Genomic Characteristics of Desulfonema ishimotonii Tokyo 01T Implying Horizontal Gene Transfer Among Phylogenetically Dispersed Filamentous Gliding Bacteria

Abstract

Desulfonema ishimotonii strain Tokyo 01^T is a filamentous sulfate-reducing bacterium isolated from a marine sediment. In this study, the genome of this strain was sequenced and analyzed with a focus on gene transfer from phylogenetically distant organisms. While the strain belongs to the class Deltaproteobacteria, hundreds of proteins encoded in the genome showed the highest sequence similarities to those of organisms outside of the class Deltaproteobacteria, suggesting that more than 20% of the genome is putatively of foreign origins. Many of these proteins had the highest sequence identities with proteins encoded in the genomes of filamentous bacteria, including giant sulfur oxidizers of the orders Thiotrichales, cyanobacteria of various genera, and uncultured bacteria of the candidate phylum KSB3. As mobile genetic elements transferred from phylogenetically distant organisms, putative inteins were identified in the GyrB and DnaE proteins encoded in the genome of strain Tokyo 01^T. Genes involved in DNA recombination and repair were enriched in comparison to the closest relatives in the same family. Some of these genes were also related to those of organisms outside of the class Deltaproteobacteria, suggesting that they were acquired by horizontal gene transfer from diverse bacteria. The genomic data suggested significant genetic transfer among filamentous gliding bacteria in phylogenetically dispersed lineages including filamentous sulfate reducers. This study provides insights into the genomic evolution of filamentous bacteria belonging to diverse lineages, characterized by various physiological functions and different ecological roles.

Keywords: Desulfonema; complete genome sequence; filamentous sulfate-reducing bacterium; genetic transfer; genome analysis.

FIGURE 1

Relative abundances of COG categories in the genomes of strain Tokyo 01^T and its closest relatives in the genera Desulfosarcina (Ds.) and Desulfococcus (Dc.). Gray lines indicate average of the Desulfosarcina and Desulfococcus species included in the analysis. Red or blue circles indicate that the marked category is significantly enriched or depleted in Tokyo 01’s genome compared to the other genomes, as calculated by the method previously described (Sekiguchi et al., 2015).

FIGURE 2

Phylogenetic tree of putative GyrB intein of strain Tokyo 01^T and related sequences identified as the top 50 BLAST hits. This tree was constructed by using maximum-likelihood method with LG + G + I model. There were 114 positions in the final dataset. Bootstrap values (percentages of 1,000 replications) are shown at nodes. Neighbor-joining tree are present for comparison in Supplementary Figure S1 in the Supplementary Material.

FIGURE 3

Phylogenetic tree of putative DnaE intein of strain Tokyo 01^T and related sequences identified as the top 50 BLAST hits. This tree was constructed by using maximum-likelihood method with LG + G + I model. There were 284 positions in the final dataset. Bootstrap values (percentages of 1,000 replications) are shown at nodes. Neighbor-joining tree are present for comparison in Supplementary Figure S2 in the Supplementary Material.

FIGURE 4

RecQ phylogeny of the strain Tokyo 01^T and Desulfosarcina cetonica. The top 55 BLAST hits to DENIS_2396 were used as the dataset to construct the tree. There were 662 positions in the final dataset. This tree was constructed by using maximum-likelihood method with LG + G + I model. Bootstrap values (percentages of 1,000 replications) are shown at nodes.

FIGURE 5

RecQ phylogeny of the strain Tokyo 01^T and D. multivorans. The dataset consists the top 50 BLAST hits to DENIS_3915 and 20 hits to the RecQ of D. multivorans. There were 560 positions in the final dataset. This tree was constructed by using maximum-likelihood method with LG + G + I model. Bootstrap values (percentages of 1,000 replications) lower than 50% are shown at nodes.