Pan-Genome Analysis of Campylobacter: Insights on the Genomic Diversity and Virulence Profile

Zhong, Chunrong; Qu, Bingpeng; Hu, Gang; Ning, Kang

doi:10.1128/spectrum.01029-22

Cited by 12 publications

(14 citation statements)

References 65 publications

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“…Using the Campylobacter genus core genome, we derived a core genome phylogeny for classifying Campylobacter isolates. The delineation of species on the core genome phylogenetic tree is consistent in many instances with previous studies, as closely related Campylobacter species in established groups can be found within the same major clades of the phylogenetic tree ( 13 , 14 , 40 , 43 , 49 – 51 ). With the rapid expansion of the Campylobacter genomes and additional diversity from new genomes sequenced, it is inevitable that new Campylobacter genomes may not be assignable to an established species or may be inconsistent with traditional species.…”

Section: Discussionsupporting

confidence: 88%

Uncovering the boundaries of Campylobacter species through large-scale phylogenetic and nucleotide identity analyses

Wu,

Payne,

Zhang

et al. 2024

mSystems

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Campylobacter species are typically helical shaped, Gram-negative, and non-spore-forming bacteria. Species in this genus include established foodborne and animal pathogens as well as emerging pathogens. The accumulation of genomic data from the Campylobacter genus has increased exponentially in recent years, accompanied by the discovery of putative new species. At present, the lack of a standardized species boundary complicates distinguishing established and novel species. We defined the Campylobacter genus core genome (500 loci) using publicly available Campylobacter complete genomes ( n = 498) and constructed a core genome phylogeny using 2,193 publicly available Campylobacter genomes to examine inter-species diversity and species boundaries. Utilizing 8,440 Campylobacter genomes representing 33 species and 8 subspecies, we found species delineation based on an average nucleotide identity (ANI) cutoff of 94.2% is consistent with the core genome phylogeny. We identified 60 ANI genomic species that delineated Campylobacter species in concordance with previous comparative genetic studies. All pairwise ANI genomic species pairs had in silico DNA-DNA hybridization scores of less than 70%, supporting their delineation as separate species. We provide the tool Campylobacter Genomic Species typer (CampyGStyper) that assigns ANI genomic species to query genomes based on ANI similarities to medoid genomes from each ANI genomic species with an accuracy of 99.96%. The ANI genomic species definitions proposed here allow consistent species definition in the Campylobacter genus and will facilitate the detection of novel species in the future. IMPORTANCE In recent years, Campylobacter has gained recognition as the leading cause of bacterial gastroenteritis worldwide, leading to a substantial rise in the collection of genomic data of the Campylobacter genus in public databases. Currently, a standardized Campylobacter species boundary at the genomic level is absent, leading to challenges in detecting emerging pathogens and defining putative novel species within this genus. We used a comprehensive representation of genomes of the Campylobacter genus to construct a core genome phylogenetic tree. Furthermore, we found an average nucleotide identity (ANI) of 94.2% as the optimal cutoff to define the Campylobacter species. Using this cutoff, we identified 60 ANI genomic species which provided a standardized species definition and nomenclature. Importantly, we have developed Campylobacter Genomic Species typer (CampyGStyper), which can robustly and accurately assign these ANI genomic species to Campylobacter genomes, thereby aiding pathogen surveillance and facilitating evolutionary and epidemiological studies of existing and emerging pathogens in the genus Campylobacter .

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Section: Discussionsupporting

confidence: 88%

Uncovering the boundaries of Campylobacter species through large-scale phylogenetic and nucleotide identity analyses

Wu,

Payne,

Zhang

et al. 2024

mSystems

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“…Previous attempts to delete htrB in C. jejuni have failed, further supporting its essentiality [ 76 ]. Zhong et al interestingly highlighted the gene htrB as a core virulence gene across 39 representative Campylobacter species [ 77 ]. The other core virulence genes that they found were porA, PEB4, cheY, Cj1135 and kspF.…”

Section: Resultsmentioning

confidence: 99%

“…Interestingly, htrB and PEB4 which have been found to be core virulence genes across Campylobacter spp. are essential and therefore would warrant further investigation [ 77 ]. The core essential gene list produced indicates that there are many essential genes that are critical to the fitness and/or survival of Campylobacter but have a hypothetical/unknown function.…”

Section: Discussionmentioning

confidence: 99%

Application of TraDIS to define the core essential genome of Campylobacter jejuni and Campylobacter coli

et al. 2023

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Campylobacter species are the major cause of bacterial gastroenteritis. As there is no effective vaccine, combined with the rapid increase in antimicrobial resistant strains, there is a need to identify new targets for intervention. Essential genes are those that are necessary for growth and/or survival, making these attractive targets. In this study, comprehensive transposon mutant libraries were created in six C. jejuni strains, four C. coli strains and one C. lari and C. hyointestinalis strain, allowing for those genes that cannot tolerate a transposon insertion being called as essential. Comparison of essential gene lists using core genome analysis can highlight those genes which are common across multiple strains and/or species. Comparison of C. jejuni and C. coli, the two species that cause the most disease, identified 316 essential genes. Genes of interest highlighted members of the purine pathway being essential for C. jejuni whilst also finding that a functional potassium uptake system is essential. Protein–protein interaction networks using these essential gene lists also highlighted proteins in the purine pathway being major ‘hub’ proteins which have a large number of interactors across the network. When adding in two more species (C. lari and C. hyointestinalis) the essential gene list reduces to 261. Within these 261 essential genes, there are many genes that have been found to be essential in other bacteria. These include htrB and PEB4, which have previously been found as core virulence genes across Campylobacter species in other studies. There were 21 genes which have no known function with eight of these being associated with the membrane. These surface-associated essential genes may provide attractive targets. The essential gene lists presented will help to prioritise targets for the development of novel therapeutic and preventative interventions.

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“…play a crucial role in advancing our knowledge of the dynamics and characteristics of circulating lineage clusters. A high genetic diversity of C. jejuni strains has been extensively documented worldwide and possesses a notable capacity for genetic exchange, enhancing its adaptability ( Golz et al, 2020 ; Bravo et al, 2021 ; Harrison et al, 2021 ; Ocejo et al, 2021 ; Prendergast et al, 2022 ; Zhong et al, 2022 ; Hull et al, 2023 ). Notably, extensive introgression (transfer of genetic material between different species), predominantly from C. jejuni to C. coli, has been observed, resulting in the replacement of approximately 10 and 23% of the C. coli core genome with C. jejuni DNA in ST-828 and ST-1150 CCs, respectively ( Sheppard et al, 2008 ; Tanoeiro et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…A recent study on the genomic diversity and virulence profile of the genus Campylobacter demonstrated that the number of genes has undergone expansion or contraction during the evolution of different Campylobacter species ( Zhong et al, 2022 ). VFDB analysis revealed that many strains (75 out of 131) carried virulence genes associated with bacterial species other than Campylobacter spp., suggesting potential gene transfer events between different bacterial species.…”

Section: Discussionmentioning

confidence: 99%

Antibiotic resistance, plasmids, and virulence-associated markers in human strains of Campylobacter jejuni and Campylobacter coli isolated in Italy

Garcia-Fernandez,

Janowicz,

Marotta

et al. 2024

Front. Microbiol.

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Campylobacteriosis, a prevalent foodborne gastrointestinal infection in Europe, is primarily caused by Campylobacter jejuni and Campylobacter coli, with rising global concerns over antimicrobial resistance in these species. This study comprehensively investigates 133 human-origin Campylobacter spp. strains (102 C. jejuni and 31 C. coli) collected in Italy from 2013 to 2021. The predominant Multilocus Sequence Typing Clonal complexes (CCs) were ST-21 CC and ST-206 CC in C. jejuni and ST-828 CC in C. coli. Ciprofloxacin and tetracycline resistance, mainly attributed to GyrA (T86I) mutation and tet(O) presence, were prevalent, while erythromycin resistance was associated with 23S rRNA gene mutation (A2075G), particularly in C. coli exhibiting multidrug-resistant pattern CipTE. Notable disparities in virulence factors among strains were observed, with C. jejuni exhibiting a higher abundance compared to C. coli. Notably, specific C. jejuni sequence types, including ST-21, ST-5018, and ST-1263, demonstrated significantly elevated counts of virulence genes. This finding underscores the significance of considering both the species and strain-level variations in virulence factor profiles, shedding light on potential differences in the pathogenicity and clinical outcomes associated with distinct C. jejuni lineages. Campylobacter spp. plasmids were classified into three groups comprising pVir-like and pTet-like plasmids families, exhibiting diversity among Campylobacter spp. The study underscores the importance of early detection through Whole Genome Sequencing to identify potential emergent virulence, resistance/virulence plasmids, and new antimicrobial resistance markers. This approach provides actionable public health data, supporting the development of robust surveillance programs in Italy.

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Pan-Genome Analysis of Campylobacter: Insights on the Genomic Diversity and Virulence Profile

Cited by 12 publications

References 65 publications

Uncovering the boundaries of Campylobacter species through large-scale phylogenetic and nucleotide identity analyses

Uncovering the boundaries of Campylobacter species through large-scale phylogenetic and nucleotide identity analyses

Application of TraDIS to define the core essential genome of Campylobacter jejuni and Campylobacter coli

Antibiotic resistance, plasmids, and virulence-associated markers in human strains of Campylobacter jejuni and Campylobacter coli isolated in Italy

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