Integrative Study of Physiological Changes Associated with Bacterial Infection in Pacific Oyster Larvae

PLoS ONE, Volume 8, Issue 5, 21 May 2013, Article numbere64534

Genard, B , Miner, P, Nicolas, J.-L., Moraga, D., Boudry, P., Pernet, F., Tremblay, R.

Institut des sciences de la mer, Université du Québec à Rimouski, Rimouski, QC, Canada

 

Abstract

Bacterial infections are common in bivalve larvae and can lead to significant mortality, notably in hatcheries. Numerous studies have identified the pathogenic bacteria involved in such mortalities, but physiological changes associated with pathogen exposure at larval stage are still poorly understood. In the present study, we used an integrative approach including physiological, enzymatic, biochemical, and molecular analyses to investigate changes in energy metabolism, lipid remodelling, cellular stress, and immune status of Crassostrea gigas larvae subjected to experimental infection with the pathogenic bacteria Vibrio coralliilyticus. Our results showed that V. coralliilyticus exposure induced (1) limited but significant increase of larvae mortality compared with controls, (2) declined feeding activity, which resulted in energy status changes (i.e. reserve consumption, β-oxidation, decline of metabolic rate), (3) fatty acid remodeling of polar lipids (changes in phosphatidylinositol and lysophosphatidylcholine composition,non-methylene–interrupted fatty acids accumulation, lower content of major C20 polyunsaturated fatty acids as well as activation of desaturases, phospholipase and lipoxygenase), (4) activation of antioxidant defenses (catalase, superoxide dismutase, peroxiredoxin) and cytoprotective processes (heat shock protein 70, pernin), and (5) activation of the immune response (non-self recognition, NF-κB signaling pathway, haematopoiesis, eiconosoids and lysophosphatidyl acid synthesis, inhibitor of metalloproteinase and antimicrobial peptides). Overall, our results allowed us to propose an integrative view of changes induced by a bacterial infection in Pacific oyster larvae, opening new perspectives on the response of marine bivalve larvae to infections.

 

Supplement:

The main interest and novelty of our study is that we characterized the response of oyster larvae to pathogen infection using a multidisciplinary approach. For the first time, the impact of a bacterial challenge on larval physiology was characterized in a bivalve mollusk at the physiological, enzymatic, biochemical and transcriptional levels. This study has shown the activation of several physiological processes which co-occurred after bacterial infection in oyster larvae. Indeed, we have observed that V. coralliilyticus exposure coincided with changes in energy status of larvae, fatty acid remodeling and the activation of antioxidant defenses and immune response. Taken together, all of these results can be gathered in a schematic diagram (Figure 1) which illustrates putative relationships between these physiological processes. This overall view open the way to further studies that will improve our knowledge about the impact of bacterial infection on larval physiology for marine invertebrates. Moreover, this study illustrates the interest of an integrative approach to improve the understanding of the innate immunity during ontogeny of marine invertebrate larvae.

Bertrand Genard-png

Figure 1. Schematic diagrams of physiological changes induced during bacterial infection in C. gigas larvae. Infection impact on larval physiology was investigated through immunity (1), cellular stress (2), energetic metabolism (3) and lipid metabolism (4) using physiological, enzymatic, biochemical and molecular analysis. Results suggest that bacterial infection induce the activation of the immune response (non-self recognition (1a), NF-κB signaling pathway (1b), haematopoiesis (1d), synthesis of inhibitor of metalloproteinase, antimicrobial peptide (1c) and phagocytosis (1e) allowing the destruction of pathogenic bacteria. The production of reactive oxygen species (ROS) during the phagocytosis process was managed by antioxidant defenses (2a) and cytoprotective proteins (2b). Infection affects the feeding activity (3a) which change the energy status of larvae (decline of metabolic rate (3b), energy reserve consumption (3c), β-oxidation activation (3d) and lower lipids storage (3e)). Besides metabolic changes, fatty acid remodeling in polar lipids (4a) is associated to pathogen exposure, as suggested by changes in phosphatidylinositol and lysophosphatidylcholine composition, non-methylene–interrupted fatty acids accumulation, lower content of major C20 polyunsaturated fatty acids and activation of desaturases. Finally, infection induces the activation of phospholipase and lipoxygenase (4b) probably through NF-κB regulation (4c) to initiate eicosanoïdes and lysophosphatidic acid (LPA) pathways.

 

Contact:

Bertrand Genard, Ph.D.

Institut des sciences de la mer

Université du Québec à Rimouski

310 allée des Ursulines

Rimouski, Qc, G5L-3A1 (CANADA)

bertrand.genard@uqar.qc.ca

 

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