Hugenholtz P, Beiko RG. 2014. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123-3124.   DOI
8 Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12(6): R60.   DOI
9 Luna LG. 1968. Manual of histologic staining methods of the Armed Forces Institute of Pathology. pp. 158-160. 3rd Edition. New York: McGraw-Hill.
10 Kim BR, Shin J, Guevarra R, Lee JH, Kim DW, Seol KH, et al. 2017. Deciphering Diversity Indices for a Better Understanding of Microbial Communities. J. Microbiol. Biotechnol. 27: 2089-2093.   DOI
11 Moon HS, Lee SA, Lee SG, Choi R, Jeoung SY, Kim D, et al. 2008. Comparison of the pathogenicity in three different Korean canine parvovirus 2 (CPV-2) isolates. Vet. Microbiol. 131: 47-56.   DOI
12 Yildiz S, Mazel-Sanchez B, Kandasamy M, Manicassamy B, Schmolke M. 2018. Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome 6(1): 9.   DOI
13 Rowan-Nash AD, Korry BJ, Mylonakis E, Belenky P. 2019. Cross-Domain and Viral Interactions in the Microbiome. Microbiol. Mol. Biol. Rev. 83(1). pii: e00044-18.
14 Guevarra RB, Lee JH, Lee SH, Seok MJ, Kim DW, Kang BN, et al. 2019. Piglet gut microbial shifts early in life: causes and effects. J. Anim. Sci. Biotechnol. 10: 1.   DOI
15 Zaneveld JR, McMinds R, Vega Thurber R. 2017. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2: 17121.   DOI
16 Sime TA, Powell LL, S childt JC, Olson EJ. 2015. Parvoviral myocarditis in a 5-week-old Dachshund. J. Vet. Emerg. Crit. Care (San Antonio) 25: 765-769.   DOI
17 Tress B, Dorn ES, Suchodolski JS, Nisar T, Ravindran P, Weber K, et al. 2017. Bacterial microbiome of the nose of healthy dogs and dogs with nasal disease. PLoS One 12: e0176736.   DOI
18 Song ES, Jung SI, Park HJ, Seo KW, Son JH, Hong S, et al. 2016. Comparison of Fecal Microbiota between German Holstein Dairy Cows with and without Left-Sided Displacement of the Abomasum. J. Clin. Microbiol. 54: 1140-1143.   DOI
19 Kim HB, Isaacson RE. 2017. Salmonella in Swine: Microbiota Interactions. Ann. Rev. Anim. Biosci. 5: 43-63.   DOI
20 Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. 2011. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol. Ecol. 76: 301-310.   DOI
21 Hooda S, Minamoto Y, Suchodolski JS, Swanson KS. 2012. Current state of knowledge: the canine gastrointestinal microbiome. Anim. Health Res. Rev. 13: 78-88.   DOI
22 Omori M, Maeda S, Igarashi H, Ohno K, Sakai K, Yonezawa T, et al. 2017. Fecal microbiome in dogs with inflammatory bowel disease and intestinal lymphoma. J. Vet. Med. Sci. 79: 1840-1847.   DOI
23 Hanshew AS, Mason CJ, Raffa KF, Currie CR. 2013. Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J. Microbiol. Methods 95: 149-155.   DOI
24 Kalenyak K, Isaiah A, Heilmann RM, Suchodolski JS, Burgener IA. 2018. Comparison of the intestinal mucosal microbiota in dogs diagnosed with idiopathic inflammatory bowel disease and dogs with food-responsive diarrhea before and after treatment. FEMS Microbiol. Ecol. 94(2). doi: 10.1093/femsec/fix173.   DOI
25 Song YG, Guevarra RB, Lee JH, Wattanaphansak S, Kang BN, Kim HB, et al. 2017. Comparative analysis of the reproductive tract microbial communities in female dogs with and without pyometra through the 16S rRNA gene pyrosequencing. Jpn. J. Vet. Res. 65: 193-200.
26 Guevarra RB, Hong SH, Cho JH, Kim BR, Shin J, Lee JH, et al. 2018. The dynamics of the piglet gut microbiome during the weaning transition in association with health and nutrition. J. Anim. Sci. Biotechnol. 9: 54.   DOI
27 Nandi S, Kumar M. 2010. Canine parvovirus: current perspective. Indian J. Virol. 21: 31-44.   DOI
28 Kilian E, Suchodolski JS, Hartmann K, Mueller RS, Wess G, Unterer S. 2018. Long-term effects of canine parvovirus infection in dogs. PLoS One 13: e0192198.   DOI
29 Kim TY, Lee JJ, Kim BS, Choi SH. 2017. Whole-Body Microbiota of Sea Cucumber (Apostichopus japonicus) from South Korea for Improved Seafood Management. J. Microbiol. Biotechnol. 27: 1753-1762.   DOI
30 Suchodolski JS, Markel ME, G arcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, et al. 2012. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One 7: e51907.   DOI
31 Suchodolski JS, Dowd SE, Wilke V, Steiner JM, Jergens AE. 2012. 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PLoS One 7: e39333.   DOI
32 Jia J, Frantz N, Khoo C, Gibson GR, Rastall RA, McCartney AL. 2010. Investigation of the faecal microbiota associated with canine chronic diarrhoea. FEMS Microbiol. Ecol. 71: 304-312.   DOI
33 Hullar MAJ, Lampe JW, Torok-Storb BJ, Harkey MA. 2018. The canine gut microbiome is associated with higher risk of gastric dilatation-volvulus and high risk genetic variants of the immune system. PLoS One 13: e0197686.   DOI
34 Petersen C, Round JL. 2014. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 16: 1024-1033.   DOI
35 Guard BC, Suchodolski JS. 2016. HORSE SPECIES SYMPOSIUM: Canine intestinal microbiology and metagenomics: From phylogeny to function. J. Anim. Sci. 94: 2247-2261.   DOI
36 Suchodolski JS, Camacho J, Steiner JM. 2008. Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiol. Ecol. 66: 567-578.   DOI
37 Heilmann RM, Guard MM, Steiner JM, Suchodolski JS, Unterer S. 2017. Fecal markers of inflammation, protein loss, and microbial changes in dogs with the acute hemorrhagic diarrhea syndrome (AHDS). J. Vet. Emerg. Crit. Care (San Antonio) 27: 586-589.   DOI
38 Cassmann E, White R, Atherly T, Wang C, Sun Y, Khoda S, et al. 2016. Alterations of the Ileal and Colonic Mucosal Microbiota in Canine Chronic Enteropathies. PLoS One 11: e0147321.   DOI
39 Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. 2015. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 26: 26191.