Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance to Salmonella in chickens.

Authors: Oladeinde, Adelumola - Ade; ABDO, ZAID - Colorado State University; ZWIRZITZ, BENJAMIN - University Of Veterinary Medicine; WOYDA, REED - Colorado State University; LAKIN, STEVEN - Colorado State University; PRESS, MAXIMILIAN - Phase Genomics, Inc; Cook, Kimberly - Kim; Cox Jr, Nelson; THOMAS, JESSE - Centers For Disease Control And Prevention (CDC) - United States; Looft, Torey; Rothrock, Michael; ZOCK, GREGORY - University Of Georgia; Plumblee Lawrence, Jodie; Cudnik, Denice; RITZ, CASEY - University Of Georgia

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2022
Publication Date: 4/13/2022
Citation: Oladeinde, A.A., Abdo, Z., Zwirzitz, B., Woyda, R., Lakin, S.M., Press, M.O., Cook, K.L., Cox Jr, N.A., Thomas, J.C., Looft, T.P., Rothrock Jr, M.J., Zock, G.S., Plumblee Lawrence, J.R., Cudnik, D., Ritz, C. 2022. Litter commensal bacteria can limit the horizontal gene transfer of antimicrobial resistance to Salmonella in chickens. Applied and Environmental Microbiology.88(9). https://doi.org/10.1128/aem.02517-21

Interpretive Summary: Antimicrobial resistance spread is a worldwide health challenge, stemming in large part, from the ability of microorganisms to share their genetic material through horizontal gene transfer. To address this issue, many countries and international organization have adopted a one health approach to curtail the proliferation of antibiotic resistant bacteria. This includes the removal and reduction of antibiotics used in food animal production and the development of alternatives to antibiotics. However, there is still a significant knowledge gap in our understanding of how antimicrobial resistance spreads in the absence of antibiotic selection and the role commensal bacteria play in reducing antibiotic resistance transfer. In this study, we show that commensal bacterial populations from reused broiler chicken litter provided colonization resistance against the transfer of multidrug resistant plasmid to Salmonella. In addition, we provide the identity of the bacterial species that perform this function in broiler chickens and determined the metabolic pathways used by these microbes.

Technical Abstract: Host microbiome homeostasis ensures that gut conditions are unfavorable to an invading pathogen such as Salmonella enterica. Consequently, fostering a “balanced” gut microbiome through the administration of microbes that can competitively exclude pathogens has gained a lot of attention and use in human and animal medicine. However, little is known on how competitive exclusion affects the transfer of antibiotic resistance. To shed more light on this question, we challenged neonatal broiler chicks raised on reused broiler chicken litter – a complex environment comprising of decomposing pine shavings, feces, uric acid, feathers, and feed, with Salmonella Heidelberg (S. Heidelberg), a model pathogen. We show that chicks raised on reused litter carried lower abundance of Salmonella and harbored a more uniform and diverse microbiome comprising of bacterial species that are known to provide colonization resistance towards Salmonella compared to chicks raised on fresh bedding composed of pine shavings. Additionally, these bacterial species were associated with a lower horizontal transfer of multidrug resistance genes to S. Heidelberg. Using in vitro competition experiments, we confirmed that conjugation between S. Heidelberg and E. coli strains from chicks raised on fresh litter resulted in the acquisition of multidrug resistant plasmids. Contrastingly, bacteriophage-mediated recombination between S. Heidelberg and E. coli strains made the acquisition of plasmid-mediated ß-lactamase gene (blaCMY-2) possible. Collectively, this study demonstrates that competitive exclusion can reduce the transfer of antibiotic resistance and provides information on the bacterial species that can be explored for their benefits to reduce antibiotic resistance transfer.