Establishment of an experimental infection protocol for the flat oyster, Ostrea edulis, with the intrahaemocytic protozoan parasite, Bonamia ostreae: application in the selection of parasite-resistant oysters

doi:10.1016/0044-8486(94)00342-L

Aquaculture

Volume 132, Issues 3–4, 1 May 1995, Pages 183-194

https://doi.org/10.1016/0044-8486(94)00342-L Get rights and content

Abstract

The availability of purified Bonamia ostreae suspensions and the development of an inoculation protocol enabled experimental infections with the European flat oyster, Ostrea edulis, to be carried out. Different infectious doses were tested and the kinetics of bonamiasis studied. The 50% infectious dose (ID), determined from inoculations with 10 to 10⁶ B. ostreae per individual, was estimated to be 80 000 parasites for 3-year-old oysters. This 50% ID was used to screen for parasite-resistant oysters. Preliminary results suggested that the F₁ progeny of oysters that survived previous outbreaks of bonamiasis were more resitant to B. ostreae.

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Cited by (53)

What do the terms resistance, tolerance, and resilience mean in the case of Ostrea edulis infected by the haplosporidian parasite Bonamia ostreae
2021, Journal of Invertebrate Pathology
Citation Excerpt :
In addition, a natural system is likely to experience the dilution of resistance genes as unexposed (susceptible) stock can often contribute to progeny of exposed areas, for example through the movement of gametes or larvae through the water column (Culloty et al., 2001; Flannery et al., 2014), and by the sale and consumption of resistant oysters before they contribute genes to future generations (Lauckner, 1983). Therefore, when analysing either the genetic architecture of disease resistance, or the biology of disease progression, it is often preferable to work with populations of oyster that have a highly structured population, have not been exposed to the parasite and can be challenged in a controlled manner (e.g. Hervio et al., 1995). In doing so, variables associated with previous exposure (such as immune priming and selective sweeps) are accounted for (Vera et al., 2019).
The decline of the European flat oyster Ostrea edulis represents a loss to European coastal economies both in terms of food security and by affecting the Good Environmental Status of the marine environment as set out by the European Council’s Marine Strategy Framework Directive (2008/56/EC). Restoration of O. edulis habitat is being widely discussed across Europe, addressing key challenges such as the devastating impact of the haplosporidian parasite Bonamia ostreae. The use of resistant, tolerant, or resilient oysters as restoration broodstock has been proposed by restoration practitioners, but the definitions and implications of these superficially familiar terms have yet to be defined and agreed by all stakeholders. This opinion piece considers the challenges of differentiating Bonamia resistance, tolerance, and resilience; challenges which impede the adoption of robust definitions. We argue that, disease-resistance is reduced susceptibility to infection by the parasite, or active suppression of the parasites ability to multiply and proliferate. Disease-tolerance is the retention of fitness and an ability to neutralise the virulence of the parasite. Disease-resilience is the ability to recover from illness and, at population level, tolerance could be interpreted as resilience. We concede that further work is required to resolve practical uncertainty in applying these definitions, and argue for a collaboration of experts to achieve consensus. Failure to act now might result in the future dispersal of this disease into new locations and populations, because robust definitions are important components of regulatory mechanisms that underpin marine management.
Ephemeral detection of Bonamia exitiosa (Haplosporida) in adult and larval European flat oysters Ostrea edulis in the Solent, United Kingdom
2020, Journal of Invertebrate Pathology
The haplosporidian parasite Bonamia exitiosa was detected using PCR in four adult and six larval brood samples of the European flat oyster Ostrea edulis from the Solent, UK. This represents the second reported detection of this parasite along the south coast of England. Adult oysters were collected and preserved from seabed populations or restoration broodstock cages between 2015 and 2018. The larvae within brooding adults sampled during 2017 and 2018 were also preserved. Molecular analysis of all samples was performed in 2019. The DNA of B. exitiosa was confirmed to be present within the gill tissue of one oyster within the Portsmouth wild fishery seabed population (n = 48), sampled in November 2015; the congeneric parasite Bonamia ostreae was not detected in this individual. This is the earliest record of B. exitiosa in the Solent. Concurrent presence of both B. ostreae and B. exitiosa, determined by DNA presence, was confirmed in the gill and heart tissue of three mature individuals from broodstock cages sampled in October 2017 (n = 99), two from a location on the River Hamble and one from the Camber Dock in Portsmouth Harbour. B. exitiosa was not detected in the November 2018 broodstock populations. A total of six larval broods were positive for B. exitiosa, with five also positive for B. ostreae. None of the brooding adults were positive for B. exitiosa suggesting that horizontal transmission from the surrounding environment to the brooding larvae is occurring. Further sampling of broodstock populations conducted by the Fish Health Inspectorate at the Centre for Environment, Fisheries and Aquaculture Science in June 2019 did not detect infection of O. edulis by B. exitiosa. These findings together suggest that the pathogen has not currently established in the area.
Is pallial mucus involved in Ostrea edulis defenses against the parasite Bonamia ostreae?
2020, Journal of Invertebrate Pathology
Bonamia ostreae is an intrahemocytic parasite that has been responsible for severe mortalities in the flat oyster Ostrea edulis since the 1970́s. The Pacific oyster Crassostrea gigas is considered to be resistant to the disease and appears to have mechanisms to avoid infection. Most studies carried out on the invertebrate immune system focus on the role of hemolymph, although mucus, which covers the body surface of molluscs, could also act as a barrier against pathogens. In this study, the in vitro effect of mucus from the oyster species Ostrea edulis and C. gigas on B. ostreae was investigated using flow cytometry. Results showed an increase in esterase activities and mortality rate of parasites exposed to mucus from both oyster species. In order to better understand the potential role of mucus in the defense of the oyster against parasites such as B. ostreae, liquid chromatography and tandem mass spectrometry were used to describe and compare mucus protein composition from both species. In all oyster species, pallial mucus contains a high level of proteins; however, O. edulis mucus produced a variety of proteins that could be involved in the immune response against the parasite, including Cu/Zn extracellular superoxide dismutase, thioxiredoxin, peroxiredon VI, heat shock protein 90 as well as several hydrolases. Conversely, a different set of antioxidant proteins, hydrolases and stress related proteins were identified in mucus from C. gigas. Our results suggest an innate immunity adaptation of oysters to develop a specific response against their respective pathogens. The mucosal protein composition also provides new insights for further investigations into the immune response in oysters.
Involvement of apoptosis in the dialogue between the parasite Bonamia ostreae and the flat oyster Ostrea edulis
2019, Fish and Shellfish Immunology
The protozoan parasite Bonamia ostreae has been associated with the decline of flat oyster Ostrea edulis populations in some European countries. Control of shellfish diseases mostly relies on prevention measures including transfer restrictions and stock management measures such as breeding programmes. These prevention and mitigation measures require a better understanding of interactions between host and pathogens. Previous in vitro studies allowed identifying apoptosis as a mechanism activated by the flat oyster in response to B. ostreae. However, these experiments also suggested that the parasite is able to regulate apoptosis in order to survive and multiply within hemocytes. By simplifying the conditions of infection, in vitro studies allow identifying most distinct features of the response of the host. In order to appreciate the relative importance of apoptosis in this response at the oyster scale, in vivo trials were carried out by injecting with parasites oysters from two French locations, Quiberon Bay (Brittany) and Diana Lagoon (Corsica). Apoptosis was investigated on pools of hemolymph from oysters collected at early and later times after injection using previously developed tools. Apoptotic cellular activities including intracytoplasmic calcium concentration, mitochondrial membrane potential and phosphatidyl serine externalization were analysed using flow cytometry. Moreover, the expression of flat oyster genes involved in both extrinsic and intrinsic pathways was measured using real time quantitative PCR.
New perspective on the haplosporidian parasites of molluscs
2015, Journal of Invertebrate Pathology
The protist phylum Haplosporidia comprises over 40 described species with representatives infecting a range of mollusc hosts, including several ecologically and economically significant pathogens. Continuing exploration of haplosporidian diversity has added ten new species in recent years and brought the phylogenetics of the group into somewhat clearer focus, with monophyletic Bonamia and Minchinia lineages continuing to be supported. However, the addition of new sequences to phylogenetic analyses has left the paraphyletic genus Haplosporidium’s picture less resolved. It is not clear that even two genera will be enough to accommodate the species presently drawn to the Haplosporidium regions of the haplosporidian tree. In this review, we summarize recent findings in haplosporidian diversity and phylogenetics, and provide a synthesis of our understanding of the life cycles and environmental influences on haplosporidians, with particular emphasis on the important pathogens Haplosporidium nelsoni and Bonamia ostreae. Additionally, we consider the evolution of the “microcell haplosporidian” lifestyle of Bonamia parasites, and suggest that colonization of high-density oyster host populations in relatively stable euhaline marine environments may have been an important development favoring the evolution of the microcell haplosporidian life strategy.
Parasite transmission through suspension feeding
2015, Journal of Invertebrate Pathology
Suspension-feeding bivalve molluscs are confronted with a wide range of materials in the benthic marine environment. These materials include various sized plankton and the organic material derived from it, macroalgae, detritus and a diversity of microbial parasites that have adapted life stages to survive in the water column. For bivalve parasites to infect hosts though, they must first survive and remain infectious in the water column to make initial contact with hosts, and once in contact, enter and overcome elaborate pathways for particle sorting and selection. Even past these defenses, bivalve parasites are challenged with efficient systems of mechanical and chemical digestion and highly evolved systems of innate immunity. Here we review how bivalve parasites evade these hurdles to complete their life cycles and establish within bivalve hosts. We broadly cover significant viral, bacterial, and protozoan parasites of marine bivalve molluscs, and illustrate the emergent properties of these host-parasite systems where parasite transmission occurs through suspension feeding.

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Aquaculture

Abstract

References (14)

Mussel (Mytilus edulis) treatment against the red copepod Mytilicola intestinalis

Aquaculture

Interactions between Bonamia ostreae (Protozoa: Ascetospora) and haemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): entry mechanisms

J. Invert. Pathol.

Resistance of Ostrea edulis to Bonamia ostreae infection

Aquaculture

Isolation and purification of the Protozoan Bonamia ostreae (Pichot et al. 1980), a parasite affecting the flat oyster Ostrea edulis L.

Aquaculture

Interactions between Bonamia ostreae (Protozoa: Ascetospora) and haemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): in vitro system establishment

J. Invert. Pathol.

Luminol-dependent chemiluminescence by haemocytes of two marine species, Ostrea edulis and Crassostrea gigas

Dis. Aquat. Org.

Bonamiasis: a model study of diseases in marine molluscs

Cited by (53)

What do the terms resistance, tolerance, and resilience mean in the case of Ostrea edulis infected by the haplosporidian parasite Bonamia ostreae

Ephemeral detection of Bonamia exitiosa (Haplosporida) in adult and larval European flat oysters Ostrea edulis in the Solent, United Kingdom

Is pallial mucus involved in Ostrea edulis defenses against the parasite Bonamia ostreae?

Involvement of apoptosis in the dialogue between the parasite Bonamia ostreae and the flat oyster Ostrea edulis

New perspective on the haplosporidian parasites of molluscs

Parasite transmission through suspension feeding