The human odorant receptor OR10A6 is tuned to the pheromone of the commensal fruit fly Drosophila melanogaster

Abstract

BackgroundAll living things speak chemical. The challenge is to discover the vocabulary, the volatile odorant chemicals that enable communication across phylogenies and to translate them to physiological, behavioural and ecological function. Olfactory receptors (ORs) interface animals with airborne odorants. Expression of single ORs in human embryonic kidney cells (HEK-293) makes it possible to interrogate ORs with synthetic chemicals and to identify cognate ligands that convey olfactory information.ResultsThe cosmopolitan strain of the vinegar fly Drosophila melanogaster has accompanied the human expansion out of Africa, more than ten thousand years ago. These flies are strictly anthropophilic and depend on human resources and housing for survival, particularly in colder climate zones. Curiously, humans sense the scent of a single fly, and more precisely the female pheromone (Z)-4 undecenal (Z4-11Al), at 10 ng/mL (0.06 µmol/L). A screening of all functional human ORs in a HEK-293 assay provides an explanation for this astounding sensitivity, as it shows that OR10A6, one of the most highly expressed human ORs, is specifically tuned to Z4-11Al. Chemical analysis of fly effluvia confirms that cosmopolitan D. melanogaster females release Z4-11Al, while females of an African fly strain from Zimbabwe release a 1:3-blend of Z4-11Al and (Z)-4 nonenal (Z4-9Al). Interestingly, a blend of Z4-9Al and Z4-11Al produces a different aroma than the the single compounds, which is why we readily differentiate cosmopolitan and Zimbabwe flies by nose.ConclusionThat we sensitively and specifically perceive the fly pheromone Z4-11Al suggests that it is a component of human odour scenes. This may have afforded a sensory drive during adaptation of commensal flies to human habitats and selected for a role of Z4-11Al in fly aggregation and premating communication. Screening ORs for key ligands leads to the discovery of messenger chemicals that enable chemical communication among and betwen vertebrate and invertebrate animals.

Heterologous expression and functional characterization of Drosophila suzukii OR69a transcript variants unveiled response to kairomones and to a candidate pheromone

“…In accordance, in the same investigation we reported chemical analysis on D. melanogaster and headspaces indicating small traces of (Z)-4-nonenal, associated with the presence of the (Z,Z)-5,9-HD isomer in limited quantities on the cuticular of these Drosophila (Coyne 1996;Billeter et al 2009;Dallerac et al 2000). Interestingly, (Z,Z)-5,9-HD is more abundant on the cuticle of the D. melanogaster subspecies Zimbabwe (Dallerac et al 2000;Yukilevich and True 2008;Grillet et al 2012), and more recent investigations supported the autoxidation hypothesis demonstrating the emission of (Z)-4-nonenal from the Zimbabwe D. melanogaster (Frey et al 2020).…”

“…These various scenario seems to be more reliable considering additional trials we performed by expressing OR69a orthologues of the D. melanogaster subspecies Zimbabwe (Online Resource 7). Testing headspaces from female insects, expecting to contain (Z)-4-nonenal (Dallerac et al 2000;Yukilevich and True 2008;Grillet et al 2012;Frey et al 2020), we did not record any effect for OR69aB. To shed more light on this aspect, additional experiments may be conducted by testing samples of Zimbabwe by GC-SSR using a different GC-column from HP-5 and adopting a different pheromone collection protocol (Frey et al 2020).…”

“…Testing headspaces from female insects, expecting to contain (Z)-4-nonenal (Dallerac et al 2000;Yukilevich and True 2008;Grillet et al 2012;Frey et al 2020), we did not record any effect for OR69aB. To shed more light on this aspect, additional experiments may be conducted by testing samples of Zimbabwe by GC-SSR using a different GC-column from HP-5 and adopting a different pheromone collection protocol (Frey et al 2020). On the other hand, activation of DsuzOR69aB to (Z)-4-nonenal, not expected to be emitted by D. suzukii, but identified in the emissions of D. melanogaster (Lebreton et al 2017) and of its subspecies Zimbabwe (Frey et al 2020), may suggest some sort of mechanisms of inter-specific communication among different insects of the genus Drosophila.…”

“…To shed more light on this aspect, additional experiments may be conducted by testing samples of Zimbabwe by GC-SSR using a different GC-column from HP-5 and adopting a different pheromone collection protocol (Frey et al 2020). On the other hand, activation of DsuzOR69aB to (Z)-4-nonenal, not expected to be emitted by D. suzukii, but identified in the emissions of D. melanogaster (Lebreton et al 2017) and of its subspecies Zimbabwe (Frey et al 2020), may suggest some sort of mechanisms of inter-specific communication among different insects of the genus Drosophila. For example, complex mechanisms exist at the base of inter-specific discrimination among insects within this genus (Wood and Ringo 1980) that are based on the different composition of cuticular hydrocarbons (Serrato-Capuchina et al 2020).…”