Darnley, J. A.; Waller, S.; French, R. K.; Parata, R.; Kumanan, K.; Finn, L.; Yick, J. L.; Kitson, J.; Cahill, P.; Davidson, I.; Hunter, R. B. J.; Newman, B.; Hutson, K. S.; Geoghegan, J. L.

Lamprey reddening syndrome (LRS) is an emerging disease affecting pouched lamprey (Geotria australis; kanakana/piharau), a culturally and ecologically significant species in Aotearoa New Zealand. Characterised by skin haemorrhaging and elevated mortality, the aetiology of LRS has remained unresolved despite previous investigations. We used a metatranscriptomic approach to characterise viral communities in 28 lamprey from New Zealand and Tasmania, Australia, comparing diseased and presumably healthy individuals. This analysis revealed eight fish-infecting RNA viruses, seven of which were novel, including two highly divergent coronaviruses. One of these coronaviruses possessed a bi-segmented genome structure, and three lamprey were co-infected with both coronaviruses. While these coronaviruses were detected in both healthy and diseased individuals, lamprey with reddening exhibited markedly higher viral abundance, driven by elevated RNA transcripts of both viruses. This pattern suggests that increased coronavirus replication in diseased individuals may be influenced by host stress to environmental factors or co-infection with other pathogens, rather than acting as a sole causative agent of disease. Beyond identifying candidate viral associations, this study expands the known virosphere of an ancient vertebrate lineage and demonstrates the utility of genomics-informed diagnostics for investigating disease in threatened wildlife.