Endogenous viral elements reveal associations between a non-retroviral RNA virus and symbiotic dinoflagellate genomes

Alex Veglia , Kalia Bistolas , Christian Voolstra (1) , Benjamin Hume (1) , Hans-Joachim Ruscheweyh (2) , Serge Planes (3) , Denis Allemand (4) , Emilie Boissin (3) , Patrick Wincker (5, 6) , Julie Poulain (6, 5) , Clémentine Moulin (7) , Guillaume Bourdin (8) , Guillaume Iwankow (3) , Sarah Romac (5, 9) , Sylvain Agostini (10) , Bernard Banaigs (3) , Emmanuel Boss (8) , Chris Bowler (5, 11) , Colomban de Vargas (12) , Éric Douville (13, 14) , Michel Flores (15) , Didier Forcioli , Paola Furla , Pierre Galand (16) , Eric Gilson , Fabien Lombard (17) , Stéphane Pesant , Stéphanie Reynaud , Shinichi Sunagawa , Olivier Thomas , Romain Troublé , Didier Zoccola , Adrienne Correa , Rebecca Vega Thurber

1 Universität Konstanz
2 D-BIOL - Department of Biology [ETH Zürich]
3 CRIOBE - Centre de recherches insulaires et observatoire de l'environnement
4 LIA ROPSE - Laboratoire International Associé Réponse des Organismes et Populations face au Stress Environnemental - Université Côte d’Azur - Centre Scientifique de Monaco
5 GOSEE - Global Oceans Systems Ecology & Evolution - Tara Oceans
6 UMR 8030 - Génomique métabolique
7 Fondation Tara Ocean
8 University of Maine
9 SBR - Station biologique de Roscoff = Roscoff Marine Station
10 Shimoda Marine Research Center
11 IBENS - Institut de biologie de l'ENS Paris
12 ADMM - Adaptation et diversité en milieu marin
13 LSCE - Laboratoire des Sciences du Climat et de l'Environnement [Gif-sur-Yvette]
14 GEOTRAC - Géochrononologie Traceurs Archéométrie
15 Weizmann Institute of Science [Rehovot, Israël]
16 LECOB - Laboratoire d'Ecogéochimie des environnements benthiques
17 LOV - Laboratoire d'océanographie de Villefranche

Abstract Endogenous viral elements (EVEs) offer insight into the evolutionary histories and hosts of contemporary viruses. This study leveraged DNA metagenomics and genomics to detect and infer the host of a non-retroviral dinoflagellate-infecting +ssRNA virus (dinoRNAV) common in coral reefs. As part of the Tara Pacific Expedition, this study surveyed 269 newly sequenced cnidarians and their resident symbiotic dinoflagellates (Symbiodiniaceae), associated metabarcodes, and publicly available metagenomes, revealing 178 dinoRNAV EVEs, predominantly among hydrocoral-dinoflagellate metagenomes. Putative associations between Symbiodiniaceae and dinoRNAV EVEs were corroborated by the characterization of dinoRNAV-like sequences in 17 of 18 scaffold-scale and one chromosome-scale dinoflagellate genome assembly, flanked by characteristically cellular sequences and in proximity to retroelements, suggesting potential mechanisms of integration. EVEs were not detected in dinoflagellate-free (aposymbiotic) cnidarian genome assemblies, including stony corals, hydrocorals, jellyfish, or seawater. The pervasive nature of dinoRNAV EVEs within dinoflagellate genomes (especially Symbiodinium ), as well as their inconsistent within-genome distribution and fragmented nature, suggest ancestral or recurrent integration of this virus with variable conservation. Broadly, these findings illustrate how +ssRNA viruses may obscure their genomes as members of nested symbioses, with implications for host evolution, exaptation, and immunity in the context of reef health and disease.

Domains: Environmental Sciences

Alex Veglia, Kalia Bistolas, Christian Voolstra, Benjamin Hume, Hans-Joachim Ruscheweyh, et al.. Endogenous viral elements reveal associations between a non-retroviral RNA virus and symbiotic dinoflagellate genomes. Communications Biology, 2023, 6 (1), pp.566. ⟨10.1038/s42003-023-04917-9⟩. ⟨hal-04176296⟩