DOI QR코드

DOI QR Code

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)
  • 투고 : 2019.01.21
  • 심사 : 2019.08.07
  • 발행 : 2019.09.28

초록

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.

키워드

참고문헌

  1. Nandi S, Kumar M. 2010. Canine parvovirus: current perspective. Indian J. Virol. 21: 31-44. https://doi.org/10.1007/s13337-010-0007-y
  2. 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. https://doi.org/10.1371/journal.pone.0192198
  3. 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. https://doi.org/10.1111/vec.12347
  4. 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. https://doi.org/10.1371/journal.pone.0176736
  5. 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. https://doi.org/10.1186/s40104-018-0308-3
  6. 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. https://doi.org/10.1128/JCM.02442-15
  7. Kim HB, Isaacson RE. 2017. Salmonella in Swine: Microbiota Interactions. Ann. Rev. Anim. Biosci. 5: 43-63. https://doi.org/10.1146/annurev-animal-022516-022834
  8. 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. https://doi.org/10.1111/j.1574-6941.2011.01058.x
  9. Hooda S, Minamoto Y, Suchodolski JS, Swanson KS. 2012. Current state of knowledge: the canine gastrointestinal microbiome. Anim. Health Res. Rev. 13: 78-88. https://doi.org/10.1017/S1466252312000059
  10. 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. https://doi.org/10.1292/jvms.17-0045
  11. 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.
  12. 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.
  13. 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. https://doi.org/10.1186/s40104-018-0269-6
  14. 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. https://doi.org/10.1016/j.mimet.2013.08.007
  15. 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. https://doi.org/10.4014/jmb.1707.07067
  16. 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. https://doi.org/10.4014/jmb.1710.10001
  17. 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. https://doi.org/10.1128/AEM.01541-09
  18. 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. https://doi.org/10.4014/jmb.1710.10021
  19. 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. https://doi.org/10.4014/jmb.1712.12031
  20. 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. https://doi.org/10.1038/nmeth.f.303
  21. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. 2014. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123-3124. https://doi.org/10.1093/bioinformatics/btu494
  22. 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. https://doi.org/10.1186/gb-2011-12-6-r60
  23. Luna LG. 1968. Manual of histologic staining methods of the Armed Forces Institute of Pathology. pp. 158-160. 3rd Edition. New York: McGraw-Hill.
  24. 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. https://doi.org/10.4014/jmb.1709.09027
  25. 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. https://doi.org/10.1016/j.vetmic.2008.02.016
  26. 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. https://doi.org/10.1186/s40168-017-0386-z
  27. 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.
  28. Zaneveld JR, McMinds R, Vega Thurber R. 2017. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol. 2: 17121. https://doi.org/10.1038/nmicrobiol.2017.121
  29. 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. https://doi.org/10.1038/nmicrobiol.2016.177
  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. https://doi.org/10.1371/journal.pone.0051907
  31. 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. https://doi.org/10.1111/j.1574-6941.2009.00812.x
  32. 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. https://doi.org/10.1371/journal.pone.0197686
  33. Petersen C, Round JL. 2014. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 16: 1024-1033. https://doi.org/10.1111/cmi.12308
  34. 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. https://doi.org/10.1371/journal.pone.0039333
  35. Guard BC, Suchodolski JS. 2016. HORSE SPECIES SYMPOSIUM: Canine intestinal microbiology and metagenomics: From phylogeny to function. J. Anim. Sci. 94: 2247-2261. https://doi.org/10.2527/jas.2015-0029
  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. https://doi.org/10.1111/j.1574-6941.2008.00521.x
  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. https://doi.org/10.1111/vec.12636
  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. https://doi.org/10.1371/journal.pone.0147321
  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.

피인용 문헌

  1. Akkermansia and Microbial Degradation of Mucus in Cats and Dogs: Implications to the Growing Worldwide Epidemic of Pet Obesity vol.7, pp.2, 2019, https://doi.org/10.3390/vetsci7020044
  2. Effects of Zinc Source and Enzyme Addition on the Fecal Microbiota of Dogs vol.12, 2019, https://doi.org/10.3389/fmicb.2021.688392
  3. Age and Giardia intestinalis Infection Impact Canine Gut Microbiota vol.9, pp.9, 2019, https://doi.org/10.3390/microorganisms9091862
  4. Dogs’ Microbiome From Tip to Toe vol.45, 2019, https://doi.org/10.1016/j.tcam.2021.100584
  5. Biomarkers of gastrointestinal functionality in dogs: A systematic review and meta-analysis vol.283, 2022, https://doi.org/10.1016/j.anifeedsci.2021.115183