Abstract

Simple SummaryHoneybees, which are important for the development and maintenance of natural ecosystems, are infected by microsporidia, Nosema apis and N. ceranae. These parasites induce a disease named nosemosis contributing to the impairment of digestion and nutrient absorption, ultimately leading to total colony collapse. The need for research into the control of N. ceranae has become increasingly important. Promising compounds for the treatment of nosemosis are porphyrins. In the present study, we examined the effects of three different porphyrins on the infectivity of N. ceranae microsporidia. A significantly lower level of infection was observed in the bees infected with the porphyrin-treated spores than in the control bees (infected with untreated spores). We showed that protoporphyrin lysine derivatives in particular prevented the development of Nosema spores and simultaneously extended bee life spans (up to 50%). The results also indicate that these porphyrins may contribute to the reduction in digestive nutrient absorption disorders in bees. The present findings can be used to develop a new class of drugs for combating nosemosis. These compounds may serve as preventive or disinfection agents through direct inactivation of Nosema both in the midgut and outside the host body, i.e., in the hive.The effect of two protoporphyrin IX derivatives conjugated with single (PP[Lys(TFA)-OH)]2) or double (PP[Lys(TFA)-Lys(TFA)-OH]2) lysine moieties on the infectious capacity of Nosema ceranae spores was examined, and their efficacies were compared with those of a cationic porphyrin (H2TTMePP). Honeybees were inoculated with spores preincubated with porphyrins or with untreated spores (control). A significantly lower level of infection was observed in the bees infected with the porphyrin-treated spores than in the infected control. Porphyrins 1 and 2 reduced the infectious capability of microsporidia more efficiently than porphyrin 3, with bee mortality declining to almost 50%. Confocal analysis of the midguts of infected bees revealed distinct differences in the number of spores between the control group and the group infected with PP[Lys(TFA)-Lys(TFA)-OH]2-treated spores. Notably, bees with a reduced level of infection consumed less sucrose syrup than the control bees, indicating a reduction in digestive disorders and an improvement in food absorption.

Highlights

  • Nosema ceranae is a parasite and member of the Microsporidia division, which is a group of obligate intracellular parasites that can infect vertebrate and invertebrate species [1,2]

  • Honeybees infected with spores, incubated separately with each of the porphyrins—H2 TTMePP, PP[Lys(TFA)-OH)]2, and PP[Lys(TFA)-Lys(TFA)-OH]2 —for 24 h showed significantly decreased spore counts after day 7 compared to the honeybees in the control group, which were exposed to untreated microsporidia (H(3, N = 80) = 67.75; p < 0.001)

  • Honeybees infected with spores, incubated separately with each of the porphyrins—H2TTMePP, PP[Lys(TFA)-OH)]2, and PP[Lys(TFA)-Lys(TFA)-OH]2—for 24 h showed significantly decreased spore counts after day 7 compared to the honeybees in the control group, which were exposed to untreated microsporidia (H(3, N = 80) = 67.75; p < 0.001)

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Summary

Introduction

Nosema ceranae is a parasite and member of the Microsporidia division, which is a group of obligate intracellular parasites that can infect vertebrate and invertebrate species [1,2]. Honeybees, which are important for the development and maintenance of natural ecosystems, are infected by two species of microsporidia, Nosema apis and N. ceranae, and they both cause the disease nosemosis [9,10,11,12,13]. N. ceranae can be spread via trophallaxis (food exchange), which can potentially increase colony infection [23,24]. Spores develop in the midgut of honeybees, followed by the polar tube extrusion and injection of the sporoplasm inside epithelial cells. N. ceranae infections cause increased energetic stress in bees [29] These adverse outcomes contribute to total colony collapse in Europe and North America [31,32,33,34,35]

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