Complete genome sequence and analysis of Wolinella succinogenes

Abstract

To understand the origin and emergence of pathogenic bacteria, knowledge of the genetic inventory from their nonpathogenic relatives is a prerequisite. Therefore, the 2.11-megabase genome sequence of Wolinella succinogenes, which is closely related to the pathogenic bacteria Helicobacter pylori and Campylobacter jejuni, was determined. Despite being considered nonpathogenic to its bovine host, W. succinogenes holds an extensive repertoire of genes homologous to known bacterial virulence factors. Many of these genes have been acquired by lateral gene transfer, because part of the virulence plasmid pVir and an N-linked glycosylation gene cluster were found to be syntenic between C. jejuni and genomic islands of W. succinogenes. In contrast to other host-adapted bacteria, W. succinogenes does harbor the highest density of bacterial sensor kinases found in any bacterial genome to date, together with an elaborate signaling circuitry of the GGDEF family of proteins. Because the analysis of the W. succinogenes genome also revealed genes related to soil- and plant-associated bacteria such as the nif genes, W. succinogenes may represent a member of the epsilon proteobacteria with a life cycle outside its host.

Fig. 1.

Circular representation of the W. succinogenes genome. The outer-most circles show predicted protein-coding regions on the + (wheel 1) and – (wheel 2) strands. The red bars on wheels 3 and 4 indicate ISs of the type IS1302. They are found on both strands, frequently flanking genomic islands and islets. These are depicted by orange bars on wheel 5 and are collinear with regions that show a large deviation from the average GC content (wheel 6). Non-protein-coding genes such as tRNA and rRNA genes are shown as brown and purple arrows on wheels 7 and 8. The origin of replication was defined by a bias of G over C (GC skew), which is clearly observable in wheel 9.

Fig. 2.

Phylogenetic analysis and taxonomy blast of the W. succinogenes genes. Each of the 2,046 W. succinogenes ORFs except the rRNAs were blasted on the protein level (blastp) against all NCBI database entries. (A) Taxonomic distribution of the genes. Approximately 32% of the predicted W. succinogenes proteins do have their closest homologue in H. pylori, another third in C. jejuni, and the remaining 38% in other organisms. Prominent herein are the Cyanobacteria (see also Fig. 3C) and the Enterobacteriaceae as well as the Pseudomonaceae (B).

Fig. 3.

Syntenic regions of the W. succinogenes genome. (A) Schematic representation of the W. succinogenes genomic island I and the syntenic region of the C. jejuni 81–176 virulence plasmid (pVir). Both loci encode multiple genes involved in type IV secretion. Connecting lines indicate corresponding orthologous genes with high homology on the protein level. (B) Schematic representation of the syntenic W. succinogenes and C. jejuni protein-glycosylation loci (pgl). (C) Schematic representation of the W. succinogenes nitrogen-fixation (nif) gene cluster in comparison to the partly syntenic nif cluster of the cyanobacterium Synechococcus RF-1. The interspersed white genes encode hypothetical proteins. The star indicates a W. succinogenes protein containing a DUF269 domain, also found within the nitrogen-fixation operons of Cyanobacteria.