Increased expression of ATG genes during nonfeeding periods in the tick Haemaphysalis longicornis

Ticks are long-lived hematophagous arthropods and have tolerance to starvation. They can survive without food during the host-seeking period for several months to years. To understand how ticks obtain energy over a long period of non-feeding (starvation), we focused on autophagy, a crucial proteolysis system via the lysosomes for various cellular processes that is induced during starvation in eukaryotes. In the present study, EST databases for several organs of the tick Haemaphysalis longicornis led to the identification of HlATG3, HlATG4 and HlATG8, homologues of 3 autophagy-related (ATG) genes, ATG3, ATG4 and ATG8/LC3/GABARAP, respectively, which are essential for the Atg8 conjugation system in model animals. Real-time PCR results revealed that the expression of HlATG3, HlATG4 and HlATG8 in the tick showed higher levels during the non-feeding period than the feeding period, suggesting that the Atg8 conjugation system is at work in unfed ticks. Notably, their expression levels were higher in the midgut, a digestive organ, of unfed than fed adults. Histological analysis demonstrated that lipids and glycogen accumulated within the epithelial cells of the midgut in unfed ticks, implying that the midgut of unfed ticks serves as storage of those components as nutrients during non-feeding. Furthermore, autophagic organelles were found in the midgut undifferentiated cells of unfed ticks. The starved condition appears to be associated with the increased expression of HlATG genes in the midgut of unfed ticks. Tick autophagy might help compensate for the loss of nutrients derived from host blood components during the non-feeding period.