The Polymycovirus-Mediated Growth Enhancement of the Entomopathogenic Fungus Beauveria bassiana Is Dependent on Carbon and Nitrogen Metabolism

Abstract

Polymycoviridae is a growing family of mycoviruses whose members typically have non-conventional capsids and multi-segmented, double-stranded (ds) RNA genomes. Beauveria bassiana polymycovirus (BbPmV) 1 is known to enhance the growth and virulence of its fungal host, the entomopathogenic ascomycete and popular biological control agent B. bassiana. Here we report the complete sequence of BbPmV-3, which has six genomic dsRNA segments. Phylogenetic analysis of RNA-dependent RNA polymerase (RdRp) protein sequences revealed that BbPmV-3 is closely related to the partially sequenced BbPmV-2 but not BbPmV-1. Nevertheless, both BbPmV-3 and BbPmV-1 have similar effects on their respective host isolates ATHUM 4946 and EABb 92/11-Dm, affecting pigmentation, sporulation, and radial growth. Production of conidia and radial growth are significantly enhanced in virus-infected isolates as compared to virus-free isogenic lines on Czapek-Dox complete and minimal media that contain sucrose and sodium nitrate. However, this polymycovirus-mediated effect on growth is dependent on the carbon and nitrogen sources available to the host fungus. Both BbPmV-3 and BbPmV-1 increase growth of ATHUM 4946 and EABb 92/11-Dm when sucrose is replaced by lactose, trehalose, glucose, or glycerol, while the effect is reversed on maltose and fructose. Similarly, both BbPmV-3 and BbPmV-1 decrease growth of ATHUM 4946 and EABb 92/11-Dm when sodium nitrate is replaced by sodium nitrite, potassium nitrate, or ammonium nitrate. In conclusion, the effects of polymycoviruses on B. bassiana are at least partially mediated via its metabolic pathways.

Freeing Aspergillus fumigatus of Polymycovirus Infection Renders It More Resistant to Competition with Pseudomonas aeruginosa Due to Altered Iron-Acquiring Tactics

“…Mycoviruses have been reported to affect a range of host phenotypes, such as morphology, pigmentation, growth, virulence, pathogenicity, toxin production, and azole resistance [11]. Polymycovirus infection has been shown previously to enhance pigment production of a fungus [12], while other mycovirus infections in A. fumigatus may differentially affect host pigmentation [13]. Although Aspergillus spp.…”

“…Another polymycovirus was shown to increase A. fumigatus virulence in the greater wax moth Galleria mellonella infection model [ 13 ]. To our knowledge, no direct link between mycovirus infection and siderophores has been reported previously; however, polymycoviruses were associated with carbon and nitrogen metabolism alterations [ 12 ]. In our study, the siderophore reservoir is consumed sooner by the VF A. fumigatus strain, which better withstood the competition for iron with P. aeruginosa [ 6 ].…”

Virus Infection of Aspergillus fumigatus Compromises the Fungus in Intermicrobial Competition

“…We would emphasize that the demonstrated equivalence of growth (in the absence of Pseudomonas) may not apply to all other growth conditions; other growth conditions would need to be studied individually. Indeed, as yet unpublished studies, with a related virus, in an entomopathogenic fungus, indicate differences between that infected and uninfected fungus, with respect to growth, are medium-dependent [47].…”

ICTV Virus Taxonomy Profile: Polymycoviridae 2022

“…Polymycovirus infection has been associated with various host alterations, including changes in pigmentation [1,2,4,5], sectoring [1,2], decreased host growth [4] and host virulence [4], as well as increased sporulation [5], host growth [2,5] and host virulence [2]. Infection has also been reported to increase sensitivity to antifungals [3] and to the bacterium Pseudomonas aeruginosa [6].…”

“…Infection has also been reported to increase sensitivity to antifungals [3] and to the bacterium Pseudomonas aeruginosa [6]. Although the molecular mechanisms underpinning the above phenotypes have not been elucidated, there is evidence that polymycoviruses modulate host carbon, nitrogen and iron metabolism [5, 7]. Finally, polymycoviruses are targeted by the host RNA silencing machinery [8].…”