Ferritin-mediated regulation of gut microbiota homeostasis promotes blood-feeding adaptation in the tick Haemaphysalis doenitzi

Abstract

As obligate hematophagous parasites, ticks have evolved to cope with substantial amounts of iron and exogenous microorganisms present in host blood during feeding. In ticks, ferritin plays an important role in maintaining the oxidative balance of gut and the homeostasis of the microbial community structure, but its regulatory mechanism has not yet been clarified. This study successfully identified a ferritin gene from Haemaphysalis doenitzi, named Hd-fer, and further studied the function of Hd-fer. The results showed that rHd-fer had antioxidant properties and antibacterial activity. The expression of Hd-fer gene in the ovary and midgut was significantly higher than other organs, and the expression in adults was significantly higher than other stages. The Hd-fer gene knock-out significantly changed the abundance of the midgut microbial community, and the relative abundance decreased generally, while the relative abundance of Achromobacter increased. The knockout of Hd-fer gene also significantly changed the structural composition of the midgut microbial species, and pathogenic microorganisms showed a growing trend, producing their unique microbial genera, including Barnesiellaceae, Carnobacterium and Pediococcus. The RNA interference of Hd-fer led to prolonging the tick's blood sucking time and reducing engorged weight. The results of this study showed that Hd-fer may affect the stability of the midgut microbial community structure by regulating iron availability, which in turn plays an important role in the survival and reproduction of ticks. These findings provide novel insights into the role of ferritin in tick biology and highlight its potential as a target for controlling tick-borne diseases.