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The deposited data is part of Hepner, S., Kuleshov, K., Tooming-Kunderud, A. et al. A high fidelity approach to assembling the complex Borrelia genome. BMC Genomics 24, 401 (2023). https://doi.org/10.1186/s12864-023-09500-4 Alignment of PFam32 nucleotide sequences (including pseudogenes) of the plasmids (Hepner_et_al_2023_PFam32_ClustalW_alignment.fasta) and maximum-likelihood tree (Hepner_et_al_2023_PFam32_phylogenetic_tree.nwk, Hepner_et_al_2023_PFam32_phylogenetic_tree.nwk.pdf).

Additional file 1: Table S1. QUAST and Merqury results. Table S2. Detailed information about assembly results after genome reconstruction of PBaeII, PBes and 89B13. Table S3. Summary of mapping statistics of PBaeII. Table S4. Mapping statistics for single genome elements of PBaeII. Table S5. List and characteristics of all isolates. Figures S1-S3. Dot plots B. bavariensis PBaeII. Figure S4. Dot plots B. garinii PBes, lp32-10, microbial assembler. Figure S5. Dot plot B. valaisiana 89B13, lp32-7, IPA. Figure S6. Dot plot B. valaisiana 89B13, lp25, microbial_circulomics. Figure S7. Mapping graphs of B. bavariensis PBaeII.

Campylobacter is among the most common causes of gastroenteritis worldwide. Campylobacter jejuni and Campylobacter coli are the most common species causing human-disease. DNA-sequence-based methods for strain characterization have focussed largely on C. jejuni, responsible for 80-90% of infections, meaning that C. coli epidemiology has lagged behind. Here we have analyzed the genome of 450 C. coli isolates to determine genetic markers that can discriminate isolates sampled from 3 major reservoir hosts (chickens, cattle and pigs). These markers were then applied to identify the source of infection of 147 C. coli from French clinical cases. Using STRUCTURE software, 259 potential host-segregating markers were revealed by probabilistic characterization of SNP frequency variation in strain collections from three different hosts. These SNPs were found in 41 genes or intergenic regions, mostly coding for proteins involved in motility and membrane functions. Source attribution of clinical isolates based on the differential presence of these markers confirmed chicken as the most common source of C. coli infection in France.

International audience; Campylobacter is among the most common causes of gastroenteritis worldwide. Campylobacter jejuni and Campylobacter coli are the most common species causing human-disease. DNA-sequence-based methods for strain characterization have focussed largely on C. jejuni, responsible for 80-90% of infections, meaning that C. coli epidemiology has lagged behind. Here we have analyzed the genome of 450 C. coli isolates to determine genetic markers that can discriminate isolates sampled from 3 major reservoir hosts (chickens, cattle and pigs). These markers were then applied to identify the source of infection of 147 C. coli from French clinical cases. Using STRUCTURE software, 259 potential host-segregating markers were revealed by probabilistic characterization of SNP frequency variation in strain collections from three different hosts. These SNPs were found in 41 genes or intergenic regions, mostly coding for proteins involved in motility and membrane functions. Source attribution of clinical isolates based on the differential presence of these markers confirmed chicken as the most common source of C. coli infection in France.IMPORTANCE Genome-wide and source attribution studies based on Campylobacter species have shown their importance for the understanding of foodborne infections. Although the use of MLST based on 7 genes from C. jejuni is a powerful method to structure populations, when applied to C. coli results have not clearly demonstrated their robustness. Therefore, we aim here to provide more accurate data based on the identification of single-nucleotide polymorphisms. Results from this study reveal an important number of host-segregating SNPs, found in proteins implied in motility, membrane functions or DNA repair systems. These findings offer new interesting opportunities for further study on C. coli adaptation to its environment. Additionally, the results demonstrate that poultry is potentially the main reservoir of C. coli in France.

Human infection with the gastrointestinal pathogen Campylobacter jejuni is dependent upon the opportunity for zoonotic transmission and the ability of strains to colonize the human host. Certain lineages of this diverse organism are more common in human infection but the factors underlying this overrepresentation are not fully understood. We analyzed 601 isolate genomes from agricultural animals and human clinical cases, including isolates from the multihost (ecological generalist) ST-21 and ST-45 clonal complexes (CCs). Combined nucleotide and amino acid sequence analysis identified 12 human-only amino acid KPAX clusters among polyphyletic lineages within the common disease causing CC21 group isolates, with no such clusters among CC45 isolates. Isolate sequence types within human-only CC21 group KPAX clusters have been sampled from other hosts, including poultry, so rather than representing unsampled reservoir hosts, the increase in relative frequency in human infection potentially reflects a genetic bottleneck at the point of human infection. Consistent with this, sequence enrichment analysis identified nucleotide variation in genes with putative functions related to human colonization and pathogenesis, in human-only clusters. Furthermore, the tight clustering and polyphyly of human-only lineage clusters within a single CC suggest the repeated evolution of human association through acquisition of genetic elements within this complex. Taken together, combined nucleotide and amino acid analysis of large isolate collections may provide clues about human niche tropism and the nature of the forces that promote the emergence of clinically important C. jejuni lineages.

Significance Human activities have had a profound effect on the Earth’s ecosystems and biodiversity. This is evident among livestock species, such as cattle, that now constitute more biomass than all wild mammals combined. For bacteria living within these animals, this massive host expansion represents an opportunity to proliferate and spread globally through trade networks. This carries significant risks as pathogenic species can potentially spread to humans, but little is known about how these zoonotic bacteria evolve to exploit the changing host niche space. Here, we explain the nature and timescale of cattle adaptation in the world’s most common enteric bacterial pathogen (Campylobacter jejuni), highlighting potential risks of intensive livestock production in pathogen emergence., Modern agriculture has dramatically changed the distribution of animal species on Earth. Changes to host ecology have a major impact on the microbiota, potentially increasing the risk of zoonotic pathogens being transmitted to humans, but the impact of intensive livestock production on host-associated bacteria has rarely been studied. Here, we use large isolate collections and comparative genomics techniques, linked to phenotype studies, to understand the timescale and genomic adaptations associated with the proliferation of the most common food-born bacterial pathogen (Campylobacter jejuni) in the most prolific agricultural mammal (cattle). Our findings reveal the emergence of cattle specialist C. jejuni lineages from a background of host generalist strains that coincided with the dramatic rise in cattle numbers in the 20th century. Cattle adaptation was associated with horizontal gene transfer and significant gene gain and loss. This may be related to differences in host diet, anatomy, and physiology, leading to the proliferation of globally disseminated cattle specialists of major public health importance. This work highlights how genomic plasticity can allow important zoonotic pathogens to exploit altered niches in the face of anthropogenic change and provides information for mitigating some of the risks posed by modern agricultural systems.