Genome sequence of the mesophilic Thermotogales bacterium Mesotoga prima MesG1.Ag.4.2 reveals the largest Thermotogales genome to date

Abstract

Here we describe the genome of Mesotoga prima MesG1.Ag4.2, the first genome of a mesophilic Thermotogales bacterium. Mesotoga prima was isolated from a polychlorinated biphenyl (PCB)-dechlorinating enrichment culture from Baltimore Harbor sediments. Its 2.97 Mb genome is considerably larger than any previously sequenced Thermotogales genomes, which range between 1.86 and 2.30 Mb. This larger size is due to both higher numbers of protein-coding genes and larger intergenic regions. In particular, the M. prima genome contains more genes for proteins involved in regulatory functions, for instance those involved in regulation of transcription. Together with its closest relative, Kosmotoga olearia, it also encodes different types of proteins involved in environmental and cell-cell interactions as compared with other Thermotogales bacteria. Amino acid composition analysis of M. prima proteins implies that this lineage has inhabited low-temperature environments for a long time. A large fraction of the M. prima genome has been acquired by lateral gene transfer (LGT): a DarkHorse analysis suggests that 766 (32%) of predicted protein-coding genes have been involved in LGT after Mesotoga diverged from the other Thermotogales lineages. A notable example of a lineage-specific LGT event is a reductive dehalogenase gene-a key enzyme in dehalorespiration, indicating M. prima may have a more active role in PCB dechlorination than was previously assumed.

Fig. 1.—

Position of M. prima within the Thermotogales. The maximum likelihood tree of 16S rRNA sequences was reconstructed using the PhyML program (Guindon and Gascuel 2003), under GTR + G + I model with 100 bootstrap replicates. Only bootstrap support values above 70% are shown. The Mesotoga prima genome contains two 16S rRNA genes, labeled A and B. Thermoanaerobacter brockii and Ammonifex thiophilus were used as an outgroup. Sequences were aligned by the NAST aligner at GreenGenes (Desantis et al. 2006). GenBank accession numbers are shown for each sequence.

Fig. 2.—

Taxonomic distribution of putatively laterally transferred genes. The candidate genes were identified using the DarkHorse program (see Methods for details). NCBI Taxonomy database was used to assign organismal classification. The upper panel shows taxonomic distribution of 766 putatively transferred genes at the phylum level, whereas the lower panel details taxonomic distribution within the three most represented taxonomic groups.

Fig. 3.—

Comparison of the distributions of transferred genes across functional categories in M. prima and K. olearia genomes. The categories on the X axis are defined according to the COG database (see Methods) and grouped into four super-categories. For each functional category, a value above the Y axis shows the overrepresentation of transferred genes in M. prima in comparison to those in K. olearia genome, whereas the value below Y axis shows the overrepresentation of transferred genes in K. olearia in comparison to the M. prima genome. Overrepresentation is defined as a ratio of the proportion of transferred genes in two genomes.