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Comparative genomics of unintrogressed Campylobacter coli clades 2 and 3.

Skarp-de Haan CP, Culebro A, Schott T, Revez J, Schweda EK, Hänninen ML, Rossi M - BMC Genomics (2014)

Bottom Line: A more extensive respiratory metabolism among unintrogressed C. coli strains was found compared to introgressed C. coli (clade 1).We propose new insights into the evolution of the accessory genome of C. coli clade 3 and C. jejuni.Also, in silico analysis of the gene content revealed that C. coli clades 2 and 3 have genes associated with infection, suggesting they are a potent human pathogen, and may currently be underreported in human infections due to niche separation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Food Hygiene and Environmental Health, Helsinki University, Helsinki, Finland. astrid.dehaan@helsinki.fi.

ABSTRACT

Background: Campylobacter jejuni and C. coli share a multitude of risk factors associated with human gastrointestinal disease, yet their phylogeny differs significantly. C. jejuni is scattered into several lineages, with no apparent linkage, whereas C. coli clusters into three distinct phylogenetic groups (clades) of which clade 1 has shown extensive genome-wide introgression with C. jejuni, yet the other two clades (2 and 3) have less than 2% of C. jejuni ancestry. We characterized a C. coli strain (76339) with four novel multilocus sequence type alleles (ST-5088) and having the capability to express gamma-glutamyltranspeptidase (GGT); an accessory feature in C. jejuni. Our aim was to further characterize unintrogressed C. coli clades 2 and 3, using comparative genomics and with additional genome sequences available, to investigate the impact of horizontal gene transfer in shaping the accessory and core gene pools in unintrogressed C. coli.

Results: Here, we present the first fully closed C. coli clade 3 genome (76339). The phylogenomic analysis of strain 76339, revealed that it belonged to clade 3 of unintrogressed C. coli. A more extensive respiratory metabolism among unintrogressed C. coli strains was found compared to introgressed C. coli (clade 1). We also identified other genes, such as serine proteases and an active sialyltransferase in the lipooligosaccharide locus, not present in C. coli clade 1 and we further propose a unique scenario for the evolution of Campylobacter ggt.

Conclusions: We propose new insights into the evolution of the accessory genome of C. coli clade 3 and C. jejuni. Also, in silico analysis of the gene content revealed that C. coli clades 2 and 3 have genes associated with infection, suggesting they are a potent human pathogen, and may currently be underreported in human infections due to niche separation.

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Phylogram representing maximum-likelihood tree of C. jejuni and C. coli. The phylogenetic position of C. coli 76339 is shown. All nodes were supported >80%, except for one node which was supported 51% and is indicated with an asterisk.
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Figure 2: Phylogram representing maximum-likelihood tree of C. jejuni and C. coli. The phylogenetic position of C. coli 76339 is shown. All nodes were supported >80%, except for one node which was supported 51% and is indicated with an asterisk.

Mentions: The phylogenetic position of C. coli 76339 is shown in Figure 2. The whole-genome alignment of 4,772,631 bp, including 64C. coli genomes and five C. jejuni strains (Additional file 1: Table S1), were treated with Gblocks which resulted in a gap-less multi-sequence alignment of 347,477 bp (~7% of the original multi-sequence alignment), which was used to build a Maximum Likelihood (ML) tree. The topology of the ML tree, based on the whole-genome alignment, resembled the neighbour-joining tree based on average genetic distances previously published by Sheppard et al. [14], and placed C. coli 76339 in clade 3 of unintrogressed strains [14]. In both the ML and the NJ tree, the branch of C. jejuni intersects the C. coli tree between clade 1a (ST-828 CC) and 1b (ST-1150 CC). As previously described, this position does not reflect the true evolution of C. coli, but instead is a consequence of introgression (interspecies recombination) of clade 1, and in particular of C. coli CC 1150, with C. jejuni[14]. This result indicates that interspecies recombination influences the topology of a ML tree when based on whole-genome alignment.


Comparative genomics of unintrogressed Campylobacter coli clades 2 and 3.

Skarp-de Haan CP, Culebro A, Schott T, Revez J, Schweda EK, Hänninen ML, Rossi M - BMC Genomics (2014)

Phylogram representing maximum-likelihood tree of C. jejuni and C. coli. The phylogenetic position of C. coli 76339 is shown. All nodes were supported >80%, except for one node which was supported 51% and is indicated with an asterisk.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3928612&req=5

Figure 2: Phylogram representing maximum-likelihood tree of C. jejuni and C. coli. The phylogenetic position of C. coli 76339 is shown. All nodes were supported >80%, except for one node which was supported 51% and is indicated with an asterisk.
Mentions: The phylogenetic position of C. coli 76339 is shown in Figure 2. The whole-genome alignment of 4,772,631 bp, including 64C. coli genomes and five C. jejuni strains (Additional file 1: Table S1), were treated with Gblocks which resulted in a gap-less multi-sequence alignment of 347,477 bp (~7% of the original multi-sequence alignment), which was used to build a Maximum Likelihood (ML) tree. The topology of the ML tree, based on the whole-genome alignment, resembled the neighbour-joining tree based on average genetic distances previously published by Sheppard et al. [14], and placed C. coli 76339 in clade 3 of unintrogressed strains [14]. In both the ML and the NJ tree, the branch of C. jejuni intersects the C. coli tree between clade 1a (ST-828 CC) and 1b (ST-1150 CC). As previously described, this position does not reflect the true evolution of C. coli, but instead is a consequence of introgression (interspecies recombination) of clade 1, and in particular of C. coli CC 1150, with C. jejuni[14]. This result indicates that interspecies recombination influences the topology of a ML tree when based on whole-genome alignment.

Bottom Line: A more extensive respiratory metabolism among unintrogressed C. coli strains was found compared to introgressed C. coli (clade 1).We propose new insights into the evolution of the accessory genome of C. coli clade 3 and C. jejuni.Also, in silico analysis of the gene content revealed that C. coli clades 2 and 3 have genes associated with infection, suggesting they are a potent human pathogen, and may currently be underreported in human infections due to niche separation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Food Hygiene and Environmental Health, Helsinki University, Helsinki, Finland. astrid.dehaan@helsinki.fi.

ABSTRACT

Background: Campylobacter jejuni and C. coli share a multitude of risk factors associated with human gastrointestinal disease, yet their phylogeny differs significantly. C. jejuni is scattered into several lineages, with no apparent linkage, whereas C. coli clusters into three distinct phylogenetic groups (clades) of which clade 1 has shown extensive genome-wide introgression with C. jejuni, yet the other two clades (2 and 3) have less than 2% of C. jejuni ancestry. We characterized a C. coli strain (76339) with four novel multilocus sequence type alleles (ST-5088) and having the capability to express gamma-glutamyltranspeptidase (GGT); an accessory feature in C. jejuni. Our aim was to further characterize unintrogressed C. coli clades 2 and 3, using comparative genomics and with additional genome sequences available, to investigate the impact of horizontal gene transfer in shaping the accessory and core gene pools in unintrogressed C. coli.

Results: Here, we present the first fully closed C. coli clade 3 genome (76339). The phylogenomic analysis of strain 76339, revealed that it belonged to clade 3 of unintrogressed C. coli. A more extensive respiratory metabolism among unintrogressed C. coli strains was found compared to introgressed C. coli (clade 1). We also identified other genes, such as serine proteases and an active sialyltransferase in the lipooligosaccharide locus, not present in C. coli clade 1 and we further propose a unique scenario for the evolution of Campylobacter ggt.

Conclusions: We propose new insights into the evolution of the accessory genome of C. coli clade 3 and C. jejuni. Also, in silico analysis of the gene content revealed that C. coli clades 2 and 3 have genes associated with infection, suggesting they are a potent human pathogen, and may currently be underreported in human infections due to niche separation.

Show MeSH
Related in: MedlinePlus