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Chapter 16 : Genomics of a Pathogen and Symbiont

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Abstract:

This chapter addresses questions related to the genomics of , compares the genome with to identify putative pathogenicity islands, and compares different in order to identify islands that are putatively specific to different species with different life cycles. At present, we have full genome sequences from both an exclusive insect pathogen, TT01, and an insect pathogen that has also been recovered from human wounds, . Comparisons between these two very different species should therefore also shed light on the evolution of vertebrate pathogenicity in the genus. Comparison of virulence cassette (PVC) loci of different strains shows that different strains possess different complements of units. In order to clarify the relationship between the insect-related (PIR) AB toxins and the protein labeled as a JHE in the Colorado potato beetle, we cloned 4093 and 4092 from TT01 and tested them for injectable activity against . Similarly, comparisons of the loci of different species show that three different deletions have led to the three independent losses of components in , , and TT01. DNA-based microarrays have been used in the comparative genomics of different species and strains in order to attempt to identify regions involved in the specificity of the nematode interaction. The authors have compared the genome of the insect pathogen with that of the human pathogen in an attempt to understand what makes asymbiotica so pathogenic.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 1
FIGURE 1

Life cycle of . The bacteria are carried by a vector nematode that seeks out and penetrates insects. The bacteria are then regurgitated from the nematode gut and are used to kill the insect and bioconvert the corpse. In the meantime, while feeding off the bacteria, the nematodes undergo several rounds of reproduction. When the cadaver is exhausted, the nematodes produce a new generation of infective juveniles, which reuptake the bacteria and exit the cadaver to seek new hosts.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 2
FIGURE 2

Diagram showing the relationship between genes found on the plasmid of the free-living and the nematode-associated . Note that the form A, B, and C components of the toxin complex proteins and that these then correspond to elements of the , and locus of , as indicated by shading.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 3
FIGURE 3

Relationship between the plasmid-borne virulence (spv) locus and and from . Note that , is predicted to be -like and that following there is a fragment of a -like gene. The predicted amino acid sequence of the N terminus of is also similar to . These organizational relationships suggest that the similarity of these three loci could relate to a common plasmid-borne ancestor (see text).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 4
FIGURE 4

Gene encoding Mcf1 toxin, found in different genomic locations in different strains. In TT01 and W14, the gene is located near a Phe tRNA in a classic PAI organization. In and , mcf1 is found at different genomic locations away from a predicted tRNA. Note that in pf5 that is encoded next to type I export machinery (see text for discussion).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 5
FIGURE 5

Genomic location of and its relationship to the rest of the group of Mcf-like toxins. The gene encoding Mcf2 in both TT01 and W14 is encoded next to type I export machinery, suggesting type I secretion for this toxin. Below this diagram is shown the modular nature of this group of toxins. In each case, the N terminus of the Mcf-like toxin encodes a putative effector domain, whereas the rest of the toxin is inferred to be involved in toxin export (C terminus) and translocation (central domain).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 6
FIGURE 6

Basic organization of a virulence cassette (PVC) and comparison with the antifeeding prophage from . Note that the PVC locus is composed of conserved PVC elements encoding phage components such as phage tails and baseplates, and a “payload” region that contains open reading frames with predicted similarity to known bacterial effectors. The organization of the antifeeding prophage from , which stops feeding of New Zealand grass grub, is shown for comparison (see text).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 7
FIGURE 7

Comparison of genomic organization of virulence cassette (PVC) loci in TT01 and ATCC43949. Note that multiple PVC units in TT01 (units 1–4) correspond to single PVC units (unit pil) in . The boxes represent predicted open reading frames (ORFs). ORFs shaded gray correspond to PVC cassettes, and those in black (highlighted with arrows) show similarity to known bacterial effectors.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 8
FIGURE 8

Plates showing the structure of a virulence cassette (PVC) as seen under transmission electron microscopy. Note the inner and outer sheath of the PVC, which is reminiscent of an R-type pyocin, which is a bacteriocin. Note that the outer sheath (arrow in B) can be contracted, revealing the long inner sheath (arrow in C).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 9
FIGURE 9

Comparison between the type III secretion systems (TTSS) in and . Note the similar organization of the genes encoding the TTSS but the variable presence of different effector genes with similarity to lopT, sycT, exoU, and spcU TTSS delivered effectors.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 10
FIGURE 10

Family tree of strains and species showing the relationship between the presence of different loci and the resulting insecticidal phenotype. Note that the common ancestor for all had a locus. The locus was then acquired by the () group containing W14 and TT01. Subsequently, was independently lost at least three times, once in the TT01 group (Δ), and then twice in the (, Δ2tca) or (, Δ) groups. This accounts for the differences in the oral toxicity of the cells (Tcd associated) and supernatants (Tca associated) seen between the strains. Solid black circles indicate the presence of a gene; shaded circles indicate its absence.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 11
FIGURE 11

Diagram showing the gain of part of the island that confers cell-associated oral toxicity to . Note that in the other species, this part of the PAI has never been present.

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 12
FIGURE 12

Independent losses of locus elements in different strains and species. Note the complete locus in W14 that confers oral toxi-city of bacterial supernatants to . Note also that the locus has been independently deleted in each of the other three strains (see text).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 13
FIGURE 13

Diagram showing -like loci in different strains and species of . In CO92, is disrupted (asterisk), but in KIM, this ORF is intact. Note that similar loci are found in the close relatives and , which may have implications for the evolution of the flea association of (see text).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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Image of FIGURE 14
FIGURE 14

Diagram showing the relative location of cosmid clones from either causing toxicity in individual insects (below the line) or allowing for the persistence of recombinant injected into insects (above the line). The line represents the complete genome sequence of . Note that clusters of clones causing either toxicity or persistence are often the same (vertical dotted lines). A general classification of these clusters is given to the left of the diagram. The star represents the location of the toxic PVC cluster (see text).

Citation: ffrench-Constant R, Dowling A, Hares M, Yang G, Waterfield N. 2007. Genomics of a Pathogen and Symbiont, p 419-439. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch16
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