1887

Abstract

Fresh samples of intestinal contents of three wild pigs originating from the Central Bohemia region were examined for the presence of bifidobacterial strains. During the study, we isolated many fructose-6-phosphate phosphoketolase-positive, strictly anaerobic, irregular rod-shaped bacterial isolates. Three of them were preliminarily identified as representing a novel species of the genus because their 16S rRNA gene sequence similarity with the closest relatives of thermophilic bifidobacteria ( DSM 20432, DSM 20210, subsp. LMG 21689, subsp. DSM 15837) was in the range of 97.9 – 98.4 %. All three bacterial isolates had identical rRNA, , , and gene sequences. Isolate RP115 was chosen as a representative of the bacterial group and DNA G+C content (mol%) determination, biochemical tests and analyses of physiological and morphological characteristics, habitat and chemotaxonomic traits (peptidoglycan structure, cellular fatty acids and polar lipids profile) were performed. The DNA–DNA hybridization analyses of RP115 and species representing the group of thermophilic bifidobacteria revealed values in the range from 33 to 53 %. This fact, together with relatively low sequence similarities of particular phylogenetic markers among examined bacterial strains and the phenotyping and chemotaxonomy results obtained, indicated that the evaluated bacterial isolate should be classified as representing a separate taxon within the specific group of thermophilic bifidobacteria. The name (of boar) sp. nov. has been proposed for the representative strain RP115 (=CCM 8605=DSM 100238=LMG 28779).

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2017-07-01
2024-03-29
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References

  1. Turroni F, Marchesi JR, Foroni E, Gueimonde M, Shanahan F et al. Microbiomic analysis of the bifidobacterial population in the human distal gut. ISME J 2009; 3:745–751 [View Article][PubMed]
    [Google Scholar]
  2. Modesto M, Michelini S, Stefanini I, Sandri C, Spiezio C et al. Bifidobacterium lemurum sp. nov., from faeces of the ring-tailed lemur (Lemur catta). Int J Syst Evol Microbiol 2015; 65:1726–1734 [View Article][PubMed]
    [Google Scholar]
  3. Michelini S, Modesto M, Filippini G, Spiezio C, Sandri C et al. Bifidobacterium aerophilum sp. nov., Bifidobacterium avesanii sp. nov. and Bifidobacterium ramosum sp. nov.: three novel taxa from the faeces of cotton-top tamarin (Saguinus oedipus L.). Syst Appl Microbiol 2016; 39:229–236 [View Article][PubMed]
    [Google Scholar]
  4. Mikkelsen LL, Bendixen C, Jakobsen M, Jensen BB. Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl Environ Microbiol 2003; 69:654–658 [View Article][PubMed]
    [Google Scholar]
  5. Bunesova V, Vlkova E, Rada V, Killer J, Musilova S. Bifidobacteria from the gastrointestinal tract of animals: differences and similarities. Benef Microbes 2014; 5:377–388 [View Article][PubMed]
    [Google Scholar]
  6. Scardovi V, Trovatelli LD, Biavati B, Zani G. Bifidobacterium cuniculi, Bifidobacterium choerinum, Bifidobacterium boum, and Bifidobacterium pseudocatenulatum: four new species and their deoxyribonucleic acid homology relationships. Int J Syst Bacteriol 1979; 29:291–311 [View Article]
    [Google Scholar]
  7. Zhu L, Li W, Dong X. Species identification of genus Bifidobacterium based on partial HSP60 gene sequences and proposal of Bifidobacterium thermacidophilum subsp. porcinum subsp. nov. Int J Syst Evol Microbiol 2003; 53:1619–1623 [View Article][PubMed]
    [Google Scholar]
  8. Simpson PJ, Ross RP, Fitzgerald GF, Stanton C. Bifidobacterium psychraerophilum sp. nov. and Aeriscardovia aeriphila gen. nov., sp. nov., isolated from a porcine caecum. Int J Syst Evol Microbiol 2004; 54:401–406 [View Article][PubMed]
    [Google Scholar]
  9. Yanokura E, Oki K, Makino H, Modesto M, Pot B et al. Subspeciation of Bifidobacterium longum by multilocus approaches and amplified fragment length polymorphism: description of B. longum subsp. suillum subsp. nov., isolated from the faeces of piglets. Syst Appl Microbiol 2015; 38:305–314 [View Article][PubMed]
    [Google Scholar]
  10. Yaeshima T, Fujisawa T, Mitsuoka T. Bifidobacterium globosum, subjective synonym of Bifidobacterium pseudolongum, and description of Bifidobacterium pseudolongum subsp. pseudolongum comb. nov. and Bifidobacterium pseudolongum subsp. globosum comb. nov. Syst Appl Microbiol 1992; 15:380–385 [View Article]
    [Google Scholar]
  11. Simpson PJ, Stanton C, Fitzgerald GF, Ross RP. Genomic diversity and relatedness of bifidobacteria isolated from a porcine cecum. J Bacteriol 2003; 185:2571–2581 [View Article][PubMed]
    [Google Scholar]
  12. Maxwell FJ, Duncan SH, Hold G, Stewart CS. Isolation, growth on prebiotics and probiotic potential of novel bifidobacteria from pigs. Anaerobe 2004; 10:33–39 [View Article][PubMed]
    [Google Scholar]
  13. Gavini F, Delcenserie V, Kopeinig K, Pollinger S, Beerens H et al. Bifidobacterium species isolated from animal feces and from beef and pork meat. J Food Prot 2006; 69:871–877 [View Article][PubMed]
    [Google Scholar]
  14. Killer J, Mrázek J, Bunešová V, Havlík J, Koppová I et al. Pseudoscardovia suis gen. nov., sp. nov., a new member of the family Bifidobacteriaceae isolated from the digestive tract of wild pigs (Sus scrofa). Syst Appl Microbiol 2013; 36:11–16 [View Article][PubMed]
    [Google Scholar]
  15. Killer J, Havlik J, Bunesova V, Vlkova E, Benada O. Pseudoscardovia radai sp. nov., another representative of a new genus within the family Bifidobacteriaceae isolated from the digestive tract of a wild pig (Sus scrofa scrofa). Int J Syst Evol Microbiol 2014; 64:2932–2938 [View Article][PubMed]
    [Google Scholar]
  16. Lamendella R, Santo Domingo JW, Kelty C, Oerther DB. Bifidobacteria in feces and environmental waters. Appl Environ Microbiol 2008; 74:575–584 [View Article][PubMed]
    [Google Scholar]
  17. Pryde SE, Richardson AJ, Stewart CS, Flint HJ. Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl Environ Microbiol 1999; 65:5372–5377[PubMed]
    [Google Scholar]
  18. Rada V, Petr J. Enumeration of bifidobacteria in animal intestinal samples. Vet-Med Czech 2002; 47:1–4
    [Google Scholar]
  19. Tomosada Y, Villena J, Murata K, Chiba E, Shimazu T et al. Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression. PLoS One 2013; 8:e59259 [View Article][PubMed]
    [Google Scholar]
  20. Ishizuka T, Kanmani P, Kobayashi H, Miyazaki A, Soma J et al. Immunobiotic bifidobacteria strains modulate rotavirus immune response in porcine intestinal epitheliocytes via pattern recognition receptor signaling. PLoS One 2016; 11:e0152416 [View Article][PubMed]
    [Google Scholar]
  21. Abe F, Ishibashi N, Shimamura S. Effect of administration of bifidobacteria and lactic acid bacteria to newborn calves and piglets. J Dairy Sci 1995; 78:2838–2846 [View Article][PubMed]
    [Google Scholar]
  22. Lugli GA, Milani C, Turroni F, Duranti S, Ferrario C et al. Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics. Appl Environ Microbiol 2014; 80:6383–6394 [View Article][PubMed]
    [Google Scholar]
  23. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012; 62:716–721 [View Article][PubMed]
    [Google Scholar]
  24. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  25. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kämpfer P et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 2002; 52:1043–1047 [View Article][PubMed]
    [Google Scholar]
  26. Rosselló-Mora R, Amann R. The species concept for prokaryotes. FEMS Microbiol Rev 2001; 25:39–67 [View Article][PubMed]
    [Google Scholar]
  27. Mattarelli P, Holzapfel W, Franz CM, Endo A, Felis GE et al. Recommended minimal standards for description of new taxa of the genera Bifidobacterium, Lactobacillus and related genera. Int J Syst Evol Microbiol 2014; 64:1434–1451 [View Article][PubMed]
    [Google Scholar]
  28. Gevers D, Huys G, Swings J. Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 2001; 205:31–36 [View Article][PubMed]
    [Google Scholar]
  29. Goris J, Suzuki KI, Vos PD, Nakase T, Kersters K. Evaluation of a microplate DNA–DNA hybridization method compared with the initial renaturation method. Can J Microbiol 1998; 44:1148–1153 [View Article]
    [Google Scholar]
  30. Cleenwerck I, Vandemeulebroecke K, Janssens D, Swings J. Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 2002; 52:1551–1558 [View Article][PubMed]
    [Google Scholar]
  31. Ezaki T, Hashimoto Y, Yabuuchi E. Fluorometric deoxyribonucleic acid–deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 1989; 39:224–229 [View Article]
    [Google Scholar]
  32. de Ley J. Reexamination of the association between melting point, buoyant density, and chemical base composition of deoxyribonucleic acid. J Bacteriol 1970; 101:738–754[PubMed]
    [Google Scholar]
  33. McConaughy BL, Laird CD, Mccarthy BJ. Nucleic acid reassociation in formamide. Biochemistry 1969; 8:3289–3295 [View Article][PubMed]
    [Google Scholar]
  34. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article][PubMed]
    [Google Scholar]
  35. von Ah U, Mozzetti V, Lacroix C, Kheadr EE, Fliss I et al. Classification of a moderately oxygen-tolerant isolate from baby faeces as Bifidobacterium thermophilum . BMC Microbiol 2007; 7:79 [View Article][PubMed]
    [Google Scholar]
  36. Killer J, Sedláček I, Rada V, Havlík J, Kopečný J. Reclassification of Bifidobacterium stercoris Kim et al. 2010 as a later heterotypic synonym of Bifidobacterium adolescentis . Int J Syst Evol Microbiol 2013; 63:4350–4353 [View Article][PubMed]
    [Google Scholar]
  37. Ventura M, Canchaya C, del Casale A, Dellaglio F, Neviani E et al. Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 2006; 56:2783–2792 [View Article][PubMed]
    [Google Scholar]
  38. Delétoile A, Passet V, Aires J, Chambaud I, Butel MJ et al. Species delineation and clonal diversity in four Bifidobacterium species as revealed by multilocus sequencing. Res Microbiol 2010; 161:82–90 [View Article][PubMed]
    [Google Scholar]
  39. Leblond-Bourget N, Philippe H, Mangin I, Decaris B. 16S rRNA and 16S to 23S internal transcribed spacer sequence analyses reveal inter- and intraspecific Bifidobacterium phylogeny. Int J Syst Bacteriol 1996; 46:102–111 [View Article][PubMed]
    [Google Scholar]
  40. Killer J, Rocková Š, Vlková E, Rada V, Havlík J et al. Alloscardovia macacae sp. nov., isolated from the milk of a macaque (Macaca mulatta), emended description of the genus Alloscardovia and proposal of Alloscardovia criceti comb. nov. Int J Syst Evol Microbiol 2013; 63:4439–4446 [View Article][PubMed]
    [Google Scholar]
  41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  42. Biavati B, Mattarelli P. Genus Bifidobacterium . In Whitman W, Goodfellow M, Kämpfer P, Busse HJ, Trujillo M. (editors) Bergey´s Manual of Systematic Bacteriology, 2nd ed. vol. 5 New York: Springer; 2012 pp. 172–179
    [Google Scholar]
  43. Bunesova V, Vlkova E, Rada V, Killer J, Kmet V. Identification of bifidobacteria isolated from Asian elephant (Elephas maximus). J Biosci 2013; 38:239–243 [View Article][PubMed]
    [Google Scholar]
  44. Killer J, Kopečný J, Mrázek J, Havlík J, Koppová I et al. Bombiscardovia coagulans gen. nov., sp. nov., a new member of the family Bifidobacteriaceae isolated from the digestive tract of bumblebees. Syst Appl Microbiol 2010; 33:359–366 [View Article][PubMed]
    [Google Scholar]
  45. Mitsuoka T. Vergleichende Untersuchungen über die Bifidobakterien aus dem Berdauungstrakt von Menschen und Tieren. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt I Orig 1969; 210:52–64
    [Google Scholar]
  46. Delcenserie V, Gavini F, Beerens H, Tresse O, Franssen C et al. Description of a new species, Bifidobacterium crudilactis sp. nov., isolated from raw milk and raw milk cheeses. Syst Appl Microbiol 2007; 30:381–389 [View Article][PubMed]
    [Google Scholar]
  47. Killer J, Kopecný J, Mrázek J, Rada V, Benada O et al. Bifidobacterium bombi sp. nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol 2009; 59:2020–2024 [View Article][PubMed]
    [Google Scholar]
  48. Killer J, Kopečný J, Mrázek J, Koppová I, Havlík J et al. Bifidobacterium actinocoloniiforme sp. nov. and Bifidobacterium bohemicum sp. nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol 2011; 61:1315–1321 [View Article][PubMed]
    [Google Scholar]
  49. Praet J, Meeus I, Cnockaert M, Aerts M, Smagghe G et al. Bifidobacterium commune sp. nov. isolated from the bumble bee gut. Antonie van Leeuwenhoek 2015; 107:1307–1313 [View Article][PubMed]
    [Google Scholar]
  50. Laureys D, Cnockaert M, de Vuyst L, Vandamme P. Bifidobacterium aquikefiri sp. nov., isolated from water kefir. Int J Syst Evol Microbiol 2016; 66:1281–1286 [View Article][PubMed]
    [Google Scholar]
  51. Michelini S, Oki K, Yanokura E, Shimakawa Y, Modesto M et al. Bifidobacterium myosotis sp. nov., Bifidobacterium tissieri sp. nov. and Bifidobacterium hapali sp. nov., isolated from faeces of baby common marmosets (Callithrix jacchus L.). Int J Syst Evol Microbiol 2016; 66:255–265 [View Article][PubMed]
    [Google Scholar]
  52. Tsuchida S, Takahashi S, Nguema PP, Fujita S, Kitahara M et al. Bifidobacterium moukalabense sp. nov., isolated from the faeces of wild west lowland gorilla (Gorilla gorilla gorilla). Int J Syst Evol Microbiol 2014; 64:449–455 [View Article][PubMed]
    [Google Scholar]
  53. Choi JH, Lee KM, Lee MK, Cha CJ, Kim GB. Bifidobacterium faecale sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 2014; 64:3134–3139 [View Article][PubMed]
    [Google Scholar]
  54. Morita H, Nakano A, Onoda H, Toh H, Oshima K et al. Bifidobacterium kashiwanohense sp. nov., isolated from healthy infant faeces. Int J Syst Evol Microbiol 2011; 61:2610–2615 [View Article][PubMed]
    [Google Scholar]
  55. Downes J, Mantzourani M, Beighton D, Hooper S, Wilson MJ et al. Scardovia wiggsiae sp. nov., isolated from the human oral cavity and clinical material, and emended descriptions of the genus Scardovia and Scardovia inopinata. Int J Syst Evol Microbiol 2011; 61:25–29 [View Article][PubMed]
    [Google Scholar]
  56. García-Aljaro C, Ballesté E, Rosselló-Móra R, Cifuentes A, Richter M et al. Neoscardovia arbecensis gen. nov., sp. nov., isolated from porcine slurries. Syst Appl Microbiol 2012; 35:374–379 [View Article][PubMed]
    [Google Scholar]
  57. Novik GI, Astapovich NI, Grzegorzewicz A, Gamian A. [Isolation and comparative analysis of glycolipid fractions in bifidobacteria]. Microbiology 2005; 74:670–677 [View Article]
    [Google Scholar]
  58. Exterkate FA, Otten BJ, Wassenberg HW, Veerkamp JH. Comparison of the phospholipid composition of Bifidobacterium and Lactobacillus strains. J Bacteriol 1971; 106:824–829[PubMed]
    [Google Scholar]
  59. Novik GI, Astapovich NI, Grzhegorzhevich A, Gamian A. [Analysis of phospholipids in bifidobacteria]. Mikrobiologiia 2006; 75:40–45 [View Article][PubMed]
    [Google Scholar]
  60. Dong X, Xin Y, Jian W, Liu X, Ling D. Bifidobacterium thermacidophilum sp. nov., isolated from an anaerobic digester. Int J Syst Evol Microbiol 2000; 50:119–125 [View Article][PubMed]
    [Google Scholar]
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