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. 2014 Oct;80(20):6383-94.
doi: 10.1128/AEM.02004-14. Epub 2014 Aug 8.

Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics

Gabriele Andrea Lugli  1 , Christian Milani  1 , Francesca Turroni  2 , Sabrina Duranti  1 , Chiara Ferrario  1 , Alice Viappiani  3 , Leonardo Mancabelli  3 , Marta Mangifesta  3 , Bernard Taminiau  4 , Véronique Delcenserie  4 , Douwe van Sinderen  2 , Marco Ventura  5
Affiliations

Investigation of the evolutionary development of the genus Bifidobacterium by comparative genomics

Gabriele Andrea Lugli et al. Appl Environ Microbiol. 2014 Oct.

Abstract

The Bifidobacterium genus currently encompasses 48 recognized taxa, which have been isolated from different ecosystems. However, the current phylogeny of bifidobacteria is hampered by the relative paucity of genotypic data. Here, we reassessed the taxonomy of this bacterial genus using genome-based approaches, which demonstrated that the previous taxonomic view of bifidobacteria contained several inconsistencies. In particular, high levels of genetic relatedness were shown to exist between particular Bifidobacterium taxa which would not justify their status as separate species. The results presented are here based on average nucleotide identity analysis involving the genome sequences for each type strain of the 48 bifidobacterial taxa, as well as phylogenetic comparative analysis of the predicted core genome of the Bifidobacterium genus. The results of this study demonstrate that the availability of complete genome sequences allows the reconstruction of a more robust bifidobacterial phylogeny than that obtained from a single gene-based sequence comparison, thus discouraging the assignment of a new or separate bifidobacterial taxon without such a genome-based validation.

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Figures

FIG 1
FIG 1
Phylogenetic trees of the Bifidobacterium genus. (a) The 16S rRNA gene-based tree of the 48 bifidobacterial taxa currently recognized. (b) The 23S rRNA gene-based tree of the same 48 bifidobacterial taxa as shown in panel a. For each tree, bootstrap values higher than 70 are marked near the respective node, and phylogenetic clusters are identified by shading as indicated on the figure. With the exception of a small number of species, seven conserved clusters (designated groups A to G) are present in each tree although the groups are arranged in different positions.
FIG 2
FIG 2
Graphical representation in three-dimensional columns of the average nucleotide identity (ANI) matrix shown in Table S4 in the supplemental material, based on the analysis of the 48 bifidobacterial type strain genome sequences. On the x axis are located the 48 bifidobacterial taxa to generate a matrix; the y axis reflects the ANI percentages such that each column represents the ANI observed between a given bifidobacterial species pair. All bifidobacterial pairs that show an ANI value of >94% are highlighted according to the legend at the top of the figure. The paired numbers above the columns correspond to the numbering identifying the organisms described in Table 1.
FIG 3
FIG 3
Supertree of the Bifidobacterium genus based on the concatenation of the 411 core BifCOG amino acid sequences identified by the PGAP analysis (core BifCOGs that include bifidobacterial paralogs have been excluded in this analysis). Bootstrap values higher than 70 are marked near the respective nodes showing a robust phylogenetic reconstruction, and the seven phylogenetic clusters are highlighted by patterned shading.
FIG 4
FIG 4
Average Ka/Ks ratio between bifidobacterial pairs represented by a fan-shaped chart. The diagram was built on the bifidobacterial core gene supertree presented in Fig. 2, and the numbers placed at the supertree leaves represent the related bifidobacterial taxa presented in Table 1. The columns indicate the average Ka/Ks ratios of the flanking bifidobacterial taxa. For bifidobacterial taxa pairs having high Ka/Ks ratios, the corresponding values are indicated above the columns.
FIG 5
FIG 5
Consensus clustering based on the inclusion of results from the phylogenetic distance matrix, the level of nucleotide identity between genomes, and the genome distance index detected between all 48 bifidobacterial taxa. (a) Polar cluster where all bifidobacterial taxa proposed here as members of the same species fall in the same cluster, highlighted by different colors. (b) Principal coordinate analysis (PCoA) of the same data set used to generate the polar cluster. In the central PCoA image, recognized bifidobacterial subspecies and related species discussed in the main text are circled in red to separate them from the remaining bifidobacterial species, which are represented by orange squares.
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