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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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Bayesian phylogeny of GT42 sialyltransferases indicating relatedness of C. jejuni and C. coli sialyltransferases.C. coli cst-I is found in the capsule (CPS) locus of C. coli clade 3 strains and is an ortholog of C. jejuni cst-I. C. coli cst-IV is found in the lipooligosaccharide (LOS) locus of C. coli clade 1 strains and C. coli cst-V is found in the LOS locus of C. coli clade 3 strains.
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Figure 6: Bayesian phylogeny of GT42 sialyltransferases indicating relatedness of C. jejuni and C. coli sialyltransferases.C. coli cst-I is found in the capsule (CPS) locus of C. coli clade 3 strains and is an ortholog of C. jejuni cst-I. C. coli cst-IV is found in the lipooligosaccharide (LOS) locus of C. coli clade 1 strains and C. coli cst-V is found in the LOS locus of C. coli clade 3 strains.

Mentions: No evidence has been found of the presence of the neuABC gene cluster in the LOS locus of any of the 42 C. coli strains analyzed in a previous study [72], although it was evident in the CPS locus classes VII and VIII [72]. However, the authors found the presence of a putative sialyltransferase (named 1501) in two LOS classes of C. coli (class B and C). In our MCL cluster analysis we found that the putative C. coli 76339 sialyltransferase BN865_09900 belongs to GO-CCO2667 which includes several other sequences from both C. coli clade 1 and 3. All the sequences of GO-CCO2667, showed a significant homology to those belonging to the CAZy glycosyltransferase family GT42, supporting the idea that all encode putative sialyltransferases [32]. Further analysis revealed that the clade 1 GO-CCO2667 sequences corresponded to sialyltransferase 1501 identified by Richards et al. [72]. Additionally, C. coli 76339 possesses a second sialyltransferase (BN865_06990), which was found to be located in the CPS locus of the strain and to have an ortholog in other clade 3 strains. This protein gave no significant BLASTP hits with other C. coli sequences (BSR cut off 0.4), but it showed 67% identity with C. jejuni ATCC 43456 Cst-I. To elucidate the phylogenetic relationship among Campylobacter sialyltransferases we inferred the phylogeny of GT42 sequences by applying Bayesian methodology (Figure 6). The LOS-associated C. coli sialyltranferases were shown to be monophyletic and distantly related to C. jejuni sialyltransferases. We propose to name these genes Cst-IV (clade 1) and Cst-V (clade 3). The distant relationship observed between LOS-associated C. coli and C. jejuni sialyltransferases could indicate evolution of different substrate specificity, which has been previously observed among Helicobacter sialyltransferases [52]. As a consequence, these bacteria may express different sialylated structures on their LOS. On the contrary, the C. coli clade 3 sialyltransferases located within the capsule locus clustered tightly together with C. jejuni Cst-I, which supports the notion of interspecies HGT and the potential of sharing similar sialylated glycan structures on the surface.


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)

Bayesian phylogeny of GT42 sialyltransferases indicating relatedness of C. jejuni and C. coli sialyltransferases.C. coli cst-I is found in the capsule (CPS) locus of C. coli clade 3 strains and is an ortholog of C. jejuni cst-I. C. coli cst-IV is found in the lipooligosaccharide (LOS) locus of C. coli clade 1 strains and C. coli cst-V is found in the LOS locus of C. coli clade 3 strains.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Bayesian phylogeny of GT42 sialyltransferases indicating relatedness of C. jejuni and C. coli sialyltransferases.C. coli cst-I is found in the capsule (CPS) locus of C. coli clade 3 strains and is an ortholog of C. jejuni cst-I. C. coli cst-IV is found in the lipooligosaccharide (LOS) locus of C. coli clade 1 strains and C. coli cst-V is found in the LOS locus of C. coli clade 3 strains.
Mentions: No evidence has been found of the presence of the neuABC gene cluster in the LOS locus of any of the 42 C. coli strains analyzed in a previous study [72], although it was evident in the CPS locus classes VII and VIII [72]. However, the authors found the presence of a putative sialyltransferase (named 1501) in two LOS classes of C. coli (class B and C). In our MCL cluster analysis we found that the putative C. coli 76339 sialyltransferase BN865_09900 belongs to GO-CCO2667 which includes several other sequences from both C. coli clade 1 and 3. All the sequences of GO-CCO2667, showed a significant homology to those belonging to the CAZy glycosyltransferase family GT42, supporting the idea that all encode putative sialyltransferases [32]. Further analysis revealed that the clade 1 GO-CCO2667 sequences corresponded to sialyltransferase 1501 identified by Richards et al. [72]. Additionally, C. coli 76339 possesses a second sialyltransferase (BN865_06990), which was found to be located in the CPS locus of the strain and to have an ortholog in other clade 3 strains. This protein gave no significant BLASTP hits with other C. coli sequences (BSR cut off 0.4), but it showed 67% identity with C. jejuni ATCC 43456 Cst-I. To elucidate the phylogenetic relationship among Campylobacter sialyltransferases we inferred the phylogeny of GT42 sequences by applying Bayesian methodology (Figure 6). The LOS-associated C. coli sialyltranferases were shown to be monophyletic and distantly related to C. jejuni sialyltransferases. We propose to name these genes Cst-IV (clade 1) and Cst-V (clade 3). The distant relationship observed between LOS-associated C. coli and C. jejuni sialyltransferases could indicate evolution of different substrate specificity, which has been previously observed among Helicobacter sialyltransferases [52]. As a consequence, these bacteria may express different sialylated structures on their LOS. On the contrary, the C. coli clade 3 sialyltransferases located within the capsule locus clustered tightly together with C. jejuni Cst-I, which supports the notion of interspecies HGT and the potential of sharing similar sialylated glycan structures on the surface.

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