Archives of Microbiology

, Volume 200, Issue 3, pp 505–515 | Cite as

Glucerabacter canisensis gen. nov., sp. nov., isolated from dog feces and its effect on the hydrolysis of plant glucosylceramide in the intestine of dogs

  • Misho Kawata
  • Ami Tsukamoto
  • Ryohei Isozaki
  • Shohei Nobukawa
  • Natsuki Kawahara
  • Shoko Akutsu
  • Masato Suzuki
  • Narito AsanumaEmail author
Original Paper


A Gram-positive, obligately anaerobic, oval-rod shaped, non-spore-forming, and non-pigmented bacterium, designated strain NATH-2371T (= JCM31739T = DSM105698T), was isolated from dog feces. Comparative 16S rRNA gene sequence analysis revealed that strain NATH-2371T belongs to Clostridium cluster XIVa, and the closest strains were Coprococcus comes ATCC 27758T (94.8% 16S rRNA gene sequence similarity) and Clostridium nexile DSM 1787T (94.0%). Strain NATH-2371T produced acetate, formate, and ethanol from glucose. Predominant cellular fatty acids are C16:0 and C16:0 DMA. On the basis of the phenotypic and genotypic differences, strain NATH-2371T represents a novel species in a new genus of the family Lachnospiraceae, for which the name Glucerabacter canisensis gen. nov., sp. nov., is proposed. This strain was found to efficiently hydrolyze plant glucosylceramide (GluCer). The abundance of strain NATH-2371T in dog feces was higher in young dogs than in old dogs. Incubation of dog fecal bacteria showed that GluCer-hydrolyzing activity decreased with the age of dogs. The cell number of strain NATH-2371T in dog feces appeared to be correlated with GluCer hydrolysis. Thus, this bacterium is likely to play a major role in GluCer hydrolysis in the dog intestine.


Ceramide Glucerabacter canisensis Glucosylceramide Intestinal bacteria Lachnospiraceae 


  1. Aida K, Kinoshita M, Sugawara T, Ono J, Miyazawa T, Ohnishi M (2004) Apoptosis inducement by plant and fungus sphingoid bases in human colon cancer cells. J Oleo Sci 53:503–510CrossRefGoogle Scholar
  2. Aida K, Kinoshita M, Tanji M, Sugawara T, Tamura M, Ono J, Ueno N, Ohnishi M (2005) Prevention of aberrant crypt foci formation by dietary maize and yeast cerebrosides in 1,2-dimethylhydrazine-treated mice. J Oleo Sci 54:45–49CrossRefGoogle Scholar
  3. Arai K, Mizoguchi Y, Tokuji Y, Aida K, Yamashita S, Ohnishi M, Kinoshita M (2015) Effects of dietary plant-origin glucosylceramide on bowel inflammation in DSS-treated mice. J Oleo Sci 64:737–742CrossRefPubMedGoogle Scholar
  4. Asanuma N, Iwamoto M, Hino T (1999) Structure and transcriptional regulation of the gene encoding pyruvate formate-lyase of a ruminal bacterium, Streptococcus bovis. Microbiology 145:151–157CrossRefPubMedGoogle Scholar
  5. Asanuma N, Iwamoto M, Yoshii T, Hino T (2004) Molecular characterization and transcriptional regulation of nitrate reductase in a ruminal bacterium, Selenomonas ruminantium. J Gen Appl Microbiol 50:55–63CrossRefPubMedGoogle Scholar
  6. Asanuma N, Kanada K, Hino T (2008) Molecular properties and transcriptional control of the phosphofructokinase and pyruvate kinase genes in a ruminal bacterium, Streptococcus bovis. Anaerobe 14:237–241CrossRefPubMedGoogle Scholar
  7. Bergey DH, Krieg NR, Holt JG (1984) Bergey’s manual of systematic bacteriology. Williams & Wilkins, BaltimoreGoogle Scholar
  8. Cuvillier O (2002) Sphingosine in apoptosis signaling. Biochim Biophys Acta 1585:153–162CrossRefPubMedGoogle Scholar
  9. Dany M, Ogretmen B (2015) Ceramide induced mitophagy and tumor suppression. Biochim Biophys Acta 1853:2834–2845CrossRefPubMedPubMedCentralGoogle Scholar
  10. Diez-Gonzalez F, Bond DR, Jennings E, Russell JB (1999) Alternative schemes of butyrate production in Butyrivibrio fibrisolvens and their relationship to acetate utilization, lactate production, and phylogeny. Arch Microbiol 171:324–330CrossRefPubMedGoogle Scholar
  11. Duan RD, Nilsson A (2009) Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development. Prog Lipid Res 48:62–72CrossRefPubMedGoogle Scholar
  12. Duan J, Sugawara T, Sakai S, Aida K, Hirata T (2011) Oral glucosylceramide reduces 2,4-dinitrofluorobenzene induced inflammatory response in mice by reducing TNF-alpha levels and leukocyte infiltration. Lipids 46:505–512CrossRefPubMedGoogle Scholar
  13. Duan J, Sugawara T, Aida K, Hirose M, Sakai S, Fujii A, Hirata T (2012) Dietary sphingolipids improve skin barrier function via up-regulation of ceramide synthases in the epidermis. Exp Dermatol 21:448–452CrossRefPubMedGoogle Scholar
  14. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638CrossRefPubMedPubMedCentralGoogle Scholar
  15. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  16. Fukuda S, Furuya H, Suzuki Y, Asanuma N, Hino T (2005) A new strain of Butyrivibrio fibrisolvens that has high ability to isomerize linoleic acid to conjugated linoleic acid. J Gen Appl Microbiol 51:105–113CrossRefPubMedGoogle Scholar
  17. Furuya H, Ide Y, Hamamoto M, Asanuma N, Hino T (2010) Isolation of a novel bacterium, Blautia glucerasei sp. nov., hydrolyzing plant glucosylceramide to ceramide. Arch Microbiol 192:365–372CrossRefPubMedGoogle Scholar
  18. Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205:31–36CrossRefPubMedGoogle Scholar
  19. Hamajima H, Matsunaga H, Fujikawa A, Sato T, Mitsutake S, Yanagita T, Nagao K, Nakayama J, Kitagaki H (2016) Japanese traditional dietary fungus koji Aspergillus oryzae functions as a prebiotic for Blautia coccoides through glycosylceramide: Japanese dietary fungus koji is a new prebiotic. SpringerPlus 5:1321–1330CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signaling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139–150CrossRefPubMedGoogle Scholar
  21. Harvald EB, Olsen ASB, Færgeman NJ (2015) Autophagy in the light of sphingolipid metabolism. Apoptosis 20:658–670CrossRefPubMedPubMedCentralGoogle Scholar
  22. Higuchi K, Kawashima M, Ichikawa Y, Imokawa G (2003) Sphingosylphosphorylcholine is a melanogenic stimulator for human melanocytes. Pigment Cell Res 16:670–678CrossRefPubMedGoogle Scholar
  23. Ideta R, Sakuta T, Nakano Y, Uchiyama T (2011) Orally administered glucosylceramide improves the skin barrier function by upregulating genes associated with the tight junction and cornified envelope formation. Biosci Biotechnol Biochem 75:1516–1523CrossRefPubMedGoogle Scholar
  24. Kawada C, Hasegawa T, Watanabe M, Nomura Y (2013) Dietary glucosylceramide enhances tight junction function in skin epidermis via induction of claudin-1. Biosci Biotechnol Biochem 77:867–869CrossRefPubMedGoogle Scholar
  25. Kinoshita M, Hori N, Aida K, Sugawara T, Ohnishi M (2007) Prevention of melanin formation by yeast cerebroside in B16 mouse melanoma cells. J Oleo Sci 56:645–648CrossRefPubMedGoogle Scholar
  26. Kinoshita M, Aida K, Tokuji Y, Sugawara T, Ohnishi M (2009) Effects of dietary plant cerebroside on gene expression in the large intestine of 1,2-dimethylhydrazine (DMH)-treated mice determined by DNA microarray analysis. J Food Lipids 16:200–208CrossRefGoogle Scholar
  27. Kurakawa T, Ogata K, Matsuda K, Tsuji H, Kubota H, Takada T, Kado Y, Asahara T, Takahashi T, Nomoto K (2015) Diversity of intestinal Clostridium coccoides group in the Japanese population, as demonstrated by reverse transcription-quantitative PCR. PLOS One 10:e0126226. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  29. Larson G, Falk P, Hoskins LC (1988) Degradation of human intestinal glycosphingolipids by extracellular glycosidases from mucin-degrading bacteria of the human fecal flora. J Biol Chem 263:10790–10798PubMedGoogle Scholar
  30. Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Zhang M, Wei H, Chen Y, Lu H, Zuo J, Su M, Qiu Y, Jia W, Xiao C, Smith LM, Yang S, Holmes E, Tang H, Zhao G, Nicholson JK, Li L, Zhao L (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci USA 105:2117–2122CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li E, Hamm CM, Gulati AS, Sartor RB, Chen H, Wu X, Zhang T, Rohlf FJ, Zhu W, Gu C, Robertson CE, Pace NR, Boedeker EC, Harpaz N, Yuan J, Weinstock GM, Sodergren E, Frank DN (2012) Inflammatory bowel diseases phenotype, C. difficile and NOD2 genotype are associated with shifts in human ileum associated microbial composition. PLOS One 7:e26284. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G + C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167CrossRefGoogle Scholar
  33. Nilsson A (1969) Metabolism of cerebroside in the intestinal tract of the rat. Biochim Biophys Acta 187:113–121CrossRefPubMedGoogle Scholar
  34. Ogimoto K, Imai S (1981) Atlas of rumen microbiology. Japan Scientific Societies Press, TokyoGoogle Scholar
  35. Ribeiro FJ, Przybylski D, Yin S, Sharpe T, Gnerre S, Abouelleil A, Berlin AM, Montmayeur A, Shea TP, Walker BJ, Young SK, Russ C, Nusbaum C, MacCallum I, Jaffe DB (2012) Finished bacterial genomes from shotgun sequence data. Genome Res 22:2270–2277CrossRefPubMedPubMedCentralGoogle Scholar
  36. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  37. Schmelz EM, Sullards MC, Dillehay DL, Merrill AH Jr (2000) Colonic cell proliferation and aberrant crypt foci formation are inhibited by dairy glycosphingolipids in 1, 2-dimethylhydrazine-treated CF1 mice. J Nutr 130:522–527CrossRefPubMedGoogle Scholar
  38. Shirakura Y, Kikuchi K, Matsumura K, Mukai K, Mitsutake S, Igarashi Y (2012) 4,8-sphingadienine and 4-hydroxy-8-sphingenine activate ceramide production in the skin. Lipids Health Dis 11:108–116CrossRefPubMedPubMedCentralGoogle Scholar
  39. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–654Google Scholar
  40. Sohpal VK, Dey A, Singh A (2010) MEGA biocentric software for sequence and phylogenetic analysis: a review. Int J Bioinform Res Appl 6:230–240CrossRefPubMedGoogle Scholar
  41. Spiegel S, Merrill AH Jr (1996) Sphingolipid metabolism and cell growth regulation. FASEB J 10:1388–1397CrossRefPubMedGoogle Scholar
  42. Stevenson DM, Weimer PJ (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75:165–174CrossRefPubMedGoogle Scholar
  43. Sugawara T, Kinoshita M, Ohnishi M, Miyazawa T (2002) Apoptosis induction by wheat-flour sphingoid bases in DLD-1 human colon cancer cells. Biosci Biotechnol Biochem 66:2228–2231CrossRefPubMedGoogle Scholar
  44. Sugawara T, Kinoshita M, Ohnishi M, Nagata J, Saito M (2003) Digestion of maize sphingolipids in rats and uptake of sphingadienine by Caco-2 cells. J Nutr 133:2777–2782CrossRefPubMedGoogle Scholar
  45. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128CrossRefGoogle Scholar
  46. Tsuji K, Mitsutake S, Ishikawa J, Takagi Y, Akiyama M, Shimizu H, Tomiyama T, Igarashi Y (2006) Dietary glucosylceramide improves skin barrier function in hairless mice. J Dermatol Sci 44:101–107CrossRefPubMedGoogle Scholar
  47. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484CrossRefPubMedGoogle Scholar
  48. Uchiyama T, Nakano Y, Ueda O, Mori H, Nakashima M, Noda A, Ishizaki C, Mizoguchi M (2008) Oral intake of glucosylceramide improves relatively higher level of transepidermal water loss in mice and healthy human subjects. J Health Sci 54:559–566CrossRefGoogle Scholar
  49. Ueda N (2015) Ceramide-induced apotosis in rental tubular cells: a role of mitochondria and sphingosine-1-phosphate. Int J Mol Sci 16:5076–5124CrossRefPubMedPubMedCentralGoogle Scholar
  50. Vesper H, Schmelz EM, Nikolova-Karakashian MN, Dillehay DL, Lynch DV, Merrill AH Jr (1999) Sphingolipids in food and the emerging importance of sphingolipids to nutrition. J Nutr 129:1239–1250CrossRefPubMedGoogle Scholar
  51. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glockner FO, Rossello-Mora R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250CrossRefPubMedGoogle Scholar
  52. Yeom M, Kim SH, Lee B, Han JJ, Chung GH, Choi HD, Lee H, Hahm DH (2012) Oral administration of glucosylceramide ameliorates inflammatory dry-skin condition in chronic oxazolone-induced irritant contact dermatitis in the mouse ear. J Dermatol Sci 67:101–110CrossRefPubMedGoogle Scholar
  53. Yunoki K, Ogawa T, Ono J, Miyashita R, Aida K, Oda Y, Ohnishi M (2008) Analysis of sphingolipid classes and their contents in meals. Biosci Biotechnol Biochem 72:222–225CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Misho Kawata
    • 1
  • Ami Tsukamoto
    • 1
  • Ryohei Isozaki
    • 1
  • Shohei Nobukawa
    • 1
  • Natsuki Kawahara
    • 1
  • Shoko Akutsu
    • 1
  • Masato Suzuki
    • 1
  • Narito Asanuma
    • 1
    Email author
  1. 1.Department of Life ScienceMeiji UniversityKawasakiJapan

Personalised recommendations