Bacterial proximity effects on the transfer of antibiotic resistance genes within the alimentary tract of yellow mealworm larvae

Authors: Crippen, Tawni - Tc; Sullivan, John; Anderson, Robin

Submitted to: Journal of Economic Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2024
Publication Date: 2/27/2024
Citation: Crippen, T.L., Sullivan, J.P., Anderson, R.C. 2024. Bacterial proximity effects on the transfer of antibiotic resistance genes within the alimentary tract of yellow mealworm larvae. Journal of Economic Entomology. 117(2):417-426. https://doi.org/10.1093/jee/toae019.
DOI: https://doi.org/10.1093/jee/toae019

Interpretive Summary: The USDA is now engaged in research within the edible insect agriculture industry. Research into the food and feed safety aspects of this industry is in its infancy. One of the major insects used in this industry is the yellow mealworm. The intestinal tract and other anatomical parts of the yellow mealworm naturally carry microorganisms. Some of these are pathogens, secrete toxins, or carry transferable antibiotic resistance genes. The risks associated with these edible insects are dependent on these naturally occurring bacteria, as well as on the bacteria inadvertently introduced during mass production. During production, individual insects are in high density which increases the possibility of their exposure to other insects which may be carrying antibiotic resistant bacteria. The purpose of this study was to determine if the gut of the yellow mealworm permitted antibiotic resistance gene transfer between pathogenic bacteria. We determined that the nutrient rich environment of the yellow mealworm gut provided favorable conditions for the transfer of antibiotic resistance genes that corresponded to the number of bacteria to which the insect was exposed. While many other factors can affect this transfer, the simple factor of the proximity of bacteria, as defined by the concentration of bacteria and the volume of the insect gut, appeared to have contributed to the efficiency of antibiotic gene transfer.

Technical Abstract: The arthropod intestinal tract and other anatomical parts naturally carry microorganisms. Some of these are pathogens, secrete toxins, or carry transferable antibiotic resistance genes. The risks associated with the production and consumption of edible arthropods are dependent on indigenous microbes and microbes introduced during rearing. This mass arthropod production puts individual arthropods in close proximity which increases the possibility of their exposure to antibiotic resistant bacteria carried by other insects, workers, or rearing feed and substrates. The purpose of this study was to determine if the alimentary tract of the yellow mealworm provided an environment permitting horizontal gene transfer between bacteria. The effect of the concentration of bacterial exposure was also assessed. Antibiotic resistance gene horizontal conjugation frequencies between Salmonella and Escherichia coli within the larval gut demonstrated a concentration gradient effect on transconjugant production. The nutrient rich environment of the yellow mealworm gut provided favorable conditions for the transfer of antibiotic resistance genes which equated to filter mating controls at the higher bacterial exposure levels. However, a lower level of exposure concentration, 10**3 cfu/cm**2, required enrichment to measure and thus may have been approaching a threshold level for proximity of the location of the two bacteria within the larval gut. While many other factors can affect this transfer, the simple factor of the proximity of donor and recipient bacteria, as defined by the concentration of bacteria and the volume of the insect gut appeared to have contributed to the efficiency of antibiotic gene transfer.