Behavioral interplay between mosquito and mycolactone produced by Mycobacterium ulcerans and bacterial gene expression induced by mosquito proximity

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

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/25/2023
Publication Date: 8/3/2023
Citation: Kim, D., Crippen, T.L., Jordan, H.R., Tomberlin, J.K. 2023. Behavioral interplay between mosquito and mycolactone produced by Mycobacterium ulcerans and bacterial gene expression induced by mosquito proximity. PLOS ONE. 18(8). Article e0289768. https://doi.org/10.1371/journal.pone.0289768.
DOI: https://doi.org/10.1371/journal.pone.0289768

Interpretive Summary: Mosquitoes blood-feeding on animals can result in transmission of pathogens, through causing livestock diseases or resulting in livestock as a reservoir of pathogens that affect other animals. Additionally, mosquitoes are an annoyance to livestock where the pain of blood-feeding may increase stress reducing livestock fitness, weight gain, and animal welfare. The environmental cues that cause attraction of mosquitoes to a blood-feeding source were explored in this study. In this model a toxin, mycolactone, produced by a bacterium, Mycobacterium ulcerans, was evaluated as the potential cause of attraction of mosquitoes to blood-feeding sources and to sites to lay eggs. Overall, the bacteria which produced the toxin induced a greater attractive response from the mosquitoes than an artificially mutated bacteria that could not produce the toxin. These data provide insight into the environmental pathways between bacteria and insects that could be used to control disease prevalence and pathogen dispersal.

Technical Abstract: Mycolactone produced by the environmental pathogen Mycobacterium ulcerans functions as a cue, or potentially an interkingdom signal, for mosquitoes to locate hosts and oviposition sites. Little is known about the mosquitoes' responses to M. ulcerans. A triple-choice assay was conducted to determine the host-seeking preference of Ae. aegypti to M. ulcerans wildtype (MU, mycolactone active) and mutant (MU**lac-, mycolactone inactive). Results demonstrated mosquito attraction to a blood-meal treated with M. ulcerans wildtype was 126.0% and 171.0% greater than M. ulcerans mutant and control, respectively. The differential MU and MU**lac- volatile organic compound profiles were measured using GC-MS analysis, implicating a wide range of possible biological interactions from quorum sensing to odor profiles. Additionally, we evaluated the interplay between Ae. aegypti proximity and M. ulcerans mRNA expression. Transcripotme data showed significant differential gene expressions between MU and MU**lac- that were either in contact with Ae. aegypti or only in near proximity. This study is the first to link mycolactone as a cue regulating interkingdom interactions between M. ulcerans and Aedes aegypti and provides insight as to possible ecological pathways between these two that could be used to mitigate disease prevelence and pathogen dispersal.