Abstract
Wolbachia are endosymbiotic bacteria found in the majority of arthropods and filarial nematodes of medical and veterinary importance. They have evolved a wide range of symbiotic associations. In filarial nematodes that cause human lymphatic filariasis (Wuchereria bancrofti, Brugia malayi) or onchocerciasis (Onchocerca volvulus), Wolbachia are important for parasite development, reproduction and survival. The symbiotic bacteria rely in part on nutrients and energy sources provided by the host. Genomic analyses suggest that the strain of Wolbachia found in B. malayi (wBm) lacks the genes for two glycolytic enzymes—6-phosphofructokinase and pyruvate kinase—and is thus potentially unable to convert glucose into pyruvate, an important substrate for energy generation. The Wolbachia surface protein, wBm00432, is complexed to six B. malayi glycolytic enzymes, including aldolase. In this study we characterized two B. malayi aldolase isozymes and found that their expression is dependent on Wolbachia fitness and number. We confirmed by immuno-transmission electron microscopy that aldolase is associated with the Wolbachia surface. RNAi experiments suggested that aldolase-2 plays a significant role in both Wolbachia survival and embryogenesis in B. malayi. Treatment with doxycycline reduced Wolbachia fitness and increased the amount of both glucose and glycogen detected in the filarial parasite, indicating that glucose metabolism and glycogen storage in B. malayi are associated with Wolbachia fitness. This metabolic co-dependency between Wolbachia and its filarial nematode indicates that glycolysis could be a shared metabolic pathway between the bacteria and B. malayi, and thus a potential new target for anti-filarial therapy.
Highlights
Endosymbiotic, maternally transmitted bacteria of the genus Wolbachia reside in the cytoplasm of all reproductive and some somatic cells of the majority of arthropods and in most of the filarial nematodes of medical and veterinary importance, including Wuchereria bancrofti, Brugia malayi, Onchocerca volvulus, O. ochengi and Dirofilaria immitis [1,2]
Of all the developmental stages of B. malayi, Mf contains the smallest number of Wolbachia found in B. malayi (wBm) while the adult female worms carry the maximum number of bacteria [26]
Western blot analyses using monospecific antibodies raised against a conservative domain of the human and parasite aldolase proteins confirmed that both proteins, BMA-ALDO-1 (39.5 kDa) and BMA-ALDO2 (42.5 kDa), are highly expressed in B. malayi adult females as compared to Mf (Fig 1B)
Summary
Endosymbiotic, maternally transmitted bacteria of the genus Wolbachia (family Rickettsiaceae) reside in the cytoplasm of all reproductive and some somatic cells of the majority of arthropods and in most of the filarial nematodes of medical and veterinary importance, including Wuchereria bancrofti, Brugia malayi, Onchocerca volvulus, O. ochengi and Dirofilaria immitis [1,2]. Wolbachia and their hosts have evolved an array of symbiotic associations, ranging from reproductive parasitism in arthropods, to mutualistic relationships observed in wasps and filarial nematodes [1,3,4]. The use of the antibiotic for mass drug administration, a measure currently used to control transmission of these infections, is not practical because of the need for long-term treatment (4–6 weeks) and the contraindication for young children (
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