Identification and Molecular Characterization of Novel Mycoviruses in Saccharomyces and Non-Saccharomyces Yeasts of Oenological Interest

Dalila Crucitti,Davide Pacifico,Daniele Oliva,Francesca La Bella,Marco Chiapello,Marco Forgia,Francesco Carimi,Massimo Turina

doi:10.3390/v14010052

Dalila Crucitti, Davide Pacifico + Show 6 more

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https://doi.org/10.3390/v14010052

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Abstract

Wine yeasts can be natural hosts for dsRNA, ssRNA viruses and retrotransposon elements. In this study, high-throughput RNA sequencing combined with bioinformatic analyses unveiled the virome associated to 16 Saccharomyces cerevisiae and 8 non-Saccharomyces strains of oenological interest. Results showed the presence of six viruses and two satellite dsRNAs from four different families, two of which—Partitiviridae and Mitoviridae—were not reported before in yeasts, as well as two ORFan contigs of viral origin. According to phylogenetic analysis, four new putative mycoviruses distributed in Totivirus, Cryspovirus, and Mitovirus genera were identified. The majority of commercial S. cerevisiae strains were confirmed to be the host for helper L-A type totiviruses and satellite M dsRNAs associated with the killer phenotype, both in single and mixed infections with L-BC totiviruses, and two viral sequences belonging to a new cryspovirus putative species discovered here for the first time. Moreover, single infection by a narnavirus 20S-related sequence was also found in one S. cerevisiae strain. Considering the non-Saccharomyces yeasts, Starmerella bacillaris hosted four RNAs of viral origin—two clustering in Totivirus and Mitovirus genera, and two ORFans with putative satellite behavior. This study confirmed the infection of wine yeasts by viruses associated with useful technological characteristics and demonstrated the presence of complex mixed infections with unpredictable biological effects.

Highlights

A wide diversity of mycoviruses has been reported in the major fungal taxa since the description of the first species in 1962 [1–3]
The majority of commercial S. cerevisiae strains were confirmed to be the host for helper L-A type totiviruses and satellite M double-stranded RNA (dsRNA) associated with the killer phenotype, both in single and mixed infections with L-BC totiviruses, and two viral sequences belonging to a new cryspovirus putative species discovered here for the first time
We identified multiple viral infections in S. bacillaris and in all S. cerevisiae strains with the exception of S. cerevisiae NDA21 and Lalvin RC212, infected only by a narnavirus and a totivirus, respectively

Summary

Introduction

A wide diversity of mycoviruses has been reported in the major fungal taxa since the description of the first species in 1962 [1–3]. The majority of fungal viruses have double-stranded RNA (dsRNA) or positive single-stranded RNA (+ssRNA) genomes, some of them have linear negative (-ssRNA) as well as circular ssDNA genomes [1]. According to the International Committee on Taxonomy of Viruses—ICTV (https://talk.ictvonline.org/taxonomy/; 2020 release, accessed on 16 December 2021)—mycoviruses with dsRNA genomes are grouped in seven families—Chrysoviridae, Endornaviridae, Megabirnaviridae, Partitiviridae, Quadriviridae, Reoviridae, Totiviridae, one genus Botybirnavirus in the kingdom Orthornavirae, and four recently established families—Amalgaviridae, Curvulaviridae, and Picobirnaviridae and Polymycoviridae. Mymonaviridae and Metaviridae families include mycoviruses with ssRNA and +ssRNA-RT genomes, respectively, while the family Genomoviridae was recently established for mycoviruses with a single-stranded DNA (ssDNA) genome [4]. Thanks to the improvement of cultivation-independent methods in virome research, new families are constantly proposed as the number of new species arises [8,11–13]

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