Ants are fascinating insects that distribute tasks among individuals belonging to different castes, including mated and virgin queens, drones and worker ants. To fulfil caste-specific functions, ants have developed a complex system of chemical communication using sensory organs (sensilla) that detect molecules carrying task-specific information (semiochemicals). This system requires carrier proteins to bind the molecules, which are hydrophobic, and transfer them to the chemoreceptors that generate electrical signals for neuronal processing in the brain. However, the number of carrier proteins known is not sufficient to bind the large number of semiochemicals that are recognized by the ants. In a recent study published in PNAS, a team of Japanese scientists lead by Yuko Ishida and Toshimasa Yamazaki identified a novel carrier protein involved in chemical communication in worker ants that appears to be capable of delivering various hydrophobic semiochemicals to the nervous system.
The antennae are the major chemosensory organs in ants. They carry numerous olfactory sensors called basiconic sensilla – which are made of different cell types, including sensory neurons – for sensing odours. Once the semiochemicals have entered the sensillum through pores, they reach the aqueous sensillum lymph, which contains carrier proteins that bind the hydrophobic molecules and deliver them to various chemoreceptors residing in the membrane of the neuron's dendrites. As ants can detect a wide variety of chemically different hydrophobic compounds, it was hypothesized that some of these carrier proteins must possess a hydrophobic binding pocket that interacts with a variety of these molecules. To identify such carrier proteins, the scientists screened for worker-specific antenna genes in the Japanese carpenter ant, Camponotus japonicus. One of the identified genes encodes a protein with high similarity to the Niemann-Pick C2 (Npc2) protein, which is an essential carrier protein for intracellular cholesterol transport in vertebrates and humans and has been suggested to be involved in the regulation of sterol homeostasis in the fruitfly Drosophila melanogaster, through the homologous NPC2 gene. However, in ants this protein appears to serve a different function, as the scientists unexpectedly found that NPC2 in C. japonicas (CjapNPC2) is exclusively expressed in the antennae and is specifically detectable in the lymph-filled cavities of the basiconic sensilla.
To examine the protein's binding properties and structure, the team expressed CjapNPC2 in E. coli cells and purified it to homogeneity. Binding studies revealed that the protein indeed interacts with a broad spectrum of different hydrophobic compounds including long-chained fatty acids, alcohols and acetates. They also found that some of the tested compounds can provoke electrophysiological signals in the worker ant's antenna. Next, the team went on to solve the 3D structure by X-ray crystallography when bound and unbound to oleic acid. They found that the structure of CjapNPC2 consists primarily of antiparallel β-sheets forming a larger hydrophobic cavity for binding of the ligand in a U-shaped manner. Most strikingly, CjapNPC2 exhibits some intrinsic flexibility (independent of ligand binding), particularly at the entry to the binding cavity, which may contribute to its moderate selectivity and thus facilitate entry and binding of a range of semiochemicals.
Ishida and Yamazaki's team has identified a new carrier protein involved in ant chemical communication. Most interestingly, the protein can bind and deliver various hydrophobic compounds. As the protein's function is different from that known in vertebrates and other insects, it seems that ants have recruited and modified this protein during evolution to comply with their need for a carrier protein of moderate ligand specificity. This study may also help in our age-old battle with these tenacious insects, as knowing the mode of ligand binding may help us to develop new tools for pest control.
