Aspergillus Goes Viral: Ecological Insights from the Geographical Distribution of the Mycovirome within an Aspergillus flavus Population and Its Possible Correlation with Aflatoxin Biosynthesis

Abstract

Microbial multi-level interactions are essential to control the success of spreading and survival of most microbes in natural environments. Phytopathogenic mycotoxigenic fungal species, such as Aspergillus flavus, represent an important issue in food safety. Usually, non-toxigenic strains are exploited for biocontrol strategies to mitigate infections by toxigenic strains. To comprehend all the biological variables involved in the aflatoxin biosynthesis, and to possibly evaluate the interplay between A. flavus toxigenic and non-toxigenic strains during intraspecific biocompetition, the “virological” perspective should be considered. For these reasons, investigations on mycoviruses associated to A. flavus populations inhabiting specific agroecosystems are highly desirable. Here, we provide the first accurate characterization of the novel mycovirome identified within an A. flavus wild population colonizing the maize fields of northern Italy: a selection of A. flavus strains was biologically characterized and subjected to RNAseq analysis, revealing new mycoviruses and a peculiar geographic pattern distribution in addition to a 20% rate of infection. More interestingly, a negative correlation between viral infection and aflatoxin production was found. Results significantly expanded the limited existent data about mycoviruses in wild A. flavus, opening new and intriguing hypotheses about the ecological significance of mycoviruses.

Virome analysis of an ectomycorrhizal fungus Suillus luteus revealing potential evolutionary implications

“…The virus SlNV4 is comprised of two segments, and likely belonging to a newly defined group of narnaviruses called splipalmiviruses ( Sutela et al., 2020 ). The RNA1 and RNA2 segments of SlNV4 display the greatest similarity to two segments of a tri-segmented narnavirus known as Aspergillus flavus narnavirus 1 ( Degola et al., 2021 ), showing 77% and 73% identity, respectively. SlNV5 showed the highest similarity to Rhizopus microsporus 20S narnavirus with 83% identity.…”

“…These viruses possess divided RdRp palm domains, which are encoded separately by two genomic segments ( Sutela et al., 2020 ; Kondo et al., 2022 ). Whereas some splipalmiviruses have been identified to possess additional segments with unknown function ( Chiba et al., 2021a ; Degola et al., 2021 ; Jia et al., 2021 ). The formation of RdRp complex has been proven by a homology modeling study, which demonstrated that the two RdRp fragments can bind together through hydrogen bonds and van der Waals forces ( Chiba et al., 2021a ).…”

Experimental verification of strain-dependent relationship between mycovirus and its fungal host

“…As described previously, the sequences of the four partitiviruses are similar to Aspergillus flavus partitivirus 1, 27 while they are apparently distanced from Aspergillus flavus partitivirus 2. 28 Notably, the four partitiviruses sequenced by FLDS contained eight segments, which differed from Aspergillus flavus partitivirus 1, which was reported to contain three segments 27 , 28 (See Table S2 ). In the partitivirus sequenced in this study, segment 1, 2, and 4 showed relatively high homology to the sequence of RNA1, RNA2, and RNA3 of Aspergillus flavus partitivirus 1 (78%–88%) respectively, while segment 3 and 5 showed low homology (30%–39%) to the RNA3 of Aspergillus flavus partitivirus 1 sequence.…”

Grapevine virome and production of healthy plants by somatic embryogenesis

“…Mycoviruses can, therefore, be considered an ecological marker for fungal spread. For instance, the fungal community presents in the plants grown in nurseries integrated with the mycobiome of the vineyard could be easily evaluated by studying the spread of mycoviruses (Degola et al ., 2021 ).…”