1. A Mycovirus Mediates the Virulence of an Insect-Killing Fungus against the Malaria Mosquito Vector
- Author
-
Robert H.A. Coutts, Ioly Kotta-Loizou, George K. Christophides, Andre N. Pitaluga, Josephine Blakiston, and Charalampos Filippou
- Subjects
Plasmodium ,biology ,fungi ,malaria ,microbiome ,Beauveria bassiana ,Virulence ,lcsh:A ,Bassiana ,biology.organism_classification ,Serratia ,Anopheles coluzzii ,Microbiology ,Immune system ,mycovirus ,RNA interference ,parasitic diseases ,Mycovirus ,Microbiome ,lcsh:General Works - Abstract
The cosmopolitan insect-pathogenic fungus and popular biocontrol agent Beauveria bassiana can be used to control Anopheles mosquito populations and restrict the spread of malaria, the deadliest vector-borne infectious disease in the world caused by the protozoan parasite Plasmodium. Here, we establish that infection with a double-stranded (ds)RNA mycovirus, Beauveria bassiana polymycovirus (BbPmV)-1, significantly reduces B. bassiana virulence against A. coluzzii, the main vector of malaria. The BbPmV-1-mediated hypovirulence can be at least partially attributed to slow fungal growth on the mosquitos. Analysis of the dual next-generation sequencing of the B. bassiana and A. coluzzii transcriptomes provided insight into the molecular mechanisms of the BbPmV-1-mediated effects. BbPmV-1-free B. bassiana has a wide impact on the A. coluzzii transcriptome, affecting immunity and metabolism, and led to the identification of novel immune response proteins. BbPmV-1 regulates the gene expression profile of its fungal host, directing the use of available resources towards sporulation and suppressing the mosquito immune system. Additionally, BbPmV-1-infected and -free B. bassiana strains differentially modulate mosquito gut microbiota; the former reduces the bacterial genus Elizabethkingia and the latter Serratia. Co-transfection of mosquitos with B. bassiana and P. berghei revealed a reduction of ookinetes in the presence of BbPmV-1, potentially due to the upregulation of a mycotoxin. Finally, BbPmV-1-mediated hypovirulence is at least partially dependent on the A. coluzzii RNAi pathway, and silencing of the dicer-2 gene restores virulence. Taken together, our data clearly demonstrate the crucial role of mycovirus infection in mediating B. bassiana virulence against A. coluzzii and suggest that BbPmV-1 protects A. coluzzii from B. bassiana, the mosquito’s own immune system, potentially harmful gut microbiota, and Plasmodium parasites.
- Published
- 2020
- Full Text
- View/download PDF