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Montagnani, C.

Publications and source records attributed to Montagnani, C..

3 recordsLinked to original sources

Epigenetic then genetic variations underpin rapid adaptation of oyster populations (Crassostrea gigas) to Pacific Oyster Mortality Syndrome (POMS)

Disease emergence is accelerating in response to human activity-induced global changes. Understanding the mechanisms by which host populations can rapidly adapt to this threat will be crucial for developing future management practices. Pacific Oyster Mortality Syndrome (POMS) imposes a substantial and recurrent selective pressure on oyster populations (Crassostrea gigas). Rapid adaptation to this disease may arise through both genetic and epigenetic mechanisms. In this study, we used a combination of whole exome capture of bisulfite-converted DNA, next-generation sequencing, and (epi)genome-wide association mapping, to show that natural oyster populations differentially exposed to POMS displayed signatures of selection both in their genome (single nucleotide polymorphisms) and epigenome (CG-context DNA methylation). Consistent with higher resistance to POMS, the genes targeted by genetic and epigenetic variations were mainly related to host immunity. By combining correlation analyses, DNA methylation quantitative trait loci, and variance partitioning, we revealed that a third of the observed phenotypic variation was explained by interactions between the genetic sequence and epigenetic information, [~]14% by the genetic sequence, and up to 25% by the epigenome alone. Thus, as well as genetic adaptation, epigenetic mechanisms governing immune responses contribute significantly to the rapid adaptation of hosts to emerging infectious diseases.

evolutionary biology↗

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

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.

microbiology↗

Phylogeography of infectious disease: genetic diversity and connectivity of the Ostreid herpesvirus 1 population in France

The genetic diversity of viral populations is a key driver of the spatial and temporal diffusion of viruses; yet, studying the diversity of whole genomes from natural populations still remains a challenge. Phylodynamic approaches are commonly used for RNA viruses harboring small genomes, but have only rarely been applied to DNA viruses with larger genomes. Here, we used the Pacific Oyster Mortality Syndrome (POMS, a disease that affects oyster farms around the world) as a model to study the genetic diversity of its causative agent, the Ostreid herpesvirus 1 (OsHV-1) in the three main French oyster-farming areas. Using ultra-deep sequencing on individual moribund oysters and an innovative combination of bioinformatics tools, we de novo assembled 21 OsHV-1 new genomes. Combining quantification of major and minor genetic variations, phylogenetic analysis and ancestral state reconstruction of discrete traits approaches; we assessed the connectivity of OsHV-1 viral populations between the three oyster-farming areas. Our results suggest that the Marennes- Oleron Bay represents the main source of OsHV-1 diversity, from where the virus has dispersed to other farming areas, a scenario consistent with current practices of oyster transfers in France. We demonstrate that phylodynamic approaches can be applied to aquatic DNA viruses to determine how epidemiological, immunological, and evolutionary processes act and potentially interact to shape their diversity patterns. ImportancePhylogeography is a field of research that attempts to reconstruct the relationships between individual genotypes within a species and then correlate these genealogical relationships with their geographic and temporal origin. This field of research has become an essential step in the understanding of pandemics, in particular to determine the origin, spread and evolution of a pathogen as currently illustrated in studies on viral pandemics. However, because phylogeographic analyses are based on genome variation, stable genomes yield less information than labile genomes. Accordingly, viruses with double-stranded DNA (dsDNA) genomes generally have lower nucleotide diversity than RNA viruses. In this study, by combining the use of both major and minor genetic variations with phylogeographic analyses of the oyster herpesvirus OsHV-1, we highlight genealogical relationships that are not depicted in phylogenetic trees based on consensus viral genomes only. These data offer a plausible scenario reflecting the origin and spread of OsHV-1 populations between oyster- farming sites.

microbiology↗