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Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Differences in the gut microbiota of dogs (Canis lupus familiaris) fed a natural diet or a commercial feed revealed by the Illumina MiSeq platform

Authors: Junhyung Kim, Jae-Uk An, Woohyun Kim, Soomin Lee, Seongbeom Cho

Published in: Gut Pathogens | Issue 1/2017

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Abstract

Background

Recent advances in next-generation sequencing technologies have enabled comprehensive analysis of the gut microbiota, which is closely linked to the health of the host. Consequently, several studies have explored the factors affecting gut microbiota composition. In recent years, increasing number of dog owners are feeding their pets a natural diet i.e., one consisting of bones, raw meat (such as chicken and beef), and vegetables, instead of commercial feed. However, the effect of these diets on the microbiota of dogs (Canis lupus familiaris) is unclear.

Methods and results

Six dogs fed a natural diet and five dogs fed a commercial feed were selected; dog fecal metagenomic DNA samples were analyzed using the Illumina MiSeq platform. Pronounced differences in alpha and beta diversities, and taxonomic composition of the core gut microbiota were observed between the two groups. According to alpha diversity, the number of operational taxonomic units, the richness estimates, and diversity indices of microbiota were significantly higher (p < 0.05) in the natural diet group than in the commercial feed group. Based on beta diversity, most samples clustered together according to the diet type (p = 0.004). Additionally, the core microbiota between the two groups was different at the phylum, family, and species levels. Marked differences in the taxonomic composition of the core microbiota of the two groups were observed at the species level; Clostridium perfringens (p = 0.017) and Fusobacterium varium (p = 0.030) were more abundant in the natural diet group.

Conclusions

The gut microbiota of dogs is significantly influenced by diet type (i.e., natural diet and commercial feed). Specifically, dogs fed a natural diet have more diverse and abundant microbial composition in the gut microbiota than dogs fed a commercial feed. In addition, this study suggests that in dogs fed a natural diet, the potential risk of opportunistic infection could be higher, than in dogs fed a commercial feed. The type of diet might therefore play a key role in animal health by affecting the gut microbiota. This study could be the basis for future gut microbiota research in dogs.
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Literature
1.
go back to reference Honneffer JB, Minamoto Y, Suchodolski JS. Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs. World J Gastroenterol. 2014;20(44):16489–97.CrossRefPubMedPubMedCentral Honneffer JB, Minamoto Y, Suchodolski JS. Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs. World J Gastroenterol. 2014;20(44):16489–97.CrossRefPubMedPubMedCentral
3.
5.
go back to reference Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104(34):13780–5.CrossRefPubMedPubMedCentral Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104(34):13780–5.CrossRefPubMedPubMedCentral
6.
go back to reference Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–21.CrossRefPubMed Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–21.CrossRefPubMed
7.
go back to reference Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–8.CrossRefPubMedPubMedCentral Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–8.CrossRefPubMedPubMedCentral
8.
go back to reference David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.CrossRefPubMed David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63.CrossRefPubMed
9.
go back to reference Barker SB, Wolen AR. The benefits of human–companion animal interaction: a review. J Vet Med Educ. 2008;35(4):487–95.CrossRefPubMed Barker SB, Wolen AR. The benefits of human–companion animal interaction: a review. J Vet Med Educ. 2008;35(4):487–95.CrossRefPubMed
10.
go back to reference Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, Kachroo P, Ivanov I, Minamoto Y, Dillman EM, et al. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS ONE. 2012;7(12):e51907.CrossRefPubMedPubMedCentral Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, Kachroo P, Ivanov I, Minamoto Y, Dillman EM, et al. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS ONE. 2012;7(12):e51907.CrossRefPubMedPubMedCentral
11.
go back to reference Handl S, German AJ, Holden SL, Dowd SE, Steiner JM, Heilmann RM, Grant RW, Swanson KS, Suchodolski JS. Faecal microbiota in lean and obese dogs. FEMS Microbiol Ecol. 2013;84(2):332–43.CrossRefPubMed Handl S, German AJ, Holden SL, Dowd SE, Steiner JM, Heilmann RM, Grant RW, Swanson KS, Suchodolski JS. Faecal microbiota in lean and obese dogs. FEMS Microbiol Ecol. 2013;84(2):332–43.CrossRefPubMed
12.
go back to reference Middelbos IS, Vester Boler BM, Qu A, White BA, Swanson KS, Fahey GC Jr. Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary fiber using 454 pyrosequencing. PLoS ONE. 2010;5(3):e9768.CrossRefPubMedPubMedCentral Middelbos IS, Vester Boler BM, Qu A, White BA, Swanson KS, Fahey GC Jr. Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary fiber using 454 pyrosequencing. PLoS ONE. 2010;5(3):e9768.CrossRefPubMedPubMedCentral
13.
go back to reference Herstad KM, Gajardo K, Bakke AM, Moe L, Ludvigsen J, Rudi K, Rud I, Sekelja M, Skancke E. A diet change from dry food to beef induces reversible changes on the faecal microbiota in healthy, adult client-owned dogs. BMC Vet Res. 2017;13(1):147.CrossRefPubMedPubMedCentral Herstad KM, Gajardo K, Bakke AM, Moe L, Ludvigsen J, Rudi K, Rud I, Sekelja M, Skancke E. A diet change from dry food to beef induces reversible changes on the faecal microbiota in healthy, adult client-owned dogs. BMC Vet Res. 2017;13(1):147.CrossRefPubMedPubMedCentral
14.
go back to reference Strohmeyer RA, Morley PS, Hyatt DR, Dargatz DA, Scorza AV, Lappin MR. Evaluation of bacterial and protozoal contamination of commercially available raw meat diets for dogs. J Am Vet Med Assoc. 2006;228(4):537–42.CrossRefPubMed Strohmeyer RA, Morley PS, Hyatt DR, Dargatz DA, Scorza AV, Lappin MR. Evaluation of bacterial and protozoal contamination of commercially available raw meat diets for dogs. J Am Vet Med Assoc. 2006;228(4):537–42.CrossRefPubMed
15.
17.
go back to reference Lefebvre SL, Reid-Smith R, Boerlin P, Weese JS. Evaluation of the risks of shedding Salmonellae and other potential pathogens by therapy dogs fed raw diets in Ontario and Alberta. Zoonoses Public Health. 2008;55(8–10):470–80.CrossRefPubMed Lefebvre SL, Reid-Smith R, Boerlin P, Weese JS. Evaluation of the risks of shedding Salmonellae and other potential pathogens by therapy dogs fed raw diets in Ontario and Alberta. Zoonoses Public Health. 2008;55(8–10):470–80.CrossRefPubMed
18.
go back to reference Joffe DJ, Schlesinger DP. Preliminary assessment of the risk of Salmonella infection in dogs fed raw chicken diets. Can Vet J. 2002;43(6):441.PubMedPubMedCentral Joffe DJ, Schlesinger DP. Preliminary assessment of the risk of Salmonella infection in dogs fed raw chicken diets. Can Vet J. 2002;43(6):441.PubMedPubMedCentral
19.
go back to reference Sandri M, Dal Monego S, Conte G, Sgorlon S, Stefanon B. Raw meat based diet influences faecal microbiome and end products of fermentation in healthy dogs. BMC Vet Res. 2017;13(1):65.CrossRefPubMedPubMedCentral Sandri M, Dal Monego S, Conte G, Sgorlon S, Stefanon B. Raw meat based diet influences faecal microbiome and end products of fermentation in healthy dogs. BMC Vet Res. 2017;13(1):65.CrossRefPubMedPubMedCentral
20.
go back to reference Laflamme D. Development and validation of a body condition score system for dogs. Canine Pract. 1997;22:10–5. Laflamme D. Development and validation of a body condition score system for dogs. Canine Pract. 1997;22:10–5.
21.
go back to reference Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform. 2012;13(1):31.CrossRef Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform. 2012;13(1):31.CrossRef
23.
go back to reference Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200.CrossRefPubMedPubMedCentral Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27(16):2194–200.CrossRefPubMedPubMedCentral
24.
go back to reference Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.CrossRefPubMed Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.CrossRefPubMed
25.
go back to reference Myers EW, Miller W. Optimal alignments in linear space. Computer applications in the biosciences: CABIOS. 1988;4(1):11–7.PubMed Myers EW, Miller W. Optimal alignments in linear space. Computer applications in the biosciences: CABIOS. 1988;4(1):11–7.PubMed
26.
27.
go back to reference Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1.CrossRefPubMed Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–1.CrossRefPubMed
28.
go back to reference Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 2010;4(1):17–27.CrossRefPubMed Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 2010;4(1):17–27.CrossRefPubMed
29.
go back to reference Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4.CrossRefPubMedPubMedCentral Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6(8):1621–4.CrossRefPubMedPubMedCentral
30.
go back to reference Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112–20.CrossRefPubMedPubMedCentral Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112–20.CrossRefPubMedPubMedCentral
31.
go back to reference Derakhshani H, Tun HM, Khafipour E. An extended single-index multiplexed 16S rRNA sequencing for microbial community analysis on MiSeq illumina platforms. J Basic Microbiol. 2016;56(3):321–6.CrossRefPubMed Derakhshani H, Tun HM, Khafipour E. An extended single-index multiplexed 16S rRNA sequencing for microbial community analysis on MiSeq illumina platforms. J Basic Microbiol. 2016;56(3):321–6.CrossRefPubMed
32.
go back to reference Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genom. 2012;13:341.CrossRef Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genom. 2012;13:341.CrossRef
33.
go back to reference Salipante SJ, Kawashima T, Rosenthal C, Hoogestraat DR, Cummings LA, Sengupta DJ, Harkins TT, Cookson BT, Hoffman NG. Performance comparison of Illumina and ion torrent next-generation sequencing platforms for 16S rRNA-based bacterial community profiling. Appl Environ Microbiol. 2014;80(24):7583–91.CrossRefPubMedPubMedCentral Salipante SJ, Kawashima T, Rosenthal C, Hoogestraat DR, Cummings LA, Sengupta DJ, Harkins TT, Cookson BT, Hoffman NG. Performance comparison of Illumina and ion torrent next-generation sequencing platforms for 16S rRNA-based bacterial community profiling. Appl Environ Microbiol. 2014;80(24):7583–91.CrossRefPubMedPubMedCentral
34.
go back to reference Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67(5):1613–7.CrossRefPubMed Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol. 2017;67(5):1613–7.CrossRefPubMed
35.
go back to reference Igarashi H, Maeda S, Ohno K, Horigome A, Odamaki T, Tsujimoto H. Effect of oral administration of metronidazole or prednisolone on fecal microbiota in dogs. PLoS ONE. 2014;9(9):e107909.CrossRefPubMedPubMedCentral Igarashi H, Maeda S, Ohno K, Horigome A, Odamaki T, Tsujimoto H. Effect of oral administration of metronidazole or prednisolone on fecal microbiota in dogs. PLoS ONE. 2014;9(9):e107909.CrossRefPubMedPubMedCentral
36.
go back to reference Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4.CrossRefPubMed Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4.CrossRefPubMed
37.
go back to reference Kennedy NA, Walker AW, Berry SH, Duncan SH, Farquarson FM, Louis P, Thomson JM, Consortium UIG, Satsangi J, Flint HJ, et al. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLoS ONE. 2014;9(2):e88982.CrossRefPubMedPubMedCentral Kennedy NA, Walker AW, Berry SH, Duncan SH, Farquarson FM, Louis P, Thomson JM, Consortium UIG, Satsangi J, Flint HJ, et al. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLoS ONE. 2014;9(2):e88982.CrossRefPubMedPubMedCentral
38.
go back to reference Wagner Mackenzie B, Waite DW, Taylor MW. Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol. 2015;6:130.CrossRefPubMedPubMedCentral Wagner Mackenzie B, Waite DW, Taylor MW. Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol. 2015;6:130.CrossRefPubMedPubMedCentral
39.
go back to reference Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature. 2007;449(7164):804.CrossRefPubMedPubMedCentral Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature. 2007;449(7164):804.CrossRefPubMedPubMedCentral
40.
go back to reference Murray SM, Patil AR, Fahey GC, Merchen NR, Hughes DM. Raw and rendered animal by-products as ingredients in dog diets. J Nutr. 1998;128(12):2812S–5S.PubMed Murray SM, Patil AR, Fahey GC, Merchen NR, Hughes DM. Raw and rendered animal by-products as ingredients in dog diets. J Nutr. 1998;128(12):2812S–5S.PubMed
41.
42.
go back to reference Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA. 2002;99(2):996–1001.CrossRefPubMedPubMedCentral Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA. 2002;99(2):996–1001.CrossRefPubMedPubMedCentral
43.
go back to reference Lindström M, Heikinheimo A, Lahti P, Korkeala H. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol. 2011;28(2):192–8.CrossRefPubMed Lindström M, Heikinheimo A, Lahti P, Korkeala H. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol. 2011;28(2):192–8.CrossRefPubMed
45.
go back to reference Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, Döpfer D, Fazil A, Fischer-Walker CL, Hald T. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med. 2015;12(12):e1001921.CrossRefPubMedPubMedCentral Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, Döpfer D, Fazil A, Fischer-Walker CL, Hald T. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med. 2015;12(12):e1001921.CrossRefPubMedPubMedCentral
46.
go back to reference Potrykus J, White RL, Bearne SL. Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium. Proteomics. 2008;8(13):2691–703.CrossRefPubMed Potrykus J, White RL, Bearne SL. Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium. Proteomics. 2008;8(13):2691–703.CrossRefPubMed
47.
go back to reference Legaria M, Lumelsky G, Rodriguez V, Rosetti S. Clindamycin-resistant Fusobacterium varium bacteremia and decubitus ulcer infection. J Clin Microbiol. 2005;43(8):4293–5.CrossRefPubMedPubMedCentral Legaria M, Lumelsky G, Rodriguez V, Rosetti S. Clindamycin-resistant Fusobacterium varium bacteremia and decubitus ulcer infection. J Clin Microbiol. 2005;43(8):4293–5.CrossRefPubMedPubMedCentral
48.
go back to reference Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut. 2003;52(1):79–83.CrossRefPubMedPubMedCentral Ohkusa T, Okayasu I, Ogihara T, Morita K, Ogawa M, Sato N. Induction of experimental ulcerative colitis by Fusobacterium varium isolated from colonic mucosa of patients with ulcerative colitis. Gut. 2003;52(1):79–83.CrossRefPubMedPubMedCentral
49.
go back to reference Dong H-J, Kim W, An J-U, Kim J, Cho S. The fecal microbial communities of dairy cattle shedding shiga toxin-producing Escherichia coli or Campylobacter jejuni. Foodborne Pathog Dis. 2016;13(9):502–8.CrossRefPubMed Dong H-J, Kim W, An J-U, Kim J, Cho S. The fecal microbial communities of dairy cattle shedding shiga toxin-producing Escherichia coli or Campylobacter jejuni. Foodborne Pathog Dis. 2016;13(9):502–8.CrossRefPubMed
Metadata
Title
Differences in the gut microbiota of dogs (Canis lupus familiaris) fed a natural diet or a commercial feed revealed by the Illumina MiSeq platform
Authors
Junhyung Kim
Jae-Uk An
Woohyun Kim
Soomin Lee
Seongbeom Cho
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0218-5

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