Antonie van Leeuwenhoek

, Volume 86, Issue 3, pp 205–223 | Cite as

Insights into the taxonomy, genetics and physiology of bifidobacteria

  • Marco Ventura
  • Douwe van Sinderen
  • Gerald F. Fitzgerald
  • Ralf Zink
Article

Abstract

Despite the generally accepted importance of bifidobacteria as probiotic components of the human intestinal microflora and their use in health promoting foods, there is only limited information about their phylogenetic position, physiology and underlying genetics. In the last few years numerous molecular approaches have emerged for the identification and characterization of bifidobacterial strains. Their use, in conjunction with traditional culturing methods, has led to a polyphasic taxonomy which has significantly enhanced our knowledge of the role played by these bacteria in the human intestinal ecosystem. The recent adaptation of culture-independent molecular tools to the fingerprinting of intestinal and food communities offers an exciting opportunity for revealing a more detailed picture of the true complexity of these environments. Furthermore, the availability of bifidobacterial genome sequences has advanced knowledge on the genetics of bifidobacteria and the effects of their metabolic activities on the intestinal ecosystem. The release of a complete Bifidobacterium longum genome sequence and the recent initiative to sequence additional strains are expected to open up a new era of comparative genomics in bifidobacterial biology. Moreover, the use of genomotyping allows a global comparative analysis of gene content between different bifidobacterial isolates of a given species without the necessity of sequencing many strains. Genomotyping provides useful information about the degree of relatedness among various strains of Bifidobacterium species and consequently can be used in a polyphasic identification approach. This review will deal mainly with the molecular tools described for bifidobacterial identification and the first insights into the underlying genetics involved in bifidobacterial physiology as well as genome variability.

Bifidobacteria Genetics Physiology and genomotyping Taxonomy 

References

  1. Becker M.R., Paster B.J., Leys E.J.L., Moeschberger M.L., Kenyon S.G., Galvin J.L., Boches S.K., Dewhirst F.E. and Griffen A. 2002. Molecular analysis of bacterial species associated with childhood caries. J. Clinical Microbiol. 40: 1001–1009.Google Scholar
  2. Beerens H. 1991. Detection of bifidobacteria by using propionic acid as a selective agent. Appl. Environ. Microbiol. 57: 2418–2419.Google Scholar
  3. Biavati B. and Matterelli P. 1991. Bifidobacterium ruminantium sp. nov. and Bifidobacterium merycicum sp. nov. from the rumens of cattle. Int. J. Syst. Bacteriol. 41: 163–168.Google Scholar
  4. Biavati B., Mattarelli P. and Crociani F. 1991. Bifidobacterium saeculare: a new species isolated from feces of rabbit. Syst. Appl. Microbiol. 14: 389–392.Google Scholar
  5. Bourget N., Simonet J.M. and Decaris B. 1993. Analysis of the ge-nome of the five Bifidobacterium breve strains: plasmid content, pulsed field gel electrophoresis genome size estimation and rrn loci number. FEMS Microbiol. Letters 110: 11–20.Google Scholar
  6. Brigidi P., Vitali B., Swennen E., Altomare L., Rossi M. and Matteuzzi D. 2000. Specific detection of Bifidobacterium strains in a 219.pharmaceutical probiotic product and in human feces by poly-merase chain reaction. System. Appl. Microbiol. 23: 391–399.Google Scholar
  7. Chan K., Baker S., Kim C.C., Detweiler C.S., Dougan G. and Falkow S. 2003. Genomic Comparison of Salmonella enterica Serovars and Salmonella bongori by Use of an S. enterica Se-rovar Typhimurium DNA Microarray. J. Bacteriol. 185: 553–563.Google Scholar
  8. Charteris W.P., Kelly P.M. and Collins J.K. 1998. Antibiotic sus-ceptibility of potentially probiotic Bifidobacterium isolates from the human gastrointestinal tract. Lett. Appl. Microbiol. 26: 333–337.Google Scholar
  9. Clewley J.P. 2002. Genomotyping: comparative bacterial genom-ics using microarrays. Commun. Dis. Public. Health. 5: 258–290.Google Scholar
  10. Collins M.D. and Gibson G.R. 1999. Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am. J. Clin. Nutr. 69: 1052–1057.Google Scholar
  11. Dai D. and Walker W.A. 1999. Protective nutrients and bacterial colonization in the immature human gut. Adv. Pediatr. 46: 353–382.Google Scholar
  12. De Vries W. and Stouthamer A.H. 1967. Fermentation of glucose, lactose, galactose, mannitol and xylose by bifidobacteria. J. Bacteriol. 96: 472–478.Google Scholar
  13. Deguchi Y., Morishita T., and Mutai M. 1985. Comparative studies on synthesis of water-soluble vitamins among human species of bifidobacteria. Agr. Biol. Chem. 49: 13–19.Google Scholar
  14. Dobrindt U., Agerer F., Michaelis K., Janka A., Buchrieser C., Samuelson M., Svanborg C., Gottschalk G., Karch H., and Hacker J. 2003. Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J. Bacteriol. 185: 1831–40.Google Scholar
  15. Dong X., Cheng G. and Jian W. 2000. Simultaneous identification of five Bifidobacterium species isolated from human beings using multiple PCR primers. System. Appl. Microbiol. 23: 386–390.Google Scholar
  16. Ehrmann M., Ludwig W., Schleifer K.H. 1994. Reverse dot blot hybridization: a useful method for the direct identification of lactic acid bacteria in fermented food.: FEMS Microbiol Lett. 117: 143–149.Google Scholar
  17. Eisen J.A. 1995. The recA protein as a model molecule for mo-lecular systematic studies of bacteria: comparison of trees of re-cAs and 16S rRNAs from the same species. J. Mol. Evol. 41: 1105–1123.Google Scholar
  18. Fanedl L., Nekrep F.V. and Augustin G. 1998. Random amplified polymorphic DNA analysis and demonstration of genetic vari-ability among bifidobacteria isolated from rats fed with raw kidney beans. Can. J. Microbiol. 44: 1094–1101.Google Scholar
  19. Fasoli S., Marzotto M., Rizzotti L., Rossi F., Dellaglio F. and Torriani S. 2003. Bacterial composition of commercial probiotic products as evaluated by PCR-DGGE analysis. Int. J. Food. Microbiol. 82: 59–70.Google Scholar
  20. Favier C.F., de Vos W.M. and Akkermans D.L. 2003. Development of bacterial and bifidobacterial communites in feces of newborn babies. Anaerobe 9: 219–229.Google Scholar
  21. Favier C.F., Vaughan E., de Vos W.M. and Akkermans D.L. 2002. Molecular monitoring of succession of bacterial communites in human neonates. Appl. Environ. Microbiol. 68: 219–226.Google Scholar
  22. Felis G.E., Dellaglio F., Mizzi L. and Torrioni S. 2001. Comparative sequence analysis of recA gene fragment brings new evi-dence for a change in the taxonomy of the Lactobacillus casei group. Int. J. Syst. Evol. Microbiol. 51: 2113–2117.Google Scholar
  23. Fitzgerald J.R., Sturdevant D.E., Mackie S.M., Gill S.R., Musser J.M. 2001. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc. Natl. Acad. Sci. USA 98: 8821–8826.Google Scholar
  24. Franks A.H., Harmsen H.J., Raangs G.C., Jansen G.J., Schut F., Welling G.W. 1998. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Envi-ron. Microbiol. 64: 3336–45.Google Scholar
  25. Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365–378.Google Scholar
  26. Gibson G.R. and Wang X. 1994. Regulatory effects of bifidobac-teria on the growth of other colonic bacteria. J. Appl. Bacteriol. 77: 412–420.Google Scholar
  27. Gibson G.R., Beatty E.R., Wang X. and Cummings J.H. 1995. Dietary modulation of the human colonic microbiota: introduc-ing the concept of prebiotics. J. Nutr. 125: 1401–1412.Google Scholar
  28. Hassinen J.B., Durbin G.T., Tomarelli R.M. and Bernhart F.W. 1951. The minimal nutritional requirements of Lactobacillus bi-fidus. J. Bacteriol. 62: 771–777.Google Scholar
  29. Hatanaka M., Tachiki T., Kumagai H. and Tochikura T. 1987. Purification and some properties of glutamine synthetases from bi-fidobacteria. Agric. Biol. Chem. 51: 425–433.Google Scholar
  30. He F., Ouwehand A.C., Hashimoto H., Isolauri E., Benno Y. and Salminen S. 2001. Adhesion of Bifidobacterium spp. to human intestinal mucus. Microbiol. Immunol. 45: 259–262.Google Scholar
  31. Hopkins M.J., Sharp R. and Macfarlane G.T. 2001. Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. GUT 48: 198–205.Google Scholar
  32. Hopkins M.J., Sharp R. and Macfarlane G.T. 2002. Variation in human intestinal microbiota with age. Dig. Liver Dis. 34: 12–18.Google Scholar
  33. Hoskins L., Agustines M., McCkee W., Boulding E., Kriaris M. and Niedermeyer G. 1985. Mucin degradation in human ecosystem. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J. Clin. Invest. 75: 944–947.Google Scholar
  34. Hung M.N. and Lee B.H. 2002. Purification and characterization of a recombinant β-galactosidase with transgalactosylation activity from Bifidobacterium infantis HL96. Appl. Microbiol. Biotechnol. 58: 439–445.Google Scholar
  35. Hung M.N., Xia Z. and Lee B.H. 2001. Molecular and biochemical analysis of two β-galactosidases from Bifidobacterium infantis HL96. Appl. Environ. Microbiol. 67: 4256–4263.Google Scholar
  36. Iwata M. and Morishita T. 1989. The presence of plasmids in Bi-fidobacterium breve. Lett. Appl. Microbiol. 9: 165–168.Google Scholar
  37. Jian W. and Dong X. 2002. Transfer of Bifidobacterium inopina-tum and Bifidobacterium denticolens to Scardovia inopinata gen. nov., comb. nov., and Parascardovia denticolens gen. nov., comb. nov., respectively. IJSEM 52: 809–12.Google Scholar
  38. Jian W., Zhu L. and Dong X. 2001. New approach to phylogenetic analysis of the genus Bifidobacterium based on partial HSP60 gene sequences. IJSEM 51: 1633–1638.Google Scholar
  39. Kaplan H. and Hutkins R. 2000. Fermentation of fructooligosac-charides by lactic acid bacteria and bifidobacteria. Appl. Environ. Microbiol. 66: 2682–2684.Google Scholar
  40. Kaufmann P., Pfefferkorn A., Teuber M. and Meile L. 1997. Identification and quantification of Bifidobacterium species isolated from food with genus-specific 16S rRNA targeted probes by 220.colony hybridization and PCR. Appl. Environ. Microbiol. 63: 1268–1273.Google Scholar
  41. Klein G., Pack A., Bonaparte C. and Reuter G. 1998. Taxonomy and physiology of probiotic lactic acid bacteria. Int. J. Food Mi-crobiol. 41: 103–125.Google Scholar
  42. Kot E. and Bezkorovainy A. 1993. Effects of Mg2+ and Ca2+ on Fe2+ uptake by Bifidobacterium thermophilum. Int. J. Biochem. 25: 1029–33.Google Scholar
  43. Kullen M.J., Brady L.J. and O'Sullivan D.J. 1997. Evaluation of using a short region of the recA gene for rapid and sensitive speciation of dominant bifidobacteria in the human large intestine. FEMS Microbiol. Letters 154: 377–383.Google Scholar
  44. Langenduk P.S., Shut F., Jansen G.J., Raangs G.C., Kamphuis G.R., Wilkinson M.H.F. and Welling G.W. 1995. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus specific 16S rRNA targeted probes and its application in fecal samples. Appl. Environ. Microbiol. 61: 3069–3075.Google Scholar
  45. Lauer E. and Kandler O. 1983. DNA-DNA homology, murein types and enzyme patterns in the type strains of the genus Bifidobac-terium. Syst. Appl. Microbiol. 4: 42–64.Google Scholar
  46. Leblond-Bourgert N., Philippe H., Mangin I. and Decaris B. 1996. 16S rRNA and 16S to 23S internal transcribed spacer sequences analyses reveal inter and intraspecific Bifidobacterium phylogeny. Int. J. System. Bacteriol. 46: 102–111.Google Scholar
  47. Lievin V., Peiffer I., Hudault S., Rochat F., Brassart D., Neeser J.R. and Servin A.L. 2000. Bifidobacterium strains from resident in-fant human gastrointestinal microflora exert antimicrobial activity. GUT 47: 646–652.Google Scholar
  48. Lim K.S., Huh C.S. and Back Y.J. 1993. Antimicrobial susceptibil-ity of bifidobacteria. J. Dairy Sci. 76: 2168–2174.Google Scholar
  49. Ludwig W., Neumaier N., Klugbauer N., Brockmann E., Roller C., Jilg S., Reetz K., Schachtner I., Ludvigsen A., Bachleitner M., Fischer U. and Schleifer K.H. 1993. Phylogenetic relationships of bacteria based on comparative sequence analysis of elonga-tion factor Tu and ATP-synthase beta subunit genes. Antonie van Leeuwenhoek 64: 285–305.Google Scholar
  50. Ludwig W., Weizenegger M., Betzl D., Leidel E., Lenz T., Ludvigsen A., Mollenhoff D., Wenzig P. and Schleifer K.H. 1990. Complete nucleotide sequences of seven eubacterial genes cod-ing for the elongation factor Tu: functional, structural and phy-logenetic evaluations. Arch. Microbiol. 153: 241–247.Google Scholar
  51. MacConaill L.E., Butler D., O'Connell-Matherway M., Fitzerald G.E. and van Sinderen D. 2003. Identification of two component regulatory systems in Bifidobacterium infantis by functional complementation and degenerate PCR approach. Appl. Environ. Microbiol. 69: 4219–4226.Google Scholar
  52. Mahairas G.G., Sabo P.J., Hickey M.J., Singh D.C. and Stover C.K. 1996. Molecular analysis of genetic differences between Myco-bacterium bovis BCG and virulent M. bovis. J. Bacteriol. 178: 1274–1282.Google Scholar
  53. Mangin I., Bouhnick Y., Bisetti N. and Decaris B. 1999. Molecular monitoring of human intestinal Bifidobacterium strain diversity. Res. Microbiol. 150: 343–350.Google Scholar
  54. Mangin I., Bourget N., Bouhnik Y., Bisetti N., Simonet J.M. and Decaris B. 1994. Identification of Bifidobacterium strains by rRNA gene restriction patterns. Appl. Environ. Microbiol. 60: 1451–1458.Google Scholar
  55. Masco L., Ventura M., Zink R., Huys G. and Swings J. 2004. Polyphasic taxonomic analysis of Bifidobacterium animalis and Bifidobacterium lactis reveals relatedness at the subspecies level: reclassification of Bifidobacterium animalis as Bifidobacterium animalis subsp. animalis comb. nov. and Bifidobacterium lactis as Bifidobacterium animalis subsp. lactis comb. nov. Int. J. Syst. Evol. Microbiol. (in press)Google Scholar
  56. Matsuki T., Watanabe K., Fujimoto J., Miyamoto Y., Takada T., Matsumoto K., Oyaizu H. and Tanaka R. 2002. Development of 16S rRNA gene targeted groups specific primers for detection and identification of predominant bacteria in human feces. Appl. Environ. Microbiol. 68: 5445–5451.Google Scholar
  57. Matsuki T., Watanabe K., Tanaka R. and Oyaizu H. 1998. Rapid identification of human intestinal bifidobacteria by 16S rRNA targeted species and group specific primers. FEMS Microbiol. Letters 167: 113–121.Google Scholar
  58. Matsuki T., Watanabe K., Tanaka R., Fukuda M. and Oyaizu H. 1999. Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA gene targeted species specific primers. Appl. Environ. Microbiol. 65: 4506–4512.Google Scholar
  59. Matsumoto M., Tani H., Ono H., Ohishi H. and Benno Y. 2002. Adhesive property of Bifidobacterium lactis LKM512 and pre-dominant bacteria of intestinal microflora to human intestinal mucin. Current Microbiol. 44: 212–215.Google Scholar
  60. Matteuzzi D., Crociani F., Zani G. and Trovatelli L.D. 1971. Bifi-dobacterium suis n. sp.: a new species of the genus Bifidobac-terium isolated from pig feces. Z. Allg. Mikrobiol. 11: 387–395.Google Scholar
  61. McCartney A.L. and Tannock G. 1995. Ribotyping of Bifidobacterium strains using cells embedded in agarose plugs and a 16S rDNA probe. Microbial. Ecology Health and Disease 8: 79–84.Google Scholar
  62. Meile L., Rohr L.M., Geissmann T.A., Herensperger M. and Teuber M. 2001. Characterization of the D-xylulose 5 phosphate/ D-fructose 6-phosphate phosphoketolase gene (xfp) from Bifidobacterium lactis. J. Bacteriol. 183: 2929–2936.Google Scholar
  63. Meile L., Ludwig W., Reuger U., Gut C., Kaufmann P., Dasen G., Wenger S. and Teuber T. 1997. Bifidobacterium lactis sp. nov., a moderately oxygen tolerant species isolated from fermented milk. System Appl. Microbiol. 20: 57–64.Google Scholar
  64. Mikkelsen L.J., Bendixen C., Jakobsen M. and Jensen B.B. 2003. Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl. Environ. Microbiol. 69: 654–658.Google Scholar
  65. Miller L.G. and Finegold S.M. 1967. Antibacterial sensitivity of Bifidobacterium (Lactobacillus bifidus). J. Bacteriol. 93: 125–130.Google Scholar
  66. Mitsuoka T. 1969. Comparative studies on bifidobacteria isolated from the alimentary tract of man and animals (incluing descriptions of Bifidobacterium thermophilum nov. spec. and Bifidobacterium pseudolongum nov. spec.). Zentralbl Bakteriol 210: 52–64.Google Scholar
  67. Modler W.H. 1994. Bifidogenic factors, sources, metabolism and applications. Int. Dairy J. 4: 383–407.Google Scholar
  68. Moller P.L., Jorgensen F., Hansen O.C., Madsen S.M. and Stougaard P. 2001. Intra-and extracellular β-galactosidases from Bifidobacterium bifidum and B. infantis: molecular cloning, heterologous expression, and comparative characterization. Appl. Environ. Microbiol. 67: 2276–2283.Google Scholar
  69. Munoa F.J. and Pares R. 1988. Selective medium for isolation and enumeration of Bifidobacterium spp. Appl. Environ. Microbiol. 54: 1715–1718.Google Scholar
  70. Nebra Y., Bonjoch X. and Blanch A. 2003. Use of Bifidobacterium dentium as an indicator of the origin of fecal water pollution. Appl. Environ. Microbiol. 69: 2651–2656.Google Scholar
  71. Nielsen D.S., Moller P.L., Rosenfeldt V., Paerregaard A., Michaelsen K.F. and Jakobsen M. 2003. Case study of the dis-tribution of mucosa-associated Bifidobacterium species, Lactobacillus species, and other lactic acid bacteria in the human colon. Appl. Environ. Microbiol. 69: 7545–7548.Google Scholar
  72. Nunes L.R., Rosato Y.B., Muto N.H., Yanai G.M., da Silva V.S., Leite D.B., Goncalves E.R., de Souza A.A., Coletta-Filho H.D., Machado M.A., Lopes S.A., de Oliveira R.C. 2003. Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements. Genome Res. 13: 570–8.Google Scholar
  73. Parkinson J.S. 1993. Signal transduction schemes in bacteria. Cell 73: 857–871.Google Scholar
  74. Peters J.E., Thate T.E. and Craig N.L. 2003. Definition of the Es-cherichia coli MC4100 Genome by Use of a DNA Array. J. Bacteriol. 185: 2017–2021.Google Scholar
  75. Requena T., Burton J., Matsuki T., Munro K., Simon M.A., Tanaka R., Watamabe K. and Tannock G.W. 2002. Identification, detection, and enumeration of human Bifidobacterium species by PCR targeting the transaldolase gene. Appl. Environ. Microbiol. 68: 2420–2427.Google Scholar
  76. Rezzonico E., Ventura M., Cuanoud G., Pessi G., Giliberti G. and Arigoni F. 2003. DNA-array based analysis of genome variation and gene expression in bifidobacteria. Poster presentation at the Congress 'Functional genomics of Gram positive Microorganisms' Baveno. ItalyGoogle Scholar
  77. Rodtong S. and Tannock G.W. 1993. Differentiation of Lactobacillus strains by ribotyping. Appl. Env. Microbiol. 59: 3480–3484.Google Scholar
  78. Rossi M., Altomare L., Vara y Rodrigez A.G., Brigidi P. and Matteuzzi D. 2000. Nucleotide sequenze, expression and transcrip-tional analysis of the Bifidobacterium longum MB 219 lacZ gene. Arch. Microbiol. 174: 74–80.Google Scholar
  79. Roy D. and Sirois S. 2000. Molecular differentiation of Bifidobac-terium species with amplified ribosomal DNA restriction analy-sis and alignment of short regions of the ldh gene. FEMS Microbiol. Letters 191: 17–24.Google Scholar
  80. Roy D., Ward P. and Champagne G. 1996. Differentiation of bifi-dobacteria by use of pulsed field gel electrophoresis and poly-merase chain reaction. Int. J. food. Microbiol. 29: 11–29.Google Scholar
  81. Saier M.H. and Reizer J. 1992. Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoe-nolpyruvate: sugar phosphotransferase systems. J. Bacteriol. 174: 1433–1438.Google Scholar
  82. Sakamoto M., Hayashi H. and Benno Y. 2003. Terminal restriction fragment length polymorphism analysis for human fecal micro-biota and its application for analysis of complex bifidobacterial communities. Microbiol. Immunol. 47: 133–142.Google Scholar
  83. Sakata S., Kitahara M., Sakamoto M., Hayashi H., Fukuyama M. and Benno Y. 2002. Unification of Bifidobacterium infantis and Bifidobacterium suis as Bifidobacterium longum. Int. J. Syst. Evol. Microbiol. 52: 1945–1951.Google Scholar
  84. Satokari R.M., Vaughan E.E., Akkermans A.D.L., Saarela M. and De Vos W.M. 2001. Bifidobacterial diversity in human feces de-tected by genus specific PCR and denaturing gradient gel elec-trophoresis. Appl. Environ. Microbiol. 67: 504–513.Google Scholar
  85. Satokari R.M., Vaughan E.E., Akkermans A.D.L., Saarela M. and De Vos W.M. 2001. Polymerase chain reaction and denaturing gradient gel electrophoresis monitoring of fecal Bifidobacterium populations in a prebiotic and probiotic feeding trial. System. Appl. Microbiol. 24: 227–231.Google Scholar
  86. Scardovi V. and Trovatelli L.D. 1965. The fructose-6-phospate Shunt as peculiar pattern of hexose degradation in the genus Bi-fidobacterium. Ann. Micr. 15: 19–29.Google Scholar
  87. Scardovi V. and Trovatelli L.D. 1974. Bifidobacterium animalis (Mitsuoka) comb. nov. and the 'minimum' and 'subtile' groups of new bifidobacteria found in sewage. Int. J. Syst. Bacteriol. 24: 21–28.Google Scholar
  88. Scardovi V. and Crociati F. 1974. Bifidobacterium catenulatum, Bifidobacterium dentium and Bifidobacterium angulatum: three new species and their deoxyribonucleic acid homology relationships. Int. J. Syst. Bacteriol. 24: 6–20.Google Scholar
  89. Scardovi V. 1984. Genus Bifidobacterium Orla-Jensen, 1924, 472, p. 1418-1434.. In: Krieg N.R. and Holt J.G. (eds), Bergey's manual of systematic bacteriology, Vol. 1. Williams and Wilkins, Baltimore, Md, USA.Google Scholar
  90. Schell M.A., Karmirantzou M., Snel B., Vilanova D., Pessi G., Zwahlen M.C., Desiere F., Bork P., Delley M. and Aigoni G. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA. 99: 14422–14427.Google Scholar
  91. Sghir A., Gramet G., Suau A., Rochet V., Pochart P. and Dore J. 2000. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl. Environ. Microbiol. 66: 2263–2266.Google Scholar
  92. Sgorbati B., Scardovi V. and LeBlanc D.J. 1982. Plasmids in the genus Bifidobacterium. J. Gen. Microbiol. 128: 2121–2131.Google Scholar
  93. Shimamura S., Abe F., Ishinashi N., Miyakawa H., Yaeshima T., Araya T. and Tomita M. 1992. Relationship between oxygen sensitivity and oxygen metabolism of Bifidobacterium species. J. Dairy Sci. 7: 3296–3306.Google Scholar
  94. Shuhaimi M., Ali A.M., Saleh N.M. and Yazid A.M. 2001. Utilisation of enterobacterial repetitive intergenic consensus (ERIC) sequence-based PCR to fingerprint the genomes of Bifidobacterium isolates and other probiotic bacteria. Biothech. Letters 23: 731–736.Google Scholar
  95. Simpson P.J., Stanton C., Fitzgerald G.F. and Ross R.P. 2003. Genomic diversity and relatedness of bifidobacteria isolated from a porcine cecum. J. Bacteriol. 185: 2571–2581.Google Scholar
  96. Smoot J.C., Barbian K.D., Van Gompel J.J., Smoot L.M., Chaussee M.S., Sylva G.L., Sturdevant D.E., Ricklefs S.M., Porcella S.F., Parkins L.D., Beres S.B., Campbell D.S., Smith T.M., Zhang Q., Kapur V., Daly J.A., Veasy L.G., Musser J.M. 2002. Genome sequence and comparative microarray analysis of sero-type M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc. Natl. Acad. Sci. USA 99: 4668–73.Google Scholar
  97. Stackebrandt E. and Ludwig W. 1994. The importance of choosing outgroups references organisms in phylogenetic studies: the Atopobium case. Syst. Appl. Microbiol. 17: 39–43.Google Scholar
  98. Stark P.L. and Lee A. 1982. The microbial ecology of the large bowel of breast-fed and formula fed infants during the first year of life. J. Med. Microbiol. 15: 189–203.Google Scholar
  99. Tamura Z. 1983. Nutriology of bifidobacteria. Bifidobacteria Microflora 2: 3–16.Google Scholar
  100. Tanaka H., Hashiba H., Kok J. and Mierau I. 2000. Bile salt hy-drolase of Bifidobacterium longum-biochemical and genetic characterization. Appl. Environ. Microbiol. 66: 2502–2512.Google Scholar
  101. Tissier H. 1900. Recherchers sur la flora intestinale normale et pathologique du nourisson. Thesis, University of Paris, Paris, France.Google Scholar
  102. Trindade M.I., Abratt V.R. and Reid S. 2003. Induction of sucrose utilization genes from Bifidobacterium lactis by sucrose and raffinose. Appl. Environ. Microbial. 69: 24–32.Google Scholar
  103. Trovatelli L.D., Crociani F., Pedinotti M. and Scardovi V. 1974. Bifidobacterium pullorum sp. nov.: a new species isolated from chicken feces and a related group of bifidobacteria isolated from rabbit feces. Arch. Microbiol. 98: 187–198.Google Scholar
  104. Van Laere K.M.J., Abee T., Schols H.A., Beldman G. and Voragen A.G.J. 2000. Characterization of a novel β-galactosidase from Bifidobacterium adolescentis DSM 20083 active towards transgalactooligosaccharides. Appl. Environ. Microbiol. 66: 1379–1384.Google Scholar
  105. Vandamme P., Pot B., Gillis M., de Vos P., Kersters K. and Swings J. 1996. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev. 60: 407–38.Google Scholar
  106. Venema K. and Maathuis A.J.H. 2003. A PCR based method for identification of bifidobacteria from the human alimentary tract at the species level. FEMS Microbiol. Letters 224: 143–149.Google Scholar
  107. Ventura M., Canchaya C., van Sinderen D., Fitzgerald G.F. and Zink R. 2004. Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon, its genetic structure, characterization and phylogenic analysis. Appl. Environ. Microbiol. (in press)Google Scholar
  108. Ventura M. and Zink R. 2003c. Comparative sequence analysis of the tuf and recA genes, as well as RFLP of the ITS-sequences supplies additional tools to discriminate Bifidobacterium lactis from Bifidobacterium animalis. Appl. Environ. Microbiol. 69: 7517–7522.Google Scholar
  109. Ventura M., Canchaya C., Meylan V., Klaenhammer T.R. and Zink R. 2003b. Analysis, characterization and loci of the tuf genes in Lactobacillus and Bifidobacterium and their direct application for species identification. Appl Environ. Microbiol. 69: 6908–22.Google Scholar
  110. Ventura M., Elli M., Remiero R. and Zink R. 2001a. Molecular microbial analysis of Bifidobacterium isolates from different en-vironments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA). FEMS Microbiol. Ecology. 36: 113–121.Google Scholar
  111. Ventura M., Meylan V. and Zink R. 2003a. Identification and trac-ing of Bifidobacterium species by Enterobacterial Repetitive In-tergenic Consensus (ERIC) sequences. Appl. Environ. Microbiol. 69: 4296–4301.Google Scholar
  112. Ventura M., Reniero R. and Zink R. 2001b. Specific identification and targeted characterization of Bifidobacterium lactis from dif-ferent environmental isolates by a combined Multiplex.PCR approach. Appl. Environ. Microbiol. 67: 2760–2765.Google Scholar
  113. Ventura M. and Zink R. 2002. Rapid identification, differentiation, and proposed new taxonomic classification of Bifidobacterium lactis. Appl. Environ. Microbiol. 68: 6429–6434.Google Scholar
  114. Versalovic J., Koeuth T. and Lupski J.R. 1991. Distribution of re-petitive DNA sequences in eubacteria and application to finger-printing of bacterial genomes. NAR 19: 6823–6831.Google Scholar
  115. Vincent D., Roy D., Mondou F. and Dery C. 1998. Characterization of bifidobacteria by random DNAamplification. Int. J. Food. Microbiol. 43: 185–193.Google Scholar
  116. Wang R.F., Beggs M.J., Robertoson L.H. and Cerniglia C.E. 2002. Design and evaluation of oligonucleotide-microarray method for the detection of human intestinal bacteria in fecal samples. FEMS Microbiol. Letters 231: 175–182.Google Scholar
  117. Wayne L.G., Brenner D.J., Colwell R.R., Grimont P.A.D., Kandler P., Krichevsky M.I., Moore L.H., Moore W.E.C., Murray R.G.E., Stackerbrandt E., Starr M.P. and Truper H.G. 1987. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Bacteriol. 37: 463–464.Google Scholar
  118. Wolfgang M.C., Kulasekara B.R., Liang X., Boyd D., Wu K., Yang O., Miyada C.G. and Lory S. 2003. Conservation of genome content and virulence determinants among clinical and environ-mental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci. 100: 8484–8489.Google Scholar
  119. Yamamoto T., Morotomi M. and Tanaka R. 1992. Species-specific oligonucleotide probes for five Bifidobacterium species detected in human intestinal microflora. Appl. Environ. Microbiol. 58: 4076–4079.Google Scholar
  120. Yoshioka H., Iseki K. and Fugita K. 1983. Development and dif-ferences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72: 317–321.Google Scholar
  121. Yildirim Z. and Johnson M.G. 1998. Characterization and antimi-crobial spectrum of bifidocin B, a bacteriocin produced by Bifi-dobacterium bifidum NCFB 1454. J. Food Prot. 61: 47–51.Google Scholar
  122. Yildirim Z., Winters D.K. and Johnson M.G. 1999. Purification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. J. Appl. Microbiol. 86: 45–54.Google Scholar
  123. Zarate S. and Lopez-Leiva M.H. 1990. Oligosaccharide formation during enzymatic lactose hydrolysis: a literature review. J. Food Prot. 53: 262–268.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Marco Ventura
    • 1
    • 2
  • Douwe van Sinderen
    • 1
    • 3
  • Gerald F. Fitzgerald
    • 1
    • 2
    • 3
  • Ralf Zink
    • 4
  1. 1.Department of MicrobiologyNational University of CorkCorkIreland
  2. 2.National Food Biotechnology CentreNational University of CorkCorkIreland
  3. 3.Alimentary Pharmabiotic CentreNational University of CorkCorkIreland
  4. 4.Department of Nutrition & Health COGNI5DusseldorfGermany

Personalised recommendations