The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating non‐retroviral RNA viruses in fungi

Abstract

Arbuscular Mycorrhizal Fungi (AMF) are key components of the plant microbiota. AMF genetic complexity is increased by the presence of endobacteria, which live inside many species. A further component of such complexity is the virome associated to AMF, whose knowledge is still very limited. Here, by exploiting transcriptomic data we describe the virome of Gigaspora margarita. A BLAST search for viral RNA-dependent RNA polymerases sequences allowed the identification of four mitoviruses, one Ourmia-like narnavirus, one Giardia-like virus, and two sequences related to Fusarium graminearum mycoviruses. Northern blot and RT-PCR confirmed the authenticity of all the sequences with the exception of the F. graminearum-related ones. All the mitoviruses are replicative and functional since both positive strand and negative strand RNA are present. The abundance of the viral RNA molecules is not regulated by the presence or absence of Candidatus Glomeribacter gigasporarum, the endobacterium hosted by G. margarita, with the exception of the Ourmia-like sequence which is absent in bacteria-cured spores. In addition, we report, for the first time, DNA fragments corresponding to mitovirus sequences associated to the presence of viral RNA. These sequences are not integrated in the mitochondrial DNA and preliminary evidence seems to exclude integration in the nuclear genome.

Biological and Molecular Characterization of Chenopodium quinoa Mitovirus 1 Reveals a Distinct Small RNA Response Compared to Those of Cytoplasmic RNA Viruses

“…Their wide diversity warrants the establishment of a family taxon called Mitoviridae, separated from the family Narnaviridae. The newly established family would comprise a number of subfamilies and genera, including the very distantly related mitovirus species characterized from the arbuscular mycorrhyzal fungus Gigaspora margarita, which are included in a clade basal to existing characterized mitoviruses (37). As already observed by other authors (17), plant mitoviruses are nested in a specific fungal mitovirus clade, raising questions about the evolutionary trajectory of plant mitoviruses, which has been discussed at length elsewhere (17).…”

Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants

“…Despite classic mitoviruses typically show genome sizes of about 2.3–2.7 kb, we identified two viral contigs which are phylogenetically related to mitoviruses but which showed genome of 3067 (Alternaria alternata mitovirus 1) and 3520 (Epicoccum nigrum mitovirus 1) nucleotides (both encoding only for the RdRp). Mitoviruses of similar genomic size were also previously reported for the arbuscular mycorrhizal fungus Gigaspora margarita (Turina et al ., ).…”

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

“…For example, the endobacterium Candidatus Glomeribacter gigasporarum was shown to increase sporulation, ATP production, reactive oxygen detoxification and responsiveness to the plant signal strigolactones of the fungal host, G. margarita (Salvioli et al ., ). In addition, viruses can thrive inside AMF, yet our knowledge on the AMF virome is limited to few AMF species (Ikeda et al ., ; Kitahara et al ., ; Turina et al ., ). In particular, Ikeda et al .…”

“…Tansley review New Phytologist fungal host, G. margarita . In addition, viruses can thrive inside AMF, yet our knowledge on the AMF virome is limited to few AMF species (Ikeda et al, 2012;Kitahara et al, 2014;Turina et al, 2018). In particular, Ikeda et al (2012) demonstrated that a virus-free fungal strain produced more spores and promoted plant growth more efficiently than the viruscontaining strain.…”