Comparison of the hemolysis machinery in two evolutionarily distant blood-feeding arthropod vectors of human diseases

Abstract

Host blood protein digestion plays a pivotal role in the ontogeny and reproduction of hematophagous vectors. The gut of hematophagous arthropods stores and slowly digests host blood and represents the primary gateway for transmitted pathogens. The initial step in blood degradation is induced lysis of host red blood cells (hemolysis), which releases hemoglobin for subsequent processing by digestive proteolytic enzymes. The activity cycles and characteristics of hemolysis in vectors are poorly understood. Hence, we investigated hemolysis in two evolutionarily distant blood-feeding arthropods: The mosquito Culex pipiens and the soft tick Argas persicus, both of which are important human and veterinary disease vectors. Hemolysis in both species was cyclical after blood meal ingestion. Maximum digestion occurs under slightly alkaline conditions in females. Hemolytic activity appears to be of lipoid origin in C. pipiens and enzymatic activity (proteolytic) in A. persicus. We have assessed the effect of pH, incubation time, and temperature on hemolytic activity and the hemolysin. The susceptibility of red blood cells from different hosts to the hemolysin and the effect of metabolic inhibition of hemolytic activity were assessed. We conclude that in C. pipiens and A. persicus midgut hemolysins control the amplitude of blood lysis step to guarantee an efficient blood digestion.

Author summary

Mosquitoes and ticks are medically important and ubiquitous hematophagous arthropods that require considerable amounts of protein for egg production. Vertebrate blood is the source of protein for adult mosquitoes and ticks to mature eggs. Culex pipiens is a vector of the filarial agent Wuchereria bancrofti and Rift Valley fever (RVFV), Sindbis (SINV), and West Nile (WNV) viruses. Ticks transmit many diseases to domestic animals and rank second to mosquitoes as vectors of human diseases. However, ticks increase potential health hazards several fold since they act as both vectors and reservoirs of pathogens though transstadial and transovarial disease transmission. Most of the nutritional value of a blood meal is proteinaceous, and the largest quantity of protein is contained inside erythrocytes. The digestive features and utilization of dietary components are similar in mosquitoes and soft ticks, but the underlying mechanisms are poorly understood. This study examines the hemolytic activity, lytic cycles, characteristics, and nature of hemolytic factors in the mosquito C. pipiens and the fowl tick A. persicus. The work reveals new insights into the distinct digestive processes in both species, improving our understanding of the basic biology of arthropod vectors.