The tracheal immune system of insects - A blueprint for understanding epithelial immunity.

The unique design of respiratory organs in multicellular organisms makes them prone to infection by pathogens. To cope with this vulnerability, highly effective local immune systems evolved that are also operative in the tracheal system of insects. Many pathogens and parasites (including viruses, bacteria, fungi, and metazoan parasites) colonize the trachea or invade the host via this route. Currently, only two modules of the tracheal immune system have been characterized in depth: 1) Immune deficiency pathway-mediated activation of antimicrobial peptide gene expression and 2) local melanization processes that protect the structure from wounding. There is an urgent need to increase our understanding of the architecture of tracheal immune systems, especially regarding those mechanisms that enable the maintenance of immune homeostasis. This need for new studies is particularly exigent for species other than Drosophila.

Adult and Larval Tracheal Systems Exhibit Different Molecular Architectures in Drosophila.

Knowing the molecular makeup of an organ system is required for its in-depth understanding. We analyzed the molecular repertoire of the adult tracheal system of the fruit fly Drosophila melanogaster using transcriptome studies to advance our knowledge of the adult insect tracheal system. Comparing this to the larval tracheal system revealed several major differences that likely influence organ function. During the transition from larval to adult tracheal system, a shift in the expression of genes responsible for the formation of cuticular structure occurs. This change in transcript composition manifests in the physical properties of cuticular structures of the adult trachea. Enhanced tonic activation of the immune system is observed in the adult trachea, which encompasses the increased expression of antimicrobial peptides. In addition, modulatory processes are conspicuous, in this case mainly by the increased expression of G protein-coupled receptors in the adult trachea. Finally, all components of a peripheral circadian clock are present in the adult tracheal system, which is not the case in the larval tracheal system. Comparative analysis of driver lines targeting the adult tracheal system revealed that even the canonical tracheal driver line breathless (btl)-Gal4 is not able to target all parts of the adult tracheal system. Here, we have uncovered a specific transcriptome pattern of the adult tracheal system and provide this dataset as a basis for further analyses of the adult insect tracheal system.