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Destoumieux-Garzon, D.

Publications and source records attributed to Destoumieux-Garzon, D..

11 recordsLinked to original sources

Diversity and predation capacities of Amoebozoa against opportunistic vibrios in contrasting Mediterranean coastal environments.

Free-living amoebae (FLA) are ubiquitous and can be found in many types of environments including soil, freshwater, air and marine environments. They feed on various microorganisms and can play an important role in the food web and its dynamics. We previously described that FLAs belonging to the Vannella genus from the oyster farming area of the Thau lagoon in France could establish stable interactions with Vibrionaceae and could play a role in the selection of some virulence factors, potentially influencing pathogen dynamics. To further investigate the ecological interactions between FLA populations and Vibrionaceae in Mediterranean coastal waters, we conducted monthly sampling for one year at three contrasting sites. Free-living amoebae populations were isolated by culturing water and sediment samples on different bacterial lawns, including E. coli or V. tasmaniensis, V. crassostreae and V. harveyi. Amoebozoan diversity was analyzed using v4-18S barcoding and revealed distinct communities between the sediment and the water column, with Vannellidae significantly enriched in the water column whereas Paramoebidae were significantly enriched in the sediments. Selection of grazers on different bacterial lawns revealed that V. tasmaniensis inhibited the growth of most Vannellidae, whereas V. crassostreae inhibited the growth of a large proportion of Paramoebidae. These differences were further confirmed in functional grazing assays using isolates belonging to each Amoebozoa taxonomic group. Overall, our results highlight the need for more comprehensive studies of the diversity and population dynamics of Amoebozoa in marine environments, and that the role of these diversified grazers in shaping vibrio communities is complex and still poorly characterized.

microbiology↗

Starvation of the bacteria Vibrio atlanticus promotes lightning group-attacks on the dinoflagellate Alexandrium pacificum

Phytoplankton serve as a source of nutrients for bacteria in the marine environment. The interactions between algae and bacteria are known to include mutualism, commensalism, competition or antagonism. This occurs in the microenvironment surrounding phytoplankton cells, the phycosphere, an interface rich in nutrients and organic molecules exuded by the cell. Here, based on in situ observations and on an in vitro interaction study, we report on a novel form of starvation-induced hunting that the cells of selected Vibrio species exert on dinoflagellates. The results showed that Vibrio atlanticus was capable of attacking and killing the dinoflagellate Alexandrium pacificum ACT03. Briefly, the observed mechanism of algal-killing consists of first, the immobilization stage involving the secretion of algicidal metabolites that disrupt the flagella of the algae. In the attack stage, Vibrios simultaneously surround algal cells at high density for a brief period without invading them. Finally, the killing stage in which the lysis and consumption of the dinoflagellates occur. By using a combination of biochemical, proteomic, molecular and fluorescence microscopy approaches, we showed that this relationship is not related to the decomposition of algal organic matter, Vibrio quorum sensing pathways, toxicity of the algae or pathogenicity of the bacterium but is conditioned by nutrient stress, iron availability and linked to the iron-vibrioferrin transport system of Vibrio atlanticus. This is the first evidence of a new mechanism that could be involved in regulating Alexandrium spp. blooms and giving Vibrio a competitive advantage in obtaining nutrients from the environment. The interaction model we propose here suggests that Vibrio could play a role in regulating the proliferation of Alexandrium spp., giving it a competitive advantage in obtaining nutrients from the environment.

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↗

Diversity and functional specialization of oyster immune cells uncovered by integrative single cell level investigations

Mollusks are a major component of animal biodiversity and play a critical role in ecosystems and global food security. The Pacific oyster, Crassostrea (Magallana) gigas, is the most farmed bivalve mollusk in the world and is becoming a model species for invertebrate biology. Despite the extensive research on hemocytes, the immune cells of bivalves, their characterization remains elusive. Here we were able to extensively characterize the diverse hemocytes and identified at least seven functionally distinct cell types and three hematopoietic lineages. A combination of single-cell RNA sequencing, quantitative cytology, cell sorting, functional assays and pseudo-time analyses was used to deliver a comprehensive view of the distinct hemocyte types. This integrative analysis enabled us to reconcile molecular and cellular data and identify distinct cell types performing specialized immune functions, such as phagocytosis, reactive oxygen species production, copper accumulation, and expression of antimicrobial peptides. This study emphasized the need for more in depth studies of cellular immunity in mollusks and non-model invertebrates and set the ground for further comparative immunology studies at the cellular level.

immunology↗

Marine transmissible cancer navigates urbanised waters, threatening to spillover

Inter-individual transmission of cancer cells represents a unique form of microparasites increasingly reported in marine bivalves. In this study, we sought to understand the ecology of the propagation of Mytilus trossulus Bivalve Transmissible Neoplasia 2 (MtrBTN2), a transmissible cancer affecting four Mytilus mussel species worldwide. We investigated the prevalence of MtrBTN2 in the mosaic hybrid zone of M. edulis and M. galloprovincialis along the French Atlantic coast, sampling contrasting natural and anthropogenic habitats. We observed a similar prevalence in both species, likely due to the spatial proximity of the two species in this region. Our results showed that ports had higher prevalence of MtrBTN2, with a possible hotspot observed at a shuttle landing dock. No cancer was found in natural beds except for two sites close to the hotspot, suggesting spillover. Ports may provide favourable conditions for the transmission of MtrBTN2, such as high mussel density, stressful conditions, sheltered and confined shores, or buffered temperatures. Ships may also spread the disease through biofouling. Our results suggest ports may serve as epidemiological hubs, with maritime routes providing artificial gateways for MtrBTN2 propagation. This highlights the importance of preventing biofouling on docks and ship hulls to limit the spread of marine pathogens hosted by fouling species.

ecology↗

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↗

Transcriptomics of mussel transmissible cancer MtrBTN2 reveals accumulation of multiple cancerous traits and oncogenic pathways shared among bilaterians

Transmissible cancer cell lines are rare biological entities giving rise to diseases at the crossroads of cancer and parasitic diseases. These malignant cells have acquired the amazing capacity to spread from host to host. They have been described only in dogs, Tasmanian devils and marine bivalves. The Mytilus trossulus Bivalve Transmissible Neoplasia 2 (MtrBTN2) lineage has even acquired the capacity to spread inter-specifically between marine mussels of the Mytilus edulis complex worldwide. To identify the oncogenic processes underpinning the biology of these atypical cancers we performed transcriptomics of MtrBTN2 cells. Differential expression, enrichment, protein-protein interaction network, and targeted analyses were used. Overall, our results suggest the accumulation of multiple cancerous traits that way be linked to the long-term evolution of MtrBTN2. We also highlight that vertebrate and lophotrochozoan cancers could share a large panel of common drivers, which supports the hypothesis of an ancient origin of oncogenic processes in bilaterians.

cancer biology↗

Emergence and clonal expansion in Europe of Vibrio aestuarianus lineages pathogenic for oysters

Crassostrea gigas oysters represent a significant global food source, with 4.7 million tons harvested per year. In 2001, the bacterium V. aesturianus francensis emerged as a pathogen that causes adult oyster mortality in France and Ireland. Its impact on oyster aquaculture has increased in Europe since its reemergence in 2012. To better understand the evolutionary mechanisms leading to the emergence and persistence over time of this pathogen, we conducted a survey of mollusk diseases through national reference laboratories (NRLs) across Europe. We analyzed 54 new genomes of V. aestuarianus (Va) isolated from multiple environmental compartments since 2001, in areas with and without bivalve mortalities. We used a combination of comparative genomics and population genetics approaches to show that Va francensis lineages have undergone clonal expansion in Europe, likely after a recent selective bottleneck. Low mutation and recombination rates may have selected particular virulent genotypes. Furthermore, we identified a specific cus-cop-containing island conferring copper resistance to Va francensis whose acquisition may have favored the emergence of pathogenic lineages adapted to oysters.

microbiology↗

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN), both emerged in a M. trossulus founder individual, have been described to date (MtrBTN1 and MtrBTN2). Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping hundred SNPs of thousands of European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts -M. edulis, M. galloprovincialis or hybrids- and the genotype of tumors of heavily infected individuals. In addition, a subset of individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M. edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found but a few individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two divergent sublineages, confirmed by mtCOI sequences, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

evolutionary biology↗

Microbial predator-prey interactions could favor coincidental selection of diverse virulence factors in marine coastal waters.

Vibrios are ubiquitous in marine environments and opportunistically colonize a broad range of hosts. Strains of Vibrio tasmaniensis present in oyster farms can thrive in oysters during juvenile mortality events. Among them, V. tasmaniensis LGP32 behaves as a facultative intracellular pathogen of oyster hemocytes, a property rather unusual in vibrios. Herein, we asked whether LGP32 resistance to phagocytosis could result from coincidental selection of virulence factors during interactions with heterotrophic protists, such as amoeba, in the environment. To answer that question, we developed an integrative study, from the first description of amoeba diversity in oyster-farming areas to the characterization of LGP32 interactions with amoebae of the Vannella genus that were found abundant in the oyster environment. LGP32 was shown to be resistant to grazing by amoebae and this phenotype was dependent on previously identified virulence factors: the secreted metalloprotease Vsm and the copper efflux p-ATPase CopA. Using dedicated in vitro assays, our results showed that these virulence factors act at different steps during amoeba-vibrio interactions than they do in oysters-vibrio interactions. Hence, the virulence factors of LGP32 are key determinants of biotic interactions with multiple hosts ranging from protozoans to metazoans, suggesting that the selective pressure exerted by amoebae in marine coastal environments favor coincidental selection of virulence factors.

microbiology↗