Apis mellifera Solinvivirus-1, a Novel Honey Bee Virus That Remained Undetected for over a Decade, Is Widespread in the USA

Eugene V Ryabov; Anthony J Nearman; Ashrafun Nessa; Kyle Grubbs; Benjamin Sallmann; Rachel Fahey; Mikayla E Wilson; Karen D Rennich; Nathalie Steinhauer; Anne Marie Fauvel; Yanping Chen; Jay D Evans; Dennis vanEngelsdorp

doi:10.3390/v15071597

Apis mellifera Solinvivirus-1, a Novel Honey Bee Virus That Remained Undetected for over a Decade, Is Widespread in the USA

Viruses. 2023 Jul 21;15(7):1597. doi: 10.3390/v15071597.

Authors

Eugene V Ryabov^{1

2}, Anthony J Nearman¹, Ashrafun Nessa¹, Kyle Grubbs², Benjamin Sallmann^{3

4

5}, Rachel Fahey¹, Mikayla E Wilson¹, Karen D Rennich¹, Nathalie Steinhauer^{1

3}, Anne Marie Fauvel^{1

3}, Yanping Chen², Jay D Evans², Dennis vanEngelsdorp¹

Affiliations

¹ Department of Entomology, University of Maryland, College Park, MD 20742, USA.
² Bee Research Laboratory, USDA-Agricultural Research Service, Beltsville, MD 20705, USA.
³ Bee Informed Partnership, College Park, MD 20742, USA.
⁴ Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA.
⁵ Department of Entomology, University of Minnesota, St. Paul, MN 55108, USA.

Abstract

A metagenomic analysis of the virome of honey bees (Apis mellifera) from an apiary with high rates of unexplained colony losses identified a novel RNA virus. The virus, which was named Apis mellifera solinvivirus 1 (AmSV1), contains a 10.6 kb positive-strand genomic RNA with a single ORF coding for a polyprotein with the protease, helicase, and RNA-dependent RNA polymerase domains, as well as a single jelly-roll structural protein domain, showing highest similarity with viruses in the family Solinviviridae. The injection of honey bee pupae with AmSV1 preparation showed an increase in virus titer and the accumulation of the negative-strand of AmSV1 RNA 3 days after injection, indicating the replication of AmSV1. In the infected worker bees, AmSV1 was present in heads, thoraxes, and abdomens, indicating that this virus causes systemic infection. An analysis of the geographic and historic distribution of AmSV1, using over 900 apiary samples collected across the United States, showed AmSV1 presence since at least 2010. In the year 2021, AmSV1 was detected in 10.45% of apiaries (95%CI: 8.41-12.79%), mostly sampled in June and July in Northwestern and Northeastern United States. The diagnostic methods and information on the AmSV1 distribution will be used to investigate the connection of AmSV1 to honey bee colony losses.

Keywords: Apis mellifera; RNA virus; family Solinviviridae; honey bee; honey bee colony losses; insect; pollination service.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Bees / genetics
Metagenome
RNA
RNA Viruses* / genetics
United States

Substances

RNA

Grants and funding

This research was funded by United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) grant 2017-06481 (EVR, YC and JDE); the USDA Animal and Plant Health Inspection Service (APHIS) agreements 19-8130-0745-IA and 18-8130-0787-IA; funding for the USDA APHIS National Honey Bee Pest and Disease Surveys include agreements 14-8100-1624-CA, and AP21PPQHQ000C017. YC and JDE are supported in part by funding from the U.S. Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS) fund #23-8130-0960.