Niemann–Pick type C2 protein mediating chemical communication in the worker ant

Abstract

Ants are eusocial insects that are found in most regions of the world. Within its caste, worker ants are responsible for various tasks that are required for colony maintenance. In their chemical communication, α-helical carrier proteins, odorant-binding proteins, and chemosensory proteins, which accumulate in the sensillum lymph in the antennae, play essential roles in transferring hydrophobic semiochemicals to chemosensory receptors. It has been hypothesized that semiochemicals are recognized by α-helical carrier proteins. The number of these proteins, however, is not sufficient to interact with a large number of semiochemicals estimated from chemosensory receptor genes. Here we shed light on this conundrum by identifying a Niemann–Pick type C2 (NPC2) protein from the antenna of the worker Japanese carpenter ant, Camponotus japonicus (CjapNPC2). CjapNPC2 accumulated in the sensillum cavity in the basiconic sensillum. The ligand-binding pocket of CjapNPC2 was composed of a flexible β-structure that allowed it to bind to a wide range of potential semiochemicals. Some of the semiochemicals elicited electrophysiolgical responses in the worker antenna. In vertebrates, NPC2 acts as an essential carrier protein for cholesterol from late endosomes and lysosomes to other cellular organelles. However, the ants have evolved an NPC2 with a malleable ligand-binding pocket as a moderately selective carrier protein in the sensillum cavity of the basiconic sensillum. CjapNPC2 might be able to deliver various hydrophobic semiochemicals to chemosensory receptor neurons and plays crucial roles in chemical communication required to perform the worker ant tasks.

Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication

“…Although a few studies have sought to implicate various small soluble proteins in pheromone recognition (17,(20)(21)(22)(23), it seems more likely that these proteins are involved in generic odorant solubilization and play little role in odor coding (24,25). The only known hymenopteran pheromone ligand-receptor pair to date is the honey bee (Apis mellifera) queen pheromone 9-ODA and the OR AmelOR11 (26).…”

Chemosensing of honeybee parasite, Varroa destructor: Transcriptomic analysis

“…Membrane-bound receptors: odorant receptors (ORs), ionotropic receptors (IRs) and their corresponding co-receptors (ORco and IRco) as well as gustatory receptors (GRs). In addition, associated proteins such as sensory neuron membrane proteins (SNMPs) were found to play a role in some organisms, and odorant-degrading enzymes (ODEs) are important for the termination of the signal 1,3–6 .…”

Isolation of a novel LPS-induced component of the ML superfamily in Ciona intestinalis

“…In invertebrates, components of the NPC2 family have been identified in D. melanogaster (Shi et al, 2012), insect (Ishida et al, 2014) and shrimp (Liao et al, 2011). However, little is known letters (28e146 a.a.).…”

“…Bar indicate the number of amino acid residues substitutions for site. (Ishida et al, 2014) or binding LPS (Liao et al, 2011;Shi et al, 2012) suggesting that the specific role of this protein is still a matter of discussion in invertebrate.…”

“…Members of the ML domain play important role in lipid metabolism (sterol homeostasis and steroid biosynthesis) but also in innate immune signal pathways (LPS induced signalling). In invertebrates, a few ML genes have been identified in Drosophila melanogaster (Shi et al, 2012), in the shrimp Litopenaeus vannamei (Liao et al, 2011) and worker ant Camponotus japonicus (Ishida et al, 2014). These proteins may have multiple roles in binding bacterial cell wall components and working in chemical and immune signal pathways.…”