Taxonomy of Lactobacilli and Bifidobacteria.

Genera Lactobacillus and Bifidobacterium include a large number of species and strains exhibiting important properties in an applied context, especially in the area of food and probiotics. An updated list of species belonging to those two genera, their phylogenetic relationships and other relevant taxonomic information are reviewed in this paper. The conventional nature of taxonomy is explained and some basic concepts and terms will be presented for readers not familiar with this important and fast-evolving area, which importance is often underestimated. The analysis of biodiversity and its cataloguing, i.e. taxonomy, constitute the basis for applications and scientific communication: reliable identification and correct naming of bacterial strains are not only primary aims of taxonomic studies, but also fundamental elements in an applied context, for the tracking of probiotic strains and a non fraudulent labelling of fermented milks and pharmaceutical products containing probiotic microorganisms. A number of resources freely available have been listed and their use is suggested for people concerned with different aspects of taxonomy. Some perspectives in taxonomy have been outlined, in particular considering the role of culture independent analyses to reveal the still unknown and uncultured microorganisms. Finally, the impact of the availability of whole-genome sequences in taxonomy is briefly explained: they have already begun to give insights on bacterial evolution, which will surely have implications on taxonomy, even if the analysis of data for lactic acid bacteria is still limited to few species.

[1]  Y. Benno,et al.  Catenibacterium mitsuokai gen. nov., sp. nov., a gram-positive anaerobic bacterium isolated from human faeces. , 2000, International journal of systematic and evolutionary microbiology.

[2]  W. Whitman,et al.  Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. , 2002, International journal of systematic and evolutionary microbiology.

[3]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[4]  M. Collins,et al.  The phylogeny of Aerococcus and Pediococcus as determined by 16S rRNA sequence analysis: description of Tetragenococcus gen. nov. , 1990, FEMS microbiology letters.

[5]  F. Clementi,et al.  Differentiation of Lactobacillus plantarum, L. pentosus and L. paraplantarum species by RAPD-PCR and AFLP. , 2001, Systematic and applied microbiology.

[6]  M. Ventura,et al.  Insights into the taxonomy, genetics and physiology of bifidobacteria , 2004, Antonie van Leeuwenhoek.

[7]  W. P. Hammes,et al.  The genera Lactobacillus and Carnobacterium , 1992 .

[8]  R. Norris,et al.  Biology of the bifidobacteria , 1973, Bacteriological reviews.

[9]  P. de Vos,et al.  Polyphasic Taxonomy , a Consensus Approach to Bacterial Systematics , 1996 .

[10]  L. Dicks,et al.  Designation of ATCC 334 in Place of ATCC 393 (NCDO 161) as the Neotype Strain of Lactobacillus casei subsp. casei and Rejection of the Name Lactobacillus paracasei (Collins et al., 1989): Request for an Opinion , 1991 .

[11]  P. A. Hansen,et al.  Lactobacillus casei (Orla-Jensen) comb. nov. , 1971 .

[12]  Y. K. Lee,et al.  Comparative analysis of the genes encoding 23S-5S rRNA intergenic spacer regions of Lactobacillus casei-related strains. , 2000, International journal of systematic and evolutionary microbiology.

[13]  M. Collins,et al.  Transfer of members of the genus Falcivibrio to the genus Mobiluncus, and emended description of the genus Mobiluncus. , 2004, Systematic and applied microbiology.

[14]  Tom Coenye,et al.  Opinion: Re-evaluating prokaryotic species. , 2005, Nature reviews. Microbiology.

[15]  S. Ehrlich,et al.  The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. , 2001, Genome research.

[16]  R. Rosselló-Móra Updating Prokaryotic Taxonomy , 2005, Journal of bacteriology.

[17]  A. Goffeau,et al.  Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus , 2004, Nature Biotechnology.

[18]  Alexander Goesmann,et al.  Complete Genome Sequence of the Prototype Lactic Acid Bacterium Lactococcus lactis subsp. cremoris MG1363 , 2007, Journal of bacteriology.

[19]  B. Pettersson,et al.  DNA-based classification and sequence heterogeneities in the 16S rRNA genes of Lactobacillus casei/paracasei and related species. , 2005, Systematic and applied microbiology.

[20]  M. Brandt,et al.  Lactobacillus secaliphilus sp. nov., isolated from type II sourdough fermentation. , 2007, International journal of systematic and evolutionary microbiology.

[21]  Katherine H. Huang,et al.  Comparative genomics of the lactic acid bacteria , 2006, Proceedings of the National Academy of Sciences.

[22]  W. Hammes,et al.  The genus Lactobacillus , 1995 .

[23]  K. Schleifer,et al.  Rapid genotypic differentiation of Lactococcus lactis subspecies and biovar , 1997 .

[24]  M. Kleerebezem,et al.  The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. , 2004, Microbiology.

[25]  G. Reid,et al.  Differentiation of Lactobacillus Species by Molecular Typing , 1998, Applied and Environmental Microbiology.

[26]  D. K. Olukoya,et al.  Lactobacillus plantarum subsp. argentoratensis subsp. nov., isolated from vegetable matrices. , 2005, International journal of systematic and evolutionary microbiology.

[27]  R. Aznar,et al.  Lactobacillus tucceti sp. nov., a new lactic acid bacterium isolated from sausage. , 2006, Systematic and applied microbiology.

[28]  D. van Sinderen,et al.  Diversity of the genus Lactobacillus revealed by comparative genomics of five species. , 2006, Microbiology.

[29]  V. Bottazzi,et al.  Deoxyribonucleic Acid Homology Among Lactobacillus Species of the Subgenus Streptobacterium Orla-Jensen , 1975 .

[30]  G. Muyzer,et al.  Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology , 2004, Antonie van Leeuwenhoek.

[31]  M. Rubner The Prolongation of Life. , 1928 .

[32]  S. Tynkkynen,et al.  Comparison of Ribotyping, Randomly Amplified Polymorphic DNA Analysis, and Pulsed-Field Gel Electrophoresis in Typing ofLactobacillus rhamnosus and L. caseiStrains , 1999, Applied and Environmental Microbiology.

[33]  R. Yolken,et al.  Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus , 1994, The Lancet.

[34]  D. Molenaar,et al.  Dichotomy in post-genomic microbiology , 2007, Nature Biotechnology.

[35]  Laetitia Fontaine,et al.  New insights in the molecular biology and physiology of Streptococcus thermophilus revealed by comparative genomics. , 2005, FEMS microbiology reviews.

[36]  D. Gevers,et al.  Re-evaluating prokaryotic species , 2005, Nature Reviews Microbiology.

[37]  L. Dicks,et al.  Reclassification of Lactobacillus casei subsp. casei ATCC 393 and Lactobacillus rhamnosus ATCC 15820 as Lactobacillus zeae nom. rev., designation of ATCC 334 as the neotype of L. casei subsp. casei, and rejection of the name Lactobacillus paracasei. , 1996, International journal of systematic bacteriology.

[38]  K. Schleifer,et al.  Phylogeny of the Genus Lactobacillus and Related Genera , 1995 .

[39]  W. Bockelmann,et al.  Rapid Identification of Streptococcus thermophilus by Primer-specific PCR Amplification Based on its lacZ Gene , 1996 .

[40]  A. Endo,et al.  Lactobacillus farraginis sp. nov. and Lactobacillus parafarraginis sp. nov., heterofermentative lactobacilli isolated from a compost of distilled shochu residue. , 2007, International journal of systematic and evolutionary microbiology.

[41]  R. Siezen,et al.  Natural diversity and adaptive responses of Lactococcus lactis. , 2006, Current opinion in biotechnology.

[42]  C. K. Mills,et al.  Lactobacterium zeae Kuznetsov, a Later Subjective Synonym of Lactobacillus casei (Orla-Jensen) Hansen and Lessel , 1973 .

[43]  D. Janssens,et al.  Characteristiques generales des bacteries lactiques , 1994 .

[44]  Lactobacillus composti sp. nov., a lactic acid bacterium isolated from a compost of distilled shochu residue. , 2007, International journal of systematic and evolutionary microbiology.

[45]  E. Koonin,et al.  Evolutionary Genomics of Lactic Acid Bacteria , 2006, Journal of bacteriology.

[46]  Y. Benno,et al.  Coprobacillus catenaformis Gen. Nov., Sp. Nov., a New Genus and Species Isolated from Human Feces , 2000, Microbiology and immunology.

[47]  S. Torriani,et al.  Reclassification of Pediococcus urinaeequi (ex Mees 1934) Garvie 1988 as Aerococcus urinaeequi comb. nov. , 2005, International journal of systematic and evolutionary microbiology.

[48]  Jonathan A. Eisen,et al.  The RecA protein as a model molecule for molecular systematic studies of bacteria: Comparison of trees of RecAs and 16S rRNAs from the same species , 1995, Journal of Molecular Evolution.

[49]  S. Torriani,et al.  Comparative sequence analysis of a recA gene fragment brings new evidence for a change in the taxonomy of the Lactobacillus casei group. , 2001, International journal of systematic and evolutionary microbiology.

[50]  S. Torriani,et al.  Differentiation of Lactobacillus plantarum,L. pentosus, and L. paraplantarum by recA Gene Sequence Analysis and Multiplex PCR Assay with recA Gene-Derived Primers , 2001, Applied and Environmental Microbiology.

[51]  J. Swings,et al.  Development and Validation of a Nested-PCR-Denaturing Gradient Gel Electrophoresis Method for Taxonomic Characterization of Bifidobacterial Communities , 2003, Applied and Environmental Microbiology.

[52]  G. Pershagen,et al.  Molecular Fingerprinting of the Fecal Microbiota of Children Raised According to Different Lifestyles , 2007, Applied and Environmental Microbiology.

[53]  Ramon Rosselló-Mora,et al.  Opinion: the species problem, can we achieve a universal concept? , 2003, Systematic and applied microbiology.

[54]  R. Colwell Polyphasic Taxonomy of the Genus Vibrio: Numerical Taxonomy of Vibrio cholerae, Vibrio parahaemolyticus, and Related Vibrio Species , 1970, Journal of bacteriology.

[55]  B. Biavati,et al.  The Family Bifidobacteriaceae , 2006 .

[56]  Elie. Metchnikoff The Prolongation of Life: Optimistic Studies , 2003 .

[57]  M. Collins,et al.  DNA base composition, DNA-DNA homology and long-chain fatty acid studies on streptococcus thermophilus and Streptococcus salivarius. , 1984, Journal of general microbiology.

[58]  Wen-Hsiung Li,et al.  Fundamentals of molecular evolution , 1990 .

[59]  S. Torriani,et al.  The status of the species Lactobacillus rogosae Holdeman and Moore 1974. Request for an opinion. , 2004, International journal of systematic and evolutionary microbiology.

[60]  K. Schleifer,et al.  Phylogenetic relationships ofBacteria based on comparative sequence analysis of elongation factor Tu and ATP-synthase β-subunit genes , 2004, Antonie van Leeuwenhoek.

[61]  P. Dawyndt,et al.  Reclassification of Lactobacillus kefirgranum Takizawa et al. 1994 as Lactobacillus kefiranofaciens subsp. kefirgranum subsp. nov. and emended description of L. kefiranofaciens Fujisawa et al. 1988. , 2004, International journal of systematic and evolutionary microbiology.

[62]  Horst Neve,et al.  Revival of the species Streptococcus thermophilus (ex Orla-Jensen, 1919) nom. rev. , 1991 .

[63]  P. Vandamme,et al.  Extracting phylogenetic information from whole-genome sequencing projects: the lactic acid bacteria as a test case. , 2003, Microbiology.

[64]  Wolfgang Ludwig,et al.  Taxonomy of Lactic Acid Bacteria , 1994 .

[65]  S. Torriani,et al.  Reclassification of Lactobacillus cellobiosus Rogosa et al. 1953 as a later synonym of Lactobacillus fermentum Beijerinck 1901. , 2004, International journal of systematic and evolutionary microbiology.

[66]  J. Gibrat,et al.  The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[67]  N. Shah,et al.  Discrimination of dairy industry isolates of the Lactobacillus casei group. , 2006, Journal of dairy science.

[68]  W B Whitman,et al.  Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. , 2001, International journal of systematic and evolutionary microbiology.

[69]  D. Tautz,et al.  A plea for DNA taxonomy , 2003 .

[70]  L. Zhu,et al.  New approach to phylogenetic analysis of the genus Bifidobacterium based on partial HSP60 gene sequences. , 2001, International journal of systematic and evolutionary microbiology.

[71]  K. Yamazaki,et al.  Comparative sequence analyses of the genes coding for 16S rRNA of Lactobacillus casei-related taxa. , 1997, International journal of systematic bacteriology.

[72]  A. Bull,et al.  Biodiversity as a source of innovation in biotechnology. , 1992, Annual review of microbiology.

[73]  R. Amann,et al.  The species concept for prokaryotes. , 2013, FEMS microbiology reviews.

[74]  M. Kleerebezem,et al.  Genome data mining of lactic acid bacteria: the impact of bioinformatics. , 2004, Current opinion in biotechnology.

[75]  J. Euzéby Request for an Opinion , 1999 .

[76]  Andrew T. Lloyd,et al.  Evolution of the recA gene and the molecular phylogeny of bacteria , 1993, Journal of Molecular Evolution.

[77]  Yin Li,et al.  Polyphasic analysis indicates that Lactobacillus salivarius subsp. salivarius and Lactobacillus salivarius subsp. salicinius do not merit separate subspecies status. , 2006, International journal of systematic and evolutionary microbiology.

[78]  M. Ventura,et al.  Analysis of bifidobacterial evolution using a multilocus approach. , 2006, International journal of systematic and evolutionary microbiology.

[79]  C. Woese,et al.  Bacterial evolution , 1987, Microbiological reviews.

[80]  A. Woodcock,et al.  Bifidobacterial Species Differentially Affect Expression of Cell Surface Markers and Cytokines of Dendritic Cells Harvested from Cord Blood , 2004, Clinical Diagnostic Laboratory Immunology.

[81]  Aldert L. Zomer,et al.  Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp cremoris MG1363 , 2007 .

[82]  K. Schleifer,et al.  Molecular Taxonomy: Classification and Identification , 1994 .

[83]  M. Ventura,et al.  Polyphasic taxonomic analysis of Bifidobacterium animalis and Bifidobacterium lactis reveals relatedness at the subspecies level: reclassification of Bifidobacterium animalis as Bifidobacterium animalis subsp. animalis subsp. nov. and Bifidobacterium lactis as Bifidobacterium animalis subsp. lactis , 2004, International journal of systematic and evolutionary microbiology.

[84]  H. Hayashi,et al.  Unification of Bifidobacterium infantis and Bifidobacterium suis as Bifidobacterium longum. , 2002, International journal of systematic and evolutionary microbiology.

[85]  W. Ludwig,et al.  Phylogenetic relationships of Bacteria based on comparative sequence analysis of elongation factor Tu and ATP-synthase beta-subunit genes. , 1993, Antonie van Leeuwenhoek.

[86]  M. Collins,et al.  Deoxyribonucleic Acid Homology Studies of Lactobacillus casei, Lactobacillus paracasei sp. nov., subsp. paracasei and subsp. tolerans, and Lactobacillus rhamnosus sp. nov., comb. nov. , 1989 .

[87]  S. Orla-Jensen The lactic acid bacteria , 1919 .

[88]  S. Torriani,et al.  The status of the species Lactobacillus casei (Orla-Jensen 1916) Hansen and Lessel 1971 and Lactobacillus paracasei Collins et al. 1989. Request for an opinion. , 2002, International journal of systematic and evolutionary microbiology.

[89]  Pha Sneath,et al.  International code of nomenclature of bacteria (1990 revision). , 1992 .