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

Author:

Nattoh Godfrey,Onyango Brenda,Makhulu Edward Edmond,Omoke Diana,Ang’ang’o Lilian Mbaisi,Kamau Luna,Gesuge Maxwell Machani,Ochomo Eric,Herren Jeremy Keith

Abstract

Abstract Background The demonstration that the recently discovered Anopheles symbiont Microsporidia MB blocks malaria transmission in Anophelesarabiensis and undergoes vertical and horizontal transmission suggests that it is a promising candidate for the development of a symbiont-based malaria transmission-blocking strategy. The infection prevalence and characteristics of Microsporidia MB in Anopheles gambiae sensu stricto (s.s.), another primary vector species of malaria in Kenya, were investigated. Methods Field-collected females were confirmed to be Microsporidia MB-positive after oviposition. Egg counts of Microsporidia MB-infected and non-infected individuals were used to infer the effects of Microsporidia MB on fecundity. The time to pupation, adult sex ratio and survival were used to determine if Microsporidia MB infection has similar characteristics in the host mosquitoes An. gambiae and An. arabiensis. The intensity of Microsporidia MB infection in tissues of the midgut and gonads, and in carcasses, was determined by quantitative polymerase chain reaction. To investigate horizontal transmission, virgin males and females that were either Microsporidia MB-infected or non-infected were placed in standard cages for 48 h and allowed to mate; transmission was confirmed by quantitative polymerase chain reaction targeting Microsporidia MB genes. Results Microsporidia MB was found to naturally occur at a low prevalence in An. gambiae s.s. collected in western Kenya. Microsporidia MB shortened the development time from larva to pupa, but other fitness parameters such as fecundity, sex ratio, and adult survival did not differ between Microsporidia MB-infected and non-infected hosts. Microsporidia MB intensities were high in the male gonadal tissues. Transmission experiments indicated that Microsporidia MB undergoes both maternal and horizontal transmission in An. gambiae s.s. Conclusions The findings that Microsporidia MB naturally infects, undergoes maternal and horizontal transmission, and is avirulent in An. gambiae s.s. indicate that many of the characteristics of its infection in An. arabiensis hold true for the former. The results of the present study indicate that Microsporidia MB could be developed as a tool for the transmission-blocking of malaria across different Anopheles species. Graphical Abstract

Funder

The International Foundation for Science, Stockholm, Sweden

Centre for Global Health Research (CGHR), Kenya Medical Research Institute, Kisumu, Kenya

International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya

Open Philanthropy (SYMBIOVECTOR Track A) and the Bill and Melinda Gates Foundation

The Childrens’ Investment Fund Foundation

Research Unit in Bioinformatics (RUBi), Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa

Centre for Biotechnology Research and Development (CBRD), Kenya Medical Research Institute, Nairobi, Kenya

The ANTi-VeC network

Publisher

Springer Science and Business Media LLC

Subject

Infectious Diseases,Parasitology,General Veterinary

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