Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus
Daniel Oyanedel, Arnaud Lagorce, Maxime Bruto, Philippe Haffner, Amandine Morot, Yannick Labreuche, Yann Dorant, Sébastien de La Forest Divonne, François Delavat, Nicolas Inguimbert, Caroline Montagnani, Benjamín Morga, Ève Toulza, Cristian Chaparro, Jean-Michel Escoubas, Yannick Gueguen, Jérémie Vidal‐Dupiol, Julien de Lorgeril, Bruno Petton, Lionel Dégremont, Delphine Tourbiez, Léa-Lou Pimparé, Marc Leroy, Océane Romatif, Juliette Pouzadoux, Guillaume Mitta, Frédérique Le Roux, Guillaume M. Charrière, Marie‐Agnès Travers, Delphine Destoumieux‐Garzón
Abstract
Polymicrobial infections threaten the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease affecting oyster production worldwide. In the French Atlantic coast, the disease involves coinfection with ostreid herpesvirus 1 (OsHV-1) and virulent Vibrio . However, it is unknown whether consistent Vibrio populations are associated with POMS in different regions, how Vibrio contribute to POMS, and how they interact with OsHV-1 during pathogenesis. By connecting field-based approaches in a Mediterranean ecosystem, laboratory infection assays and functional genomics, we uncovered a web of interdependencies that shape the structure and function of the POMS pathobiota. We show that Vibrio harveyi and Vibrio rotiferianus are predominant in OsHV-1-diseased oysters and that OsHV-1 drives the partition of the Vibrio community observed in the field. However only V. harveyi synergizes with OsHV-1 by promoting mutual growth and accelerating oyster death. V. harveyi shows high-virulence potential and dampens oyster cellular defenses through a type 3 secretion system, making oysters a more favorable niche for microbe colonization. In addition, V. harveyi produces a key siderophore called vibrioferrin. This important resource promotes the growth of V. rotiferianus , which cooccurs with V. harveyi in diseased oysters, and behaves as a cheater by benefiting from V. harveyi metabolite sharing. Our data show that cooperative behaviors contribute to synergy between bacterial and viral coinfecting partners. Additional cheating behaviors further shape the polymicrobial consortium. Controlling cooperative behaviors or countering their effects opens avenues for mitigating polymicrobial diseases.