Differences in the propensity of different antimicrobial resistance determinants to be disseminated via transformation in Campylobacter jejuni and Campylobacter coli

Authors: HANAFY, ZAHRA - North Carolina State University; OSBORNE, JASON - North Carolina State University; Miller, William - Bill; Parker, Craig; OLSON, JONATHAN - North Carolina State University; JACKSON III, JAMES - North Carolina State University; KATHARIOU, SOPHIA - North Carolina State University

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2022
Publication Date: 6/10/2022
Citation: Hanafy, Z., Osborne, J.A., Miller, W.G., Parker, C.T., Olson, J.W., Jackson III, J.H., Kathariou, S. 2022. Differences in the propensity of different antimicrobial resistance determinants to be disseminated via transformation in Campylobacter jejuni and Campylobacter coli. Microorganisms. 10(6). Article 1194. https://doi.org/10.3390/microorganisms10061194.
DOI: https://doi.org/10.3390/microorganisms10061194

Interpretive Summary: Campylobacter jejuni and Campylobacter coli are foodborne bacterial pathogens commonly associated with poultry. Antibiotics used to treat human Campylobacter infections include erythromycin and also fluoroquinolones, such as nalidixic acid and ciprofloxacin. Drug resistance can be transferred between Campylobacter strains by one of two methods: incorporation of chromosomal DNA fragments containing the resistance determinant into a drug-sensitive strain or passage of extrachromosomal DNA elements from resistant strains to sensitive strains. This study measured the ability of resistant Campylobacter strains to transform sensitive strains. Transformation frequencies were highest for nalidixic acid, streptomycin and gentamicin (although gentamicin transformation was strain-dependent) with tetracycline resistance less commonly transferred. This study provides further insights on antibiotic resistance within Campylobacter strains of poultry origin.

Technical Abstract: Campylobacter jejuni and Campylobacter coli are leading zoonotic foodborne bacterial pathogens and the drugs of choice for human campylobacteriosis are macrolides such as erythromycin and fluoroquinolones. However, increasing antimicrobial resistance (AMR) in Campylobacter can compromise treatment efficacy. C. jejuni and C. coli are naturally competent for transformation via naked DNA uptake, but potential differences in the propensity of different AMR determinants to be disseminated via transformation remain poorly understood. We investigated the transformation frequency for resistance to different antibiotics, i.e., nalidixic acid, gentamicin, streptomycin, erythromycin, and tetracycline. We used a derivative of C. jejuni NCTC 11168 (strain SN:CM) as recipient with donor DNA from C. jejuni or C. coli resistant to multiple antimicrobial classes. Transformation frequency for nalidixic acid resistance was significantly the highest (~1.4x10-3), followed by resistance to streptomycin and gentamicin. Tetracycline resistance via chromosomal tet(O) was less commonly transferred (~7.6x10-7) while transformation to erythromycin resistance was rarely encountered (= 4.7x10-8). To determine whether similar trends occurred in contemporary poultry-derived Campylobacter strains, we examined C. jejuni FSIS 11810577 and C. coli FSIS 1710488 as recipients. Transformation frequencies to nalidixic acid and streptomycin resistance remained the highest (~7x 10-4). However, transfer of gentamicin resistance was remarkably inefficient in certain recipient-donor combinations and average erythromycin resistance transfer for these FSIS recipients were noticeably higher (~3x10-6) than observed with SN:CM. Findings from this experimental model provide insights on factors that may impact transformation-mediated transfer of AMR in food, animals or the environment, leading to dissemination of antibiotic resistance in the agricultural ecosystem.