Decoding the RNA virome of the tree parasite Armillaria provides new insights into the viral community of soil‐borne fungi

Abstract

The globally distributed basidiomycete genus Armillaria includes wood decomposers that can act as opportunistic parasites, causing deadly root rot on woody plants. To test whether RNA viruses are involved in this opportunistic behaviour, a large isolate collection of five Armillaria species collected over 40 years in Switzerland from trees, dead wood and soil was analysed. De novo assembly of RNA‐Seq data revealed 21 viruses, 14 of which belong to putative new species. Two dsRNA viruses and an unclassified Tymovirales are formally described for the first time for Armillaria. One mitovirus occurred with a high prevalence of 71.1%, while all other viruses were much less prevalent (0.6%–16.9%). About half of all viruses were found only in one fungal species, others occurred in 2–6 fungal species. Co‐infections of 2–7 viruses per isolate were not uncommon (34.9%), and most viruses persisted circulating within fungal populations for decades. Some viruses were related to viruses associated with other Armillaria species, supporting the hypothesis that virus transmission can occur between different fungal species. Although no specific correlation between viruses and the fungal trophic strategy was found, this study opens new insights into viral diversity hidden in the soil microbiome.

Characterization of Mycoviruses in Armillaria ostoyae and A. cepistipes in the Czech Republic

“…Interestingly, isolates 1 and 7, between which virus interspecies transmission has occurred, were collected at localities approximately 50 km apart. These results suggest that ambiviruses are transmitted efficiently in Armillaria in the Czech Republic, as seems to happen in other regions of the Northern hemisphere [ 13 , 24 ], where ambi-like viruses have been found to be very common in Armillaria isolates and occur often in A. borealis and A. mellea from Finland, Siberia, and Switzerland. This efficiency could also be related to the fact that members of the genus Armillaria , as well as other fungi causing tree root rot, such as Heterobasidion spp.…”

“…Then, they were discovered in Cryphonectria parasitica [ 52 ] and many agaricomycetes including Armillaria spp. [ 13 , 24 ], Heterobasidion spp. [ 20 ], Rhizoctonia spp.…”

“…Although most viruses in the order Tymovirales are plant viruses, several members of this order are known to infect plant pathogenic fungi, including Botrytis cinerea , Fusarium boothii , Fusarium graminearum , R. solani , and S. sclerotiorum [ 62 , 63 , 64 , 65 , 66 ]. Armillaria ostoyae tymovirus 1 is the second tymovirus described within the genus Armillaria after the study of Shami et al (2004) [ 24 ].…”

“…There are important forest pathogenic fungi, such as Cryphonectria parasitica , Phytophthora spp., Ophiostoma spp., Gremmeniella abietina , Hymenoscyphus fraxineus , Heterobasidion annosum and Armillaria spp., which host mycoviruses with diverse fungus-virus relationships [ 18 , 19 , 20 ]. In Armillaria , early studies by Blattny (1973) [ 21 ] and Reaves et al (1988) [ 22 ] described the presence of virus-like particles in A. mellea and A. ostoyae , but it was not until 2021 that viruses were confirmed by molecular characterization [ 13 , 23 , 24 ].…”

“…Several positive- and negative-stranded ssRNA viruses and even two dsRNA mycoviruses have been described. Mitoviruses, ourmia-like viruses, tymoviruses, phlegiviruses, ambi-like viruses, several previously unclassified (+)ssRNA and two unclassified dsRNA viruses have been described in five different Armillaria species ( A. mellea , A. borealis , A. cepistipes , A. ostoyae , A. gallica ) [ 13 , 23 , 24 ].…”