Genome sequence of the pathogenic intestinal spirochete brachyspira hyodysenteriae reveals adaptations to its lifestyle in the porcine large intestine

Abstract

Brachyspira hyodysenteriae is an anaerobic intestinal spirochete that colonizes the large intestine of pigs and causes swine dysentery, a disease of significant economic importance. The genome sequence of B. hyodysenteriae strain WA1 was determined, making it the first representative of the genus Brachyspira to be sequenced, and the seventeenth spirochete genome to be reported. The genome consisted of a circular 3,000,694 base pair (bp) chromosome, and a 35,940 bp circular plasmid that has not previously been described. The spirochete had 2,122 protein-coding sequences. Of the predicted proteins, more had similarities to proteins of the enteric Escherichia coli and Clostridium species than they did to proteins of other spirochetes. Many of these genes were associated with transport and metabolism, and they may have been gradually acquired through horizontal gene transfer in the environment of the large intestine. A reconstruction of central metabolic pathways identified a complete set of coding sequences for glycolysis, gluconeogenesis, a non-oxidative pentose phosphate pathway, nucleotide metabolism, lipooligosaccharide biosynthesis, and a respiratory electron transport chain. A notable finding was the presence on the plasmid of the genes involved in rhamnose biosynthesis. Potential virulence genes included those for 15 proteases and six hemolysins. Other adaptations to an enteric lifestyle included the presence of large numbers of genes associated with chemotaxis and motility. B. hyodysenteriae has diverged from other spirochetes in the process of accommodating to its habitat in the porcine large intestine.

Figure 1. Circular representation of the B. hyodysenteriae WA1 genome, with annotated genes.

A, Chromosome (CI); B , Plasmid (PI). Circles range from 1 (outer circle) to 6 (inner circle) for CI and I (outer circle) to IV (inner circle) for PI. Circles 1/I and 2/II, genes and forward and reverse strand; circle 3, tRNA genes; circle 4, rRNA genes, circle 5/III, GC bias/skew ((G-C)/(G+C); red indicates values >0; green indicates values <0); circles 6/IV, A+T percentage content. All genes are color-coded according to Cluster of Orthologous Group (COG) functions: violet for translation, ribosomal structure and biogenesis; plum for RNA processing and modification; pink for transcription; deep pink for DNA replication, recombination and repair; hot pink for chromatin structure and dynamics; wheat for cell division and chromosome partitioning; light salmon for nuclear structure; yellow for defence mechanisms; gold for signal transduction mechanisms; pale green for cell envelope biogenesis, outer membrane; spring green for cell motility and secretion; lawn green for cytoskeleton; yellow green for extracellular structures; aquamarine for intracellular trafficking, secretion, and vesicular transport; medium aquamarine for posttranslational modification, protein turnover, chaperones; cyan for energy production and conversion; deep sky blue for carbohydrate transport and metabolism; sky blue for amino acid transport and metabolism; light slate blue for nucleotide transport and metabolism; orchid for coenzyme metabolism; medium orchid for lipid metabolism; dark orchid for inorganic ion transport and metabolism; blue violet for secondary metabolites biosynthesis, transport and catabolism; slate grey for general function prediction only; grey for function unknown; gray for not in COGS; black for tRNA.

Figure 2. Central metabolic pathway construction for B. hyodysenteriae WA1.