Oral Presentation 12th Australasian Virology Society Meeting 2024

Extending the evolutionary history of disease-causing RNA viruses (#44)

Mary E Petrone 1 2 , Joe Grove 3 , Rhys H Parry 4 , Julien Mélade 1 , Jonathon CO Mifsud 1 , Kate Van Brussel 1 , Ian Vorhees 5 6 , Zoe T Richards 7 8 , Ezequiel M Marzinelli 9 , Edward C Holmes 1 2
  1. School of Medical Sciences, The University of Sydney, Sydney, NSW, Australia
  2. Laboratory of Data Discovery for Health Limited, Hong Kong, China
  3. MRC University of Glasgow Centre for Virus Research, Glasgow, UK
  4. School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia
  5. Baker Institute for Animal Health, Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
  6. Vir Biotechnology, San Francisco, California, USA
  7. Coral Conservation and Research Group, Trace and Environmental DNA Laboratory, School of Molecular and Life Sciences, Curtin University, Perth, Western Australia, Australia
  8. Collections and Research, Western Australian Museum, Welshpool, Western Australia, Australia
  9. School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia

RNA viruses that cause disease in humans and other vertebrates comprise a tiny fraction of the RNA virosphere. This is due, in part, to the more recent evolution of vertebrate hosts (~800Mya) compared to that of the first animals: marine invertebrates (~1200Mya). To address fundamental questions about the origins of disease-causing RNA viruses and the evolutionary patterns that shaped them, we used total RNA sequencing to discover and characterise novel viruses associated with marine invertebrates. We identified divergent viruses belonging to the order Articulavirales in the metatranscriptomes of Australian corals. These, combined with additional viruses associated with marine invertebrates, formed a novel family (the “Cnidenomoviridae”). The phylogenetic placement of this family suggested that the Articulavirales underwent an aquatic to terrestrial transition hundreds of millions of years ago. We discovered influenza-like viruses associated with fish and tunicates (Urochordata), indicating that influenza viruses may have undergone a similar transition. The association of influenza viruses with Urochordata, which form the sister taxa to vertebrates in the Chordata, is the first documented evidence of invertebrate-associated influenza-like viruses and suggests that this genus emerged before the evolution of vertebrates. To investigate patterns in the evolution of RNA virus genome size, we characterised a novel ~40kb flavi-like virus associated with an Australian sea sponge. This is the longest known RNA virus outside of the order the Nidovirales and the longest to encode a single polyprotein. We did not detect a known error-correcting mechanism in its genome, suggesting that RNA viruses have evolved multiple strategies for overcoming constraints on their genome size. Given that life likely first evolved in the ocean, so too did RNA viruses. Thus, viruses that infect marine invertebrates represent vestiges of the ancestors of vertebrate pathogens and therefore provide powerful insight into the long-term evolutionary history of viruses that cause disease today.