Widespread Occurrence and Diverse Origins of Polintoviruses Influence Lineage-specific Genome Dynamics in Stony Corals

Abstract

AbstractStony corals (OrderScleractinia) are central to vital marine habitats known as coral reefs. Numerous stressors in the Anthropocene are contributing to the ongoing decline in coral reef health and coverage. While viruses are established modulators of marine microbial dynamics, their interactions within the coral holobiont and impact on coral health and physiology remain unclear. To address this key knowledge gap, we investigated diverse stony coral genomes for ‘endogenous’ viruses. Our study uncovered a remarkable number of integrated viral elements recognized as ‘Polintoviruses’ (ClassPolintoviricetes) in 30Scleractiniagenomes, with several species harboring hundreds to thousands of polintoviruses. We reveal massive paralogous expansion of polintoviruses in stony corals, alongside presence of integrated elements closely related to Polinton-like viruses (PLVs), a group of viruses that exist as free virions. These results suggest multiple integrations of polintoviruses and PLV-relatives, followed by their paralogous expansions shaped stony coral genomes. Gene expression analysis reveals all polintovirus structural and non-structural hallmark genes are expressed, strongly supporting free virion production from polintoviruses. Our results revealing a significant polintovirus diversity across theScleractiniaorder open a new research avenue into their possible roles in disease, genomic plasticity, and environmental adaptation in this key group of organisms.