Horizontal Transmission of the Symbiont Microsporidia MB in Anopheles arabiensis

Abstract

The recently discovered Anopheles symbiont, Microsporidia MB, has a strong malaria transmission-blocking phenotype in Anopheles arabiensis, the predominant Anopheles gambiae species complex member in many active transmission areas in eastern Africa. The ability of Microsporidia MB to block Plasmodium transmission together with vertical transmission and avirulence makes it a candidate for the development of a symbiont-based malaria transmission blocking strategy. We investigate the characteristics and efficiencies of Microsporidia MB transmission between An. arabiensis mosquitoes. We show that Microsporidia MB is not transmitted between larvae but is effectively transmitted horizontally between adult mosquitoes. Notably, Microsporidia MB was only found to be transmitted between male and female An. arabiensis, suggesting sexual horizontal transmission. In addition, Microsporidia MB cells were observed infecting the An. arabiensis ejaculatory duct. Female An. arabiensis that acquire Microsporidia MB horizontally are able to transmit the symbiont vertically to their offspring. We also investigate the possibility that Microsporidia MB can infect alternate hosts that live in the same habitats as their An. arabiensis hosts, but find no other non-anopheline hosts. Notably, Microsporidia MB infections were found in another primary malaria African vector, Anopheles funestus s.s. The finding that Microsporidia MB can be transmitted horizontally is relevant for the development of dissemination strategies to control malaria that are based on the targeted release of Microsporidia MB infected Anopheles mosquitoes.

Microsporidia MB in the primary malaria vector Anopheles gambiae s.s. is avirulent and undergoes maternal and horizontal transmission

“…arabiensis with Plasmodium transmission blocking capabilities has generated interest in the potential development of alternative symbiont-based malaria control strategy. In addition to Plasmodium transmission blocking, other characteristic such as transovarial transmission [9],horizontal transmission [10] and avirulence are highly important for the potential of symbiont-based transmission blocking since they contribute to the ability of Microsporidia MB to spread through and be maintained in Anopheles mosquito populations. Microsporidia MB is present in Anopheles species outside of An.…”

“…Horizontal transmission of Microsporidia MB previously observed in An. arabiensis was from individuals of opposite sex [10], hence this experiment was limited only in individuals of opposite sex. Subsequently all An.…”

“…Alternative mosquito-borne control interventions utilizing symbionts stably maintained in the mosquito that mediate protection of Anopheles against Plasmodium falciparum [4,5], and/or Aedes against arboviruses [6-8] have been proposed. The discovery of a novel Microsporidia MB symbiont in wild Anopheles arabiensis mosquitoes and the nding that it protects these hosts against Plasmodium parasite infection [9], and is vertically and horizontally transmitted in adults [10], has led to the suggestion that it could be a promising candidate for integrated vector management.…”

The gut commensal bacterium Enterococcus faecalis LX10 contributes to defending against Nosema bombycis infection in Bombyx mori

“…4 The microsporidian pathogens are also considered effective biological control agents for mosquitoes, gypsy moth, locust, and corn borer red imported fire ants. [5][6][7] In 1980, Paranosema locustae became the first microsporidium to be registered and successfully commercially marketed in the United States (USEPA 2000). It is still being sold for bait-and-spray applications for Mormon cricket and grasshopper control due to the high grasshopper mortality associated with products, such as Nolo Bait™ and Semaspore™.…”

“…To date, pebrine disease is the only disease with a mandatory quarantine in the silk production industry due to its destructive consequences 4 . The microsporidian pathogens are also considered effective biological control agents for mosquitoes, gypsy moth, locust, and corn borer red imported fire ants 5–7 . In 1980, Paranosema locustae became the first microsporidium to be registered and successfully commercially marketed in the United States (USEPA 2000).…”