The toxicity of the monoterpenes from lemongrass is mitigated by the detoxifying symbiosis of bacteria and fungi in the tick Haemaphysalis longicornis

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The entry mode of terpenes into the atmosphere is via volatilization of hydrocarbons from foliage over heavily forested areas besides entering the environment through surface water runoff. Some monoterpenes in essential oils are phytotoxins, acting as plant chemical defenses against bacteria or fungi infections and plant-eating insects. For organisms to survive, their enzymatic systems are activated in response to an assault by potentially harmful compounds. Certain bacterial and fungal genera have developed special abilities to transform toxic terpenes into less toxic derivatives. Here, we investigated the response of the bacterial and fungal community in Haemaphysalis longicornis exposed to Cymbopogon citratus (lemongrass) essential oil (EO) and citronellal. Sequencing of bacterial 16S rRNA and fungal ITS1 regions on an Illumina NovaSeq PE250 sequencing platform was performed for H. longicornis tick samples treated with 15 and 20 mg/mL of lemongrass essential oil and citronellal. The diversity recorded in samples treated with C. citratus EO was higher in comparison to those treated with citronellal but significantly lower in the control samples as reflected by the Shannon diversity index. All major H. longicornis bacterial phyla, including Proteobacteria (93.81 %), Firmicutes (2.58 %), and Bacteroidota (0.99 %) were detected. A switch of dominance from Coxiella to Pseudomonas, which has high biotransformation capacity, was observed in the bacterial community, whereas the phylum Ascomycota (Genera: Aspergillus, Archaeorhizomyces, Alternaria, and Candida) dominated in the fungal community indicating detoxifying symbiosis. Other significantly abundant bacterial genera include Ralstonia, Acinetobacter, Vibrio, and Pseudoalteromonas, while Ganoderma and Trichosporon (yeasts) spp. represented the fungi Basidiomycota. This study expanded the understanding of enzymatic modification of phytotoxic substances by microorganisms, which could provide deeper insights into the mitigation of harmful phytotoxins and the synthesis of eco-friendly derivatives for the control of ticks.