Rectal bacteria produce sex pheromones in the male oriental fruit fly

Abstract

In recent decades, a growing body of literature has indicated that microbial symbionts of insects can modulate their hosts’ chemical profiles and mate choice decisions. However, there is currently little direct evidence indicate that insect pheromones can be produced by symbionts. Using Bactrocera dorsalis as a model system, we demonstrate that Bacillus sp. in the rectum of male B. dorsalis plays a pivotal role in sex pheromones production. We demonstrate that 2,3,5-trimethylpyrazine (TMP) and 2,3,5,6-tetramethylpyrazine (TTMP) are sex pheromones produced in the male rectums. Mature virgin females can be strongly attracted by TMP and TTMP. TMP and TTMP contents in male rectums can be decreased when rectal bacteria are inhibited with antibiotics. Moreover, Bacillus sp. isolated from male rectum can produce TMP and TTMP when providing with substrates-glucose and threonine, for which the contents are significantly higher in rectums of mature males. These findings highlight the influence of microbial symbionts on insect pheromones and provide an example of direct bacterial production of pheromones in insects.

From Insect Pheromones to Mating Disruption

“…Pheromone precursors are acquired from four main sources: (i) de novo synthesis, (ii) conversion of precursors that insects acquire from host plants or substrate, (iii) direct incorporation from the host plants, and/or (iv) from endosymbionts [21,[249][250][251][252]. Thus, it is likely that different variables influence the pheromone blend.…”

Gut fungal community and its probiotic effect onBactrocera dorsalis

“…Recently, B. dorsalis has spread northward in Asia to areas previously considered as unsuitable habitats, thereby posing a severe threat to agriculture in the temperate zone (Nugnes et al, 2018). Given the critical roles of gut microbiota in host fitness, the microbial composition and functions have been studied (Wang et al, 2011;Wang et al, 2013;Cheng et al, 2017;Cai et al, 2018;Li et al, 2020;Raza et al, 2020aRaza et al, , 2020bRen et al, 2021). Enterobacteriaceae are the dominant commensal bacteria in the gut of B. dorsalis (Wang et al, 2011;Khan et al, 2019).…”

Sex pheromones: Made with a little help from my (bacterial) friends

“…As a consequence, they often engage in stable (symbiotic) associations and coevolve these preexisting compounds and their perception into specific signals, or pheromones. A new study by Ren et al 8 published in this issue of Current Biology describes such a case: Bacillus bacteria harbored in the rectum of the oriental fruit fly Bactrocera dorsalis (Tephretidae) are the source of a male sex pheromone containing the two compounds 2,3,5-trimethylpyrazine (TMP) and 2,3,5,6-tetramethylpyrazine (TTMP) (Figure 1).…”

“…Both sexes of Tephretid flies are known to employ pheromones to attract the opposite sex, including the maleproduced compound TMP [9][10][11] . Ren et al 8 first conducted a deeper analysis of extracts from mature male recta that proved to attract virgin females. Gas chromatography coupled to mass spectrometry revealed TMP as well as TTMP, 2-ethyl-3,5-dimethylpyrazine, and 2,3,5-trimethyl-6-ethylpyrazine.…”

“…When these antennae are exposed to a single pure compound or complex blend, an electrical signal can be measured if the proteins on their surface are sensitive to at least one of the compounds. When Ren et al 8 tested the male rectal extracts on female antennae, only two of the abovementioned compounds, TMP and TTMP, proved to elicit such a response in female antennae. However, this insight still did not prove that they are the actual attractants from the complex extractsother compounds could be present in the extract that were just not discovered in the chemical analysis.…”