Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oysters on the French North Atlantic coast revealed that the disease involves co-infection with the endemic ostreid herpesvirus 1 (OsHV-1) and virulent bacterial species such as Vibrio crassostreae. 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 the OsHV-1 virus during pathogenesis. We resolved the Vibrio population structure in oysters from a Mediterranean ecosystem and investigated their functions in POMS development. We find that Vibrio harveyi and Vibrio rotiferianus are the predominant species found in OsHV-1-diseased oysters and show that OsHV-1 is necessary to reproduce the partition of the Vibrio community observed in the field. By characterizing the interspecific interactions between OsHV-1, V. harveyi and V. rotiferianus, we find that only V. harveyi synergizes with OsHV-1. When co-infected, OsHV-1 and V. harveyi behave cooperatively by promoting mutual growth and accelerating oyster death. V. harveyi showed high virulence potential in oysters and dampened host cellular defenses, making oysters a more favorable niche for microbe colonization. We next investigated the interactions underlying the co-occurrence of diverse Vibrio species in diseased oysters. We found that V. harveyi harbors genes responsible for the biosynthesis and uptake of a key siderophore called vibrioferrin. This important resource promotes the growth of V. rotiferianus, a cheater that efficiently colonizes oysters during POMS without costly investment in host manipulation nor metabolite sharing. By connecting field-based approaches, laboratory infection assays and functional genomics, we have uncovered a web of interdependencies that shape the structure and function of the POMS pathobiota. We showed that cooperative behaviors contribute to synergy between bacterial and viral co-infecting partners. Additional cheating behaviors further shape the polymicrobial consortium. Controlling such behaviors or countering their effects opens new avenues for mitigating polymicrobial diseases.
The elevation of atmospheric CO2 leads to a decline in the plant mineral content, which poses a major threat to food security in the coming decades. To date, very few genes have been identified as having a role in the negative effect of elevated CO2 on plant mineral composition. Yet, several studies have shown a certain degree of diversity in the ionome's response to elevated CO2, associated with genotypic variation. This suggests the existence of genetic factors controlling the effect of CO2 on ionome composition. However, no large-scale studies have been carried out to date to explore the genetic diversity of the ionome responses to elevated CO2. Here, we used six hundred Arabidopsis thaliana accessions, representing geographical distributions ranging from worldwide to regional and local environments, to analyze the natural genetic variation underlying the negative effect of elevated CO2 on the ionome composition in plants. We show that the growth under elevated CO2 leads to a global and important decrease of the ionome content whatever the geographic distribution of the population. We also observed a high range of genetic diversity in the response of the ionome composition to elevated CO2, and we identified sub-populations, showing effects on their ionome ranging from the most pronounced to resilience or even to a benefit in response to elevated CO2. Using genome-wide association mapping on the response of each mineral element to elevated CO2 or on integrative traits, we identified a large set of QTLs and genes associated with the ionome response to elevated CO2. Finally, we demonstrate that manipulating the function of one of these genes can mitigate the negative effect of elevated CO2 on the plant mineral composition. Therefore, this resource will contribute to understand the genetic mechanisms underlying the negative effect of elevated CO2 on the mineral composition of plants, and to the development of biofortified crops adapted to a high-CO2 world.
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