Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics - PubMed (original) (raw)
Comparative Study
Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics
Alex Mira et al. BMC Evol Biol. 2004.
Abstract
Background: The phylogenetic position and evolutionary relationships of Fusobacteria remain uncertain. Especially intriguing is their relatedness to low G+C Gram positive bacteria (Firmicutes) by ribosomal molecular phylogenies, but their possession of a typical gram negative outer membrane. Taking advantage of the recent completion of the Fusobacterium nucleatum genome sequence we have examined the evolutionary relationships of Fusobacterium genes by phylogenetic analysis and comparative genomics tools.
Results: The data indicate that Fusobacterium has a core genome of a very different nature to other bacterial lineages, and branches out at the base of Firmicutes. However, depending on the method used, 35-56% of Fusobacterium genes appear to have a xenologous origin from bacteroidetes, proteobacteria, spirochaetes and the Firmicutes themselves. A high number of hypothetical ORFs with unusual codon usage and short lengths were found and hypothesized to be remnants of transferred genes that were discarded. Some proteins and operons are also hypothesized to be of mixed ancestry. A large portion of the Gram-negative cell wall-related genes seems to have been transferred from proteobacteria.
Conclusions: Many instances of similarity to other inhabitants of the dental plaque that have been sequenced were found. This suggests that the close physical contact found in this environment might facilitate horizontal gene transfer, supporting the idea of niche-specific gene pools. We hypothesize that at a point in time, probably associated to the rise of mammals, a strong selective pressure might have existed for a cell with a Clostridia-like metabolic apparatus but with the adhesive and immune camouflage features of Proteobacteria.
Figures
Figure 1
Phylogenetic tree (Bayesian method) using the combined sequence of the 16S-23S rRNA of representative bacterial species. The Fusobacteria are a coherent and taxonomically independent group, that branches out at the base of the lineage leading to Firmicutes. Numbers represent bootstrap values. In the case of the branching of Fusobacteria/Firmicutes, the numbers represent the values obtained by four different methods: BA: Bayesian; NJ: Neighbor-joining; MP: Parsimony; ML: Maximum likelihood.
Figure 2
(G-C)/(G+C) values (GC-skew) plotted every 5000 bp for Fusobacterium nucleatum, the low-GC Gram positive Clostridium tetani and the bacteroidete Bacteroides thetaiotaomicron. Red wide arrows represent replication origin (bottom) and terminus (top). Orange thin arrows indicate the 36 "clusters" of four or more contiguous genes that are potentially transferred from species outside the Firmicutes. Note that some of F. nucleatum shifts in GC skew coincide with putative HGT regions.
Figure 3
Gene-position plot with a reconstruction of vertical descent and potentially-transferred genes across F. nucleatum genome. Plus signs indicate genes whose phylogenetic affiliation to a certain group on the left is supported by BLAST analysis only. Crosses indicate genes whose phylogenetic origin is supported by BLAST and by one or two other methods (phylogenetic tree reconstruction and gene order conservation). Thirty-six clusters are indicated containing four or more consecutive genes that appear to have a xenologous origin (i.e. a phylogenetic affiliation outside the Firmicutes). Details of these clusters are explained in Table 2. Arrowheads at the top indicate the position of transposases. Arrowheads at the bottom indicate position of phage-related genes. Plus signs and crosses indicate potential transfers to/from Firmicutes (Firm), Spirochaetes (Sp), alpha-beta-gamma Proteobacteria (αβγ-Pr), delta-epsilon Proteobacteria (δε-Pr), Cytophaga-Flexibacter-Bacteroides Group (CFB), other bacterial groups (Others), Archaea, or genes that are consistent with the phylogeny (CWP) shown in Figure 1 and additional file 1.
Figure 4
Gene order conservation in some representative cases of potentially-transferred clusters. Homologous genes are shown with the same colour in F. nucleatum and the species with which it is compared. Small black boxes represent short orphan genes. Non-contiguous genes are separated by an interrupted line. Genes are not drawn to scale.
Figure 5
Chimeric operons (metabolic pathways of putatively mixed origin) in F. nucleatum. Arrowed boxes represent gene orientation, coloured by BLAST top hit. White boxes: top hit to Firmicutes; grey boxes: top hit to Archaeal species; black boxes: top hit in Gram negative species. Numbers below boxes indicate the percent of top ten hits that have matches in Firmicutes. Names above indicate gene names (I-BP: Iron binding protein; NIP: Nitrogenase iron protein; Oxdtase: Oxidoreductase; B, C, D, F: dipeptide permeases B, C, D, F; BP: dipeptide binding protein; Tr: ABC transporter; unk: unknown function gene; Rec: Hemin receptor). Best match taxa by the phylogenetic tree and gene order methods are also indicated (A: Archaea; Pr: Proteobacteria; Sp: Spirochaetes; CP: consistent with (ribosomal) phylogeny; O: other eubacteria; x: unresolved; --: not analysed. Plus signs indicate unusual DNA composition by the method of García-Vallvé et al. 2003.
Figure 6
Length frequency distributions for F. nucleatum proteins. Genes are divided by the group with closest sequence similarity match. ORFs without sequence similarity on the non-redundant NCBI database (orphan genes) are significantly shorter than the rest.
References
- Duncan MJ. Genomics of oral bacteria. Crit Rev Oral Biol Med. 2003;14:175–187. - PubMed
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