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Petton, B.

Publications and source records attributed to Petton, B..

12 recordsLinked to original sources

Multi-Omics Reprogramming Drives a Counterintuitive Reversal of Disease Susceptibility During Ageing

Ageing is a progressive and irreversible biological process characterized by the deterioration of physiological functions and increased vulnerability to mortality. Although extensively studied in vertebrates, ageing in long-lived invertebrates remains comparatively unexplored. While ageing typically leads to greater susceptibility to infectious diseases, a striking and unexpected reversal was identified in oysters: older oysters exhibit markedly increased tolerance to the Pacific Oyster Mortality Syndrome (POMS), a panzootic disease primarily driven by the OsHV-1 herpesvirus and responsible for severe losses in global aquaculture. To investigate this counterintuitive pattern, we challenged oysters aged 4, 16, and 28 months from four biparental families and conducted an integrative multi-omics analysis, including epigenomics, transcriptomics, and metabolomics on the two families showing the strongest age-related increase in survival. Our results reveal that ageing in Magallana gigas is characterized by coordinated epigenetic, transcriptional, and metabolic reprogramming that reduces host permissiveness to POMS. We show that the epigenetic remodeling of key immune regulators (e.g., Toll-like receptors, MyD88) aligns with transcriptional rewiring of NF-{kappa}B and ubiquitin pathways, producing a finely tuned innate immune state marked by enhanced antiviral activity but reduced antibacterial responsiveness. We also identify age-related repression of mTOR signaling, likely promoting autophagy and improving viral control. These regulatory changes are tightly linked to metabolic adjustments, including reduced TCA cycle flux, remodeled nitrogen metabolism, and altered glutathione dynamics, which collectively support a stress-tolerant, energy-conserving phenotype. Together, our findings reveal a fundamental evolutionary trade-off: juveniles prioritize growth at the cost of viral susceptibility, whereas adults invest in cellular maintenance and antiviral preparedness.

genomics↗

Bacteria with antibacterial activities isolated from Magallana gigas microbiota as potential probiotics against Vibrio aestuarianus infections in oyster farming

IntroductionOyster farming is a significant industry worldwide, but it is threatened by various diseases such as Pacific Oyster Mortality Syndrome or vibriosis. V. aestuarianus is a major cause of mortality for market-size oysters, resulting in significant economic losses for oyster farmers. Among the various control methods developed, probiotics appear to be a promising approach. More specifically, the use of the antibacterial activity of bacteria from the natural microbiota of the oyster Magallana gigas appears to be a sustainable solution against V. aestuarianus infections. ResultsOur study investigated the probiotic potential of bacteria isolated from the microbiota of M. gigas oysters. We screened a collection of 334 bacteria against eight target pathogens, including V. aestuarianus, and identified 78 bacteria with antibacterial activity for which eight retained this activity in their culture supernatants. Five strains were selected for further testing and exposed to oysters prior to V. aestuarianus infection. Our results show that four strains significantly reduced oyster mortality, with a maximum reduction of 70%. In addition, changes in oyster microbiota composition were observed following exposure, but the administered bacteria were not detected in the microbiota. ConclusionOur findings demonstrate the potential of oyster microbiota-derived bacteria as probiotics for disease control in oyster farming. This approach could provide a sustainable and environmentally friendly solution for the oyster farming industry. Further research is needed to understand the underlying mechanisms and to develop effective probiotic-based strategies for preventing V. aestuarianus infection.

microbiology↗

Vibrio are a potential source of novel colistin-resistance genes in European coastal environments

Colistin is a widespread last resort antibiotic for treatment of multidrug-resistant bacteria. The recent worldwide emergence of colistin resistance (Col-R) conferred by mcr-1 in human pathogens has raised concern, but the putative sources and reservoirs of novel mcr genes in the marine environment remain underexplored. We observed a high prevalence of Col-R, particularly in Vibrio isolated from European coastal waters by using a unique stock of specific-pathogen-free (SPF) oysters as a bioaccumulator. The high sequence diversity found in the mcr/eptA gene family was geographically structured, particularly for three novel eptA gene variants, which were restricted to the Mediterranean (France, Spain) and occurred as a dgkA-eptA operon controlled by the RstA/RstB two component system. By analyzing 29427 Vibrionaceae genome assemblies, we showed that this mechanism of intrinsic resistance is prevalent and specific to the Harveyi clade, which includes strains of Vibrio parahaemolyticus and Vibrio alginolyticus causing infections in humans. The operon conferred colistin-resistance when transferred to sensitive non-Vibrio strains. While mcr-and arn-based Col-R mechanisms were also identified, the widespread presence of eptA gene variants in Vibrio suggests they play a key role in intrinsic resistance to colistin. Beyond these ancient eptA gene copies having evolved with the Vibrio lineage, we also identified mobile eptA paralogues that have been recently transferred between and within Vibrio clades. This highlights Vibrio as a potential source of Col-R mechanisms, emphasizing the need for enhanced surveillance to prevent colistin-resistant infections in coastal areas.

microbiology↗

Microbial education plays a crucial role in harnessing the beneficial properties of microbiota for infectious disease protection in Crassostrea gigas

BackgroundRecently, the frequency and severity of marine diseases have increased in association with global changes, and molluscs of economic interest are particularly concerned. Among them, the Pacific oyster (Crassostrea gigas) production faces challenges from several diseases such as the Pacific Oyster Mortality Syndrome (POMS) or vibriosis. Various strategies such as genetic selection or immune priming have been developed to fight some of these infectious diseases. The microbial education, which consist of exposing the host immune system to beneficial microorganisms during early life stages is a promising approach against diseases. This study explores the concept of microbial education using controlled and pathogen-free bacterial communities and assesses its protective effects against POMS and Vibrio aestuarianus infections, highlighting potential applications in oyster production. ResultsWe demonstrate that it is possible to educate the oyster immune system by adding microorganisms during the larval stage. Adding culture based bacterial mixes to larvae protects only against the POMS disease while adding whole microbial communities from oyster donors protects against both POMS and vibriosis. The efficiency of the immune protection depends both on oyster origin and on the composition of the bacterial mixes used for exposure. No preferential protection was observed when the oysters were stimulated with their sympatric strains. We further show that the added bacteria were not maintained in the oyster microbiota after the exposure, but this bacterial addition induced long term changes in the microbiota composition and oyster immune gene expression. ConclusionOur study reveals successful immune system education of oysters by introducing beneficial micro-organisms during the larval stage. We improved the long-term resistance of oysters against critical diseases (POMS disease and Vibrio aestuarianus infections) highlighting the potential of microbial education in aquaculture.

microbiology↗

Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus

The increase of the frequency and severity of marine diseases affecting farmed marine mollusks are currently threatening the sustainability of this aquaculture sector, with few available prophylactic or therapeutic solutions. Recent advances have shown that the innate immune system of invertebrates can develop memory mechanisms allowing for efficient protection against pathogens. These properties have been called innate immune memory, immune priming or trained immunity. Previous results demonstrated the possibility to elicit antiviral immune priming to protect Pacific oysters against the ostreid herpes virus 1 (OsHV-1), currently plaguing M. gigas production worldwide. Here, we demonstrate that UV-inactivated OsHV-1 is also a potent elicitor of immune priming. Previous exposure to the inactivated virus was able to efficiently protect oysters against OsHV-1, significantly increasing oyster survival. We demonstrate that this exposure blocked viral replication and was able to induce antiviral gene expression potentially involved in controlling the infection. Finally, we show that this phenomenon can persist for at least 3 months, suggesting the induction of innate immune memory mechanisms. This study unravels new ways to train the Pacific oyster immune system that could represent an opportunity to develop new prophylactic strategies to improve health and to sustain the development of marine mollusk aquaculture.

immunology↗

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↗

Profiling of N6-methyladenosine dynamics indicates regulation of oyster development by m6A-RNA epitranscriptomes

The N6-methylation of RNA adenosines (m6A) is an important regulator of gene expression with critical implications in vertebrate and insect development. However, the developmental significance of epitranscriptomes in lophotrochozoan organisms remains unknown. Using MeRIP-seq, we generated transcriptome-wide m6A-RNA methylomes covering the whole development of the oyster from oocytes to juveniles. Oyster RNA classes display specific m6A signatures, with mRNAs and lncRNAs exhibiting distinct profiles and being highly methylated compared to transposon transcripts. Epitranscriptomes are dynamic and correspond to chronological steps of development (cleavage, gastrulation, organogenesis and metamorphosis), with a minimal mRNA and lncRNA methylation at the morula stage followed by a global increase. mRNA m6A levels are correlated to transcript levels and shifts in methyladenine profiles correspond to expression kinetics. Differentially methylated transcripts cluster according to embryo-larval stages and bear the corresponding developmental functions (cell division, signal transduction, morphogenesis and cell differentiation). The m6A level of transposon transcripts is also regulated and peaks during the gastrulation. We demonstrate that m6A-RNA methylomes are dynamic and associated to gene expression regulation during oyster development. The putative epitranscriptome implication in the cleavage, maternal-to-zygotic transition and cell differentiation in a lophotrochozoan model brings new insights into the control and evolution of developmental processes

genomics↗

Genetic determinism of phage-bacteria coevolution in natural populations

Coevolution between bacteriophage (or phage) and their bacterial host is thought to be key for the coexistence of these antagonists. Recent studies have revealed the major role of mobile genetic elements in the emergence of phage resistant hosts but how phage escape these defenses in the wild remained to be explored. Here we show a striking parallel in phage evolving counter defenses to host defenses in natural population. We established a large collection of phages and their bacterial hosts and we explored the genetic structure of their interaction. We find that clearly delineated genomic clusters of phage are specific for distinct clades within a bacterial species, Vibrio crassostreae, yet while all phages can adsorb, only a subset of hosts are killed due to intracellular defense mechanisms. Host genomes contain multiple mobile defense genes and susceptibility to phage is negatively correlated with genome size. Phages also display extensive gene content variation, but their genome size remains conserved. We show that this gene content variation in hosts and phage is due to rapid turnover of genes involved in defense and escape, and that by exchanging anti-defense genes, phages irreversibly switch host. This could be indicative of co-evolution following the matching-allele-model of specificity and the spatial and temporal variability of phage infectivity further suggests that negative-frequency dependent selection drives phage-vibrio coevolutionary dynamics. We propose a "pan-escape system" that can be shared among phages by homologous recombination within a population that infects a bacterial host.

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↗

A core of functionally complementary bacteria colonizes oysters in Pacific Oyster Mortality Syndrome.

BackgroundThe Pacific oyster Crassostrea gigas is one of the main cultivated invertebrate species worldwide. Since 2008, oyster juveniles have been confronted with a lethal syndrome known as the Pacific Oyster Mortality Syndrome (POMS). POMS is a polymicrobial disease initiated by a primary infection with the herpesvirus OsHV-1 Var that creates an oyster immunocompromised state and evolves towards a secondary fatal bacteremia. In the present article, we describe the implementation of an unprecedented combination of metabarcoding and metatranscriptomic approaches to show that the sequence of events in POMS pathogenesis is conserved across infectious environments. We also identified a core bacterial consortium which, together with OsHV-1 Var, forms the POMS pathobiota. This bacterial consortium is characterized by high transcriptional activities and complementary metabolic functions to exploit hosts resources. A significant metabolic specificity was highlighted at the bacterial genus level, suggesting low competition for nutrients between members of the core bacteria. Lack of metabolic competition might favor complementary colonization of host tissues and contribute to the conservation of the POMS pathobiota across distinct infectious environments.

microbiology↗

Diversity and stability of microbiota are key factors associated to healthy and diseased Crassostrea gigas oysters

Pacific Oyster Mortality Syndrome (POMS) affects Crassostrea gigas oysters worldwide and caused important economic losses. Disease dynamics was recently deciphered and revealed a multiple and progressive infection caused by the Ostreid herpesvirus OsHV-1 {micro}Var, triggering an immunosuppression followed by microbiota destabilization and bacteraemia by opportunistic bacterial pathogens. However, it remains unknown if microbiota might participate to oyster protection to POMS, and if microbiota characteristics might be predictive of oyster mortalities. To tackle this issue, we transferred full-sib progenies of resistant and susceptible oyster families from hatchery to the field during a period in favour of POMS. After five days of transplantation, oysters from each family were either sampled for individual microbiota analyses using 16S rRNA gene-metabarcoding or transferred into facilities to record their survival using controlled condition. As expected, all oysters from susceptible families died, and all oysters from the resistant family survived. Quantification of OsHV-1 and bacteria showed that five days of transplantation was long enough to contaminate oysters by POMS, but not for entering the pathogenesis process. Thus, it was possible to compare microbiota characteristics between resistant and susceptible oyster families at the early steps of infection. Strikingly, we found that microbiota evenness and abundances of Cyanobacteria (Subsection III, family I), Mycoplasmataceae, Rhodobacteraceae, and Rhodospirillaceae were significantly different between resistant and susceptible oyster families. We concluded that these microbiota characteristics might predict oyster mortalities.

microbiology↗