Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection

Fallet, Manon; Montagnani, Caroline; Petton, Bruno; Lorgeril, Julien de; Comarmond, Sébastien; Chaparro, Cristian; Toulza, Ève; Boitard, Simon; Escoubas, Jean-Michel; Vergnes, Agnès; Grand, Jacqueline Le; Bulla, Ingo; Gueguen, Yannick; Vidal-Dupiol, Jérémie; Grunau, Christoph; Mitta, Guillaume; Cosseau, Céline

doi:10.21203/rs.3.rs-1366702/v1

Cited by 4 publications

(13 citation statements)

References 43 publications

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“…POMS has been observed in all coastal regions of France [3][4][5] and numerous other countries worldwide [1,[6][7][8][9][10]. Multiple factors contribute to the disease and its severity including seawater temperature, oyster genetics, oyster age, microbiota and infectious agents [11][12][13][14][15][16][17][18]. Thus, dramatic POMS mortality events have coincided with the recurrent detection of Ostreid herpesvirus variants in moribund oysters [3][4][5] as well as bacterial strains of the genus Vibrio [19,20].…”

Section: Introductionmentioning

confidence: 99%

A core of functional complementary bacteria infects oysters in Pacific Oyster Mortality Syndrome

Lucasson

Luo

Mortaza

et al. 2020

Preprint

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The Pacific oyster Crassostrea gigas is one of the main cultivated invertebrate species around the world. Since 2008, oyster juveniles have been confronted with a lethal syndrome, Pacific Oyster Mortality Syndrome (POMS). The etiology of POMS is complex. Recently, we demonstrated that POMS is a polymicrobial disease. It is initiated by a primary infection with the herpesvirus OsHV-1 μ Var, and evolves towards a secondary fatal bacteremia that is enabled by the oyster’s immunocompromised state. 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 and susceptible oyster genetic backgrounds. We also identify a core colonizing bacterial consortium which, together with OsHV-1 μ Var, forms the POMS pathobiota. This bacterial core is characterized by highly active global metabolism and key adaptive responses to the within-host environment (e.g. stress responses and redox homeostasis). Several marine gamma proteobacteria in the core express different and complementary functions to exploit the host’s resources. Such cross-benefits are observed in colonization-related functions, and reveal specific strategies used by these bacteria to adapt and colonize oysters (e.g. adhesion, cell defense, cell motility, metal homeostasis, natural competence, quorum sensing, transport, and virulence). Interdependence and cooperation within the microbial community for metabolic requirements is best exemplified by sulfur metabolism, which is a property of the pathobiota as a whole and not of a single genus. We argue that this interdependence may dictate the conservation of the POMS pathobiota across distinct environments and oyster genetic backgrounds.

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Section: Introductionmentioning

confidence: 99%

A core of functional complementary bacteria infects oysters in Pacific Oyster Mortality Syndrome

Lucasson

Luo

Mortaza

et al. 2020

Preprint

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“…We have shown recently that eliciting oyster antiviral defenses through so-called immune priming is sufficient to prevent colonization by OsHV-1 and subsequent disease development [37,68]. Similarly, exposure to microbial communities at early developmental stages (referred to as biological embedding) was also protective against POMS [69]. Such solutions, which make the host a less favorable niche for the OsHV-1 virus [68] and/or bacteria [69], are promising avenues for preventing or reducing the assembly of microbial consortia that produce POMS.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, exposure to microbial communities at early developmental stages (referred to as biological embedding) was also protective against POMS [69]. Such solutions, which make the host a less favorable niche for the OsHV-1 virus [68] and/or bacteria [69], are promising avenues for preventing or reducing the assembly of microbial consortia that produce POMS.…”

Section: Discussionmentioning

confidence: 99%

Cooperation and cheating orchestrateVibrioassemblages and polymicrobial synergy in oysters infected with OsHV-1 virus

Oyanedel

Lagorce

Bruto

et al. 2023

Preprint

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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.

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“…25 These changes in the haemolymph microbiota contributes to increased mortality in these two bivalves in response to infections. Other studies performed in the clams Chamelea gallina 26,[38][39][40][41][42][43][44][45][46][47][48][49][50] and Tegillarca granosa 27 have shown that chemical pollution leads to microbiota shift associated with the proliferation of opportunistic pathogens potentially contributing to the declining health of clams.…”

Section: Introductionmentioning

confidence: 99%

“…[39][40][41] Otherwise, in a broader context, several studies have evidenced the critical role of microbiota during the early developmental steps to educate and durably imprint the host innate immune system in mammals 37,42,43 , in fish 44 in crustaceans 45,46 and in molluscs. 47,48 Despite these evidence, antagonistic approaches toward microbial communities, such as water sterilisation and antibiotic treatment, have been favoured so far. 49,50 In this review, we promote the potential application of natural microorganisms as a treatment during the early developmental stage (larval rearing) to shape and sustain lifelong innate immune competence in aquaculture.…”

Section: Introductionmentioning

confidence: 99%

Microbial education for marine invertebrate disease prevention in aquaculture

Dantan,

Toulza,

Petton

et al. 2024

Reviews in Aquaculture

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The holobiont theory expands the notion of individual multicellular organisms as a community composed of a host and all its associated microorganisms. This concept has been extensively studied in the field of aquaculture, where increasing evidence has highlighted the importance of the host associated microorganisms in species fitness. Here, we focus our review on mollusc and crustacean species in which microbiota dysbiosis has recently been described in the context of various diseases, resulting in significant economic losses. Influencing the holobiont structure through the use of probiotics is a potential strategy that could improve the fitness or the robustness of cultivated species. We discuss here the possibility of developing microbiome targeted prophylactic approaches by promoting (1) methods to identify host microbial community that fosters good health status and (2) early life microbial education to favour long‐term resistance to stress or disease. This review aims to inform the aquaculture industry about potential strategies in rearing practices to mitigate diseases and economic losses.

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Early life microbial exposures shape the Crassostrea gigas immune system for lifelong and intergenerational disease protection

Cited by 4 publications

References 43 publications

A core of functional complementary bacteria infects oysters in Pacific Oyster Mortality Syndrome

A core of functional complementary bacteria infects oysters in Pacific Oyster Mortality Syndrome

Cooperation and cheating orchestrateVibrioassemblages and polymicrobial synergy in oysters infected with OsHV-1 virus

Microbial education for marine invertebrate disease prevention in aquaculture

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