Quorum sensing gene regulation in Staphylococcus epidermidis reduces the attraction of Aedes aegypti (L.) (Diptera: Culicidae)

Authors: KIM, DONGMIN - Texas A&M University; Crippen, Tawni - Tc; JORDAN, HEATHER - Mississippi State University; TOMBERLIN, JEFFERY - Texas A&M University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/22/2023
Publication Date: 6/22/2023
Citation: Kim, D., Crippen, T.L., Jordan, H., Tomberlin, J.K. 2023. Quorum sensing gene regulation in Staphylococcus epidermidis reduces the attraction of Aedes aegypti (L.) (Diptera: Culicidae). Nature Communications. 14. Article 1208241. https://doi.org/10.3389/fmicb.2023.1208241.
DOI: https://doi.org/10.3389/fmicb.2023.1208241

Interpretive Summary: Bacteria communicate through a chemical process known as quorum sensing to stimulate production of many volatile organic compounds. These chemical discussions occur between bacteria and insects and affect insect behavior. This study is a model interdisciplinary study and the first example providing concrete evidence that crosstalk between bacteria and insects occurs through bacterial quorum sensing pathways and that this crosstalk relies on volatile organic compound production that can be controlled by manipulating the molecules within the pathway. We demonstrate the shifts in insect behavior as a result of bacterial quorum sensing mechanisms. The implications of such a discovery are far reaching and multidisciplinary. Imagine disrupting veterinary or agricultural disease spread, not by the attempted eradication of the insect vector nor by the elimination of pathogenic microorganisms (i.e. Salmonella or E. Coli) or by resistance prone methods (e.g. antimicrobial resistance), but by interrupting the attraction of insect vectors to their host, thereby inhibiting their interaction and possible spread of the disease-causing microbe. This is just one example of its implications. It contributes data of significant research, important to many fields including microbiology, entomology, and vector ecology and provides a framework for future studies to understand the interdependence of microbes, genes, and volatile organic compounds with respect to insect behavior in agricultural issues, such as at livestock and poultry production facilities.

Technical Abstract: Aedes aegypti is a vector of pathogens where transmission leads to many infectious diseases, such as Zika, Dengue, and Yellow Fever. Skin-inhabiting bacteria, such as Staphylococcus epidermidis, produce specific volatile organic compounds (VOCs) which participate in attracting mosquitoes to human hosts. Several studies have investigated microbial VOCs enroute to developing mosquito control methods; however, information about bacterial ecology and its role in mosquito behavior is lacking, specifically, whether bacterial communication through quorum sensing (QS) modulates VOCs production that affects mosquito behavior. This study demonstrated disrupting QS by S. epidermidis with an inhibitor (QSI) reduced the VOCs composition by 35.0% and suppressed mosquito attraction by 55.1%. RNASeq data underscored the regulation of metabolism and stress response of S. epidermidis and resulting protein transport of secondary metabolites potentially leading to altered VOCs production. This interdisciplinary study provides the first evidence of interkingdom crosstalk between bacteria and eukaryotic organisms that can be altered by QS manipulation.