The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes

Abstract

Members of the genus Xenorhabdus are entomopathogenic bacteria that associate with nematodes. The nematode-bacteria pair infects and kills insects, with both partners contributing to insect pathogenesis and the bacteria providing nutrition to the nematode from available insect-derived nutrients. The nematode provides the bacteria with protection from predators, access to nutrients, and a mechanism of dispersal. Members of the bacterial genus Photorhabdus also associate with nematodes to kill insects, and both genera of bacteria provide similar services to their different nematode hosts through unique physiological and metabolic mechanisms. We posited that these differences would be reflected in their respective genomes. To test this, we sequenced to completion the genomes of Xenorhabdus nematophila ATCC 19061 and Xenorhabdus bovienii SS-2004. As expected, both Xenorhabdus genomes encode many anti-insecticidal compounds, commensurate with their entomopathogenic lifestyle. Despite the similarities in lifestyle between Xenorhabdus and Photorhabdus bacteria, a comparative analysis of the Xenorhabdus, Photorhabdus luminescens, and P. asymbiotica genomes suggests genomic divergence. These findings indicate that evolutionary changes shaped by symbiotic interactions can follow different routes to achieve similar end points.

Figure 1. Circular maps of the Xenorhabdus nematophila chromosome, its plasmid, and the Xenorhabdus bovienii chromosome.

Shown are schematic maps of the X. nematophila chromosome (A) the X. nematophila plasmid (B) and the X. bovienii chromosome (C). In all three maps, the outer circle represents scale in base pair coordinates, and moving inward, circles 1 and 2 indicate predicted coding regions transcribed clockwise and counterclockwise respectively. Coding sequences are color coded by their Clusters of Orthologous Groups of proteins (COG) assignments. Information storage and processing: green, translation, ribosomal structure and biogenesis; forest green, RNA processing and modification; sea green, transcription; medium aquamarine, replication, recombination and repair; aquamarine, chromatin structure and dynamics; Cellular processes and signaling: blue; cell cycle control, cell division, chromosome partitioning; purple, nuclear structure; magenta, defense mechanisms; turquoise, signal transduction mechanisms; sky blue, cell wall/membrane/envelope biogenesis; medium blue, cell motility; royal blue, cytoskeleton; slate blue, extracellular structures; cornflower blue, intracellular trafficking, secretion, and vesicular transport; lavender, posttranslational modification, protein turnover, chaperones; Metabolism: red, energy production and conversion; yellow, carbohydrate transport and metabolism; orange, amino acid transport and metabolism; salmon, nucleotide transport and metabolism; pink, coenzyme transport and metabolism; chocolate, lipid transport and metabolism; gold, inorganic ion transport and metabolism; firebrick, secondary metabolites biosynthesis, transport and catabolism; Poorly characterized: black, general function prediction only; gray, function unknown. In (A) and (C) circle 3 shows coding regions for non-ribosomal peptide and polyketide synthases, while circle 4 shows genes present in the respective genome, but absent from Escherichia coli K12 MG1655; Photorhabdus luminescens TTO1; P. asymbiotica ATCC 43949 and Salmonella typhimurium LT2. For all three maps the innermost circle represents the GC content in 1000-bp windows relative to the mean GC content of the whole sequence.

Figure 2. Comparison of the phylogenetic relationships between Enterobacteria and their respective nematode hosts.

A 16S rRNA phylogenetic tree for selected bacteria within the phylum Proteobacteria is shown on the left. An 18S inter-ribosomal RNA sequence phylogenetic tree for selected nematodes is shown on the right. The associations of Xenorhabdus and Photorhabdus bacteria (yellow) with their known hosts are shown with pink and blue lines, respectively. Both phylogenies were constructed using maximum likelihood with bootstrap values indicated at tree nodes (100 replicates).

Figure 3. Comparison of the orthologs between sequenced Xenorhabdus with Photorhabdus bacteria.

A Venn diagram showing the number of orthologs between all four genomes.