Genomic Relatedness, Antibiotic Resistance and Virulence Traits of Campylobacter jejuni HS19 Isolates From Cattle in China Indicate Pathogenic Potential.

Xiaoqi Zang,Jie Li,Jinlin Huang,Pingyu Huang,Xinan Jiao

doi:10.3389/fmicb.2021.783750

Abstract

Although campylobacteriosis is a zoonotic foodborne illness, high-risk isolates from animal sources are rarely characterized, and the pathogenic potential of zoonotic strains remains an obstacle to effective intervention against human infection. HS19 has been acknowledged as a maker serotype represented by Campylobacter jejuni (C. jejuni) isolates from patients with post-infection Guillain-Barré syndrome (GBS), which is circulation in developed countries. However, a previous serotype epidemiological study of C. jejuni isolates in an animal population revealed that HS19 was also prevalent in isolates from cattle in China. In this study, to investigate the hazardous potential of zoonotic strains, 14 HS19 isolates from cattle were systematically characterized both by genotype and phenotype. The results showed that all of these cattle isolates belonged to the ST-22 complex, a high-risk lineage represented by 77.2% HS19 clinical isolates from patients worldwide in the PubMLST database, indicating that the ST-22 complex is the prominent clonal complex of HS19 isolates, as well as the possibility of clonal spread of HS19 isolates across different regions and hosts. Nevertheless, these cattle strains clustered closely with the HS19 isolates from patients, suggesting a remarkable phylogenetic relatedness and genomic similarity. Importantly, both tetracycline genes tet(O) and gyrA (T86I) reached a higher proportional representation among the cattle isolates than among the human clinical isolates. A worrying level of multidrug resistance (MDR) was observed in all the cattle isolates, and two MDR profiles of the cattle isolates also existed in human clinical isolates. Notably, although shared with the same serotype HS19 and sequence type ST-22, 35.7% of cattle isolates induced severe gastrointestinal pathology in the IL-10–/– C57BL/6 mice model, indicating that some bacteria could change due to host adaptation to induce a disease epidemic, thus the associated genetic elements deserve further investigation. In this study, HS19 isolates from cattle were first characterized by a systematic evaluation of bacterial genomics and in vitro virulence, which improved our understanding of the potential zoonotic hazard from food animal isolates with high-risk serotypes, and provided critical information for the development of targeted C. jejuni mitigation strategies.

Highlights

Campylobacter jejuni is the leading cause of bacterial foodborne gastroenteritis in humans, both in developed and developing countries (Ruiz-Palacios, 2007; Kaakoush et al, 2015), making it a great threat to the public’s health
CC22 accounted for 86.6% (n = 13) of Guillain-Barré syndrome (GBS) isolates, which were mainly sampled from the Netherlands (38.4%, n = 5), followed by Japan (23.0%, n = 3), China (15.3%, n = 2), United States (15.3%, n = 2), and Mexico (7.6%, n = 1)
Infection of HS19 isolates often increases the risk of developing GBS (Nachamkin et al, 1998), while HS19 isolates are present in the diarrhea populations circulating in various countries

Summary

Introduction

Campylobacter jejuni is the leading cause of bacterial foodborne gastroenteritis in humans, both in developed and developing countries (Ruiz-Palacios, 2007; Kaakoush et al, 2015), making it a great threat to the public’s health. The high incidence of C. jejuni-associated disease in humans is largely due to its prevalence as a zoonotic agent in animals (Sheppard et al, 2011; Burnham and Hendrixson, 2018). Significant associations emerged between certain clonal complexes from human infection and the contact with cattle, the consumption of unpasteurized milk and raw minced meat, raising the question about the pathogenic potential of cattle isolates (Kärenlampi et al, 2007; Wilson et al, 2008; Costard et al, 2017; Hsu et al, 2020). Not all strains or genetic lineages pose equal risks to human health. Campylobacteriosis is a zoonotic foodborne disease, the majority of the reported highrisk strains were from clinical patients, and isolates from animal sources have rarely been characterized

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