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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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Comparison of the topology of a C. coli phylogenetic tree obtained with different approaches. A. Based on whole genome alignment using C. jejuni as an outgroup [13]. B. Based on 35 unrecombined rps genes using C. jejuni as an outgroup [14]. C. Based on 543 core genes using C. upsaliensis as an outgroup.
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Figure 3: Comparison of the topology of a C. coli phylogenetic tree obtained with different approaches. A. Based on whole genome alignment using C. jejuni as an outgroup [13]. B. Based on 35 unrecombined rps genes using C. jejuni as an outgroup [14]. C. Based on 543 core genes using C. upsaliensis as an outgroup.

Mentions: A previous study showed that in a tree based on 35 ribosomal proteins with no evidence of homologous recombination, the branch containing C. jejuni intersected the C. coli tree near to clade 3 [14]. Rooting this tree using C. jejuni as an outgroup showed that clade 3 has evolved from a common ancestor before the separation of clade 1 and 2 [Figure 3A and B, ref. [14], indicating that the unintrogressed C. coli strains are paraphyletic. In order to verify the evolution of C. coli, we inferred the species tree using a different approach. We selected one genome for each C. coli clade and C. upsaliensis, which has been demonstrated to be a sister group to the C. jejuni/C. coli clade [61], was chosen as an outgroup. We selected a total of 228 core genes out of 543 showing no statistically significant recombination among the strains. The ML tree obtained after concatenating those 228 unrecombined core genes showed that C. upsaliensis intersects the C. coli tree between clade 1, and clades 2 and 3 (Figure 3C). Both nodes are well supported with χ2-based parametric branch values of > 99%. In addition, the same topology was inferred by estimating the consensus tree of each of the 228 single gene trees using the extended majority rule method (data not shown), supporting the results obtained with concatenated genes. In fact, the splits ‘clade1a, clade1b / C. upsaliensis, clade 2, clade 3’ and ‘clade1a, clade1b, C. upsaliensis / clade 2, clade 3’ were present in 60.9% and 43.4% of the gene trees, respectively. In contrast, the split ‘clade 2, clade1a, clade1b / C. upsaliensis, clade 3’, which would support the topology of the concatenated unrecombined rps genes proposed by Sheppard et al. [14], was present in only 28% of the gene trees.


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)

Comparison of the topology of a C. coli phylogenetic tree obtained with different approaches. A. Based on whole genome alignment using C. jejuni as an outgroup [13]. B. Based on 35 unrecombined rps genes using C. jejuni as an outgroup [14]. C. Based on 543 core genes using C. upsaliensis as an outgroup.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Comparison of the topology of a C. coli phylogenetic tree obtained with different approaches. A. Based on whole genome alignment using C. jejuni as an outgroup [13]. B. Based on 35 unrecombined rps genes using C. jejuni as an outgroup [14]. C. Based on 543 core genes using C. upsaliensis as an outgroup.
Mentions: A previous study showed that in a tree based on 35 ribosomal proteins with no evidence of homologous recombination, the branch containing C. jejuni intersected the C. coli tree near to clade 3 [14]. Rooting this tree using C. jejuni as an outgroup showed that clade 3 has evolved from a common ancestor before the separation of clade 1 and 2 [Figure 3A and B, ref. [14], indicating that the unintrogressed C. coli strains are paraphyletic. In order to verify the evolution of C. coli, we inferred the species tree using a different approach. We selected one genome for each C. coli clade and C. upsaliensis, which has been demonstrated to be a sister group to the C. jejuni/C. coli clade [61], was chosen as an outgroup. We selected a total of 228 core genes out of 543 showing no statistically significant recombination among the strains. The ML tree obtained after concatenating those 228 unrecombined core genes showed that C. upsaliensis intersects the C. coli tree between clade 1, and clades 2 and 3 (Figure 3C). Both nodes are well supported with χ2-based parametric branch values of > 99%. In addition, the same topology was inferred by estimating the consensus tree of each of the 228 single gene trees using the extended majority rule method (data not shown), supporting the results obtained with concatenated genes. In fact, the splits ‘clade1a, clade1b / C. upsaliensis, clade 2, clade 3’ and ‘clade1a, clade1b, C. upsaliensis / clade 2, clade 3’ were present in 60.9% and 43.4% of the gene trees, respectively. In contrast, the split ‘clade 2, clade1a, clade1b / C. upsaliensis, clade 3’, which would support the topology of the concatenated unrecombined rps genes proposed by Sheppard et al. [14], was present in only 28% of the gene trees.

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