Genomes of the class Erysipelotrichia clarify the firmicute origin of the class Mollicutes

Abstract

The tree of life is paramount for achieving an integrated understanding of microbial evolution and the relationships between physiology, genealogy and genomics. It provides the framework for interpreting environmental sequence data, whether applied to microbial ecology or to human health. However, there remain many instances where there is ambiguity in our understanding of the phylogeny of major lineages, and/or confounding nomenclature. Here we apply recent genomic sequence data to examine the evolutionary history of members of the classes Mollicutes (phylum Tenericutes) and Erysipelotrichia (phylum Firmicutes). Consistent with previous analyses, we find evidence of a specific relationship between them in molecular phylogenies and signatures of the 16S rRNA, 23S rRNA, ribosomal proteins and aminoacyl-tRNA synthetase proteins. Furthermore, by mapping functions over the phylogenetic tree we find that the erysipelotrichia lineages are involved in various stages of genomic reduction, having lost (often repeatedly) a variety of metabolic functions and the ability to form endospores. Although molecular phylogeny has driven numerous taxonomic revisions, we find it puzzling that the most recent taxonomic revision of the phyla Firmicutes and Tenericutes has further separated them into distinct phyla, rather than reflecting their common roots.

Fig. 1.

The ribosomal phylogeny of the mollicutes and low G+C Gram-positive bacteria. Previously described groups are coloured (Weisburg et al., 1989). Members of the class Erysipelotrichia are shown in blue, the anaeroplasma group is shown in orange, the asteroleplasma group is shown in teal, the spiroplasma group is shown in purple, the Mycoplasma hominis group is shown in green and the Mycoplasma pneumoniae group is shown in red. Other low G+C Gram-positives are shown in grey. A wedge depicts taxonomic groups that have been collapsed. The top and bottom of the wedge describes the longest and shortest branch lengths found in each group. The total number of taxa is shown in parentheses. The root position for each tree is arbitrary. All trees are maximum-likelihood. Bootstrap values are for 1000 replicates. Bars, 0.5 substitutions per position. Fully expanded trees are shown in Fig. S2.

Fig. 2.

The frequency of gaps occurring at positions in the 16S rRNA gene sequence. 16S alignments were made for a) the class Clostridia (82 individual species), b) the class Bacilli (76 individual species), c) the class Erysipelotrichia (26 organisms with more than one strain of a species) and d) the phylum Tenericutes (56 organisms with more than one strain of a species). Each block in the diagram represents a nucleotide position and colouring is as follows: grey, a gap occurring at a frequency of less than 0.001; violet, a gap occurring at a frequency of less than 0.05; blue, a gap occurring a frequency of less than 0.2; green, a gap occurring at a frequency of less than 0.35; yellow, a gap occurring at a frequency of less than 0.5; orange, a gap occurring at a frequency of less than 0.75; and red, a gap occurring at a frequency of greater than 0.75. Variable regions V1–V9 are indicated for reference (Böttger, 1996).

Fig. 3.

Characteristics of the genomes of members of the classes Erysipelotrichia and Mollicutes. The 23S rRNA gene tree from Fig. 1(b) is shown. For each genome, the first three columns of data show the number of protein-encoding genes, the mean DNA G+C content for all protein-encoding genes, and the percentage of genes in the genome that match the modal codon usage of any mollicute genome. In each case, collapsed taxa are depicted as a range. The remaining columns indicate whether the given genome has known genes for: purine biosynthesis (Pur, red), pyrimidine biosynthesis (Pyr, orange), fatty acid biosynthesis (Fab, yellow), arginine biosynthesis (Arg, green), tryptophan biosynthesis (Trp, blue) and the formation of endospores (Spo, purple). Presumed pathway losses are indicated by correspondingly coloured vertical bars on the branches in the tree.