Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus

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 <i>Vibrio</i>. However, it is unknown whether consistent <i>Vibrio</i> populations are associated with POMS in different regions, how <i>Vibrio</i> 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 <i>Vibrio harveyi</i> and <i>Vibrio rotiferianus</i> are predominant in OsHV-1-diseased oysters and that OsHV-1 drives the partition of the <i>Vibrio</i> community observed in the field. However only <i>V. harveyi</i> synergizes with OsHV-1 by promoting mutual growth and accelerating oyster death. <i>V. harveyi</i> 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, <i>V. harveyi</i> produces a key siderophore called vibrioferrin. This important resource promotes the growth of <i>V. rotiferianus</i>, which cooccurs with <i>V. harveyi</i> in diseased oysters, and behaves as a cheater by benefiting from <i>V. harveyi</i> 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.