The new insights into the oyster antimicrobial defense: Cellular, molecular and genetic view

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Abstract

Oysters are sessile filter feeders that live in close association with abundant and diverse communities of microorganisms that form the oyster microbiota. In such an association, cellular and molecular mechanisms have evolved to maintain oyster homeostasis upon stressful conditions including infection and changing environments. We give here cellular and molecular insights into the Crassostrea gigas antimicrobial defense system with focus on antimicrobial peptides and proteins (AMPs). This review highlights the central role of the hemocytes in the modulation and control of oyster antimicrobial response. As vehicles for AMPs and other antimicrobial effectors, including reactive oxygen species (ROS), and together with epithelia, hemocytes provide the oyster with local defense reactions instead of systemic humoral ones. These reactions are largely based on phagocytosis but also, as recently described, on the extracellular release of antimicrobial histones (ETosis) which is triggered by ROS. Thus, ROS can signal danger and activate cellular responses in the oyster. From the current literature, AMP production/release could serve similar functions. We provide also new lights on the oyster genetic background that underlies a great diversity of AMP sequences but also an extraordinary individual polymorphism of AMP gene expression. We discuss here how this polymorphism could generate new immune functions, new pathogen resistances or support individual adaptation to environmental stresses.

Introduction

Oysters are bivalve mollusks belonging to the Ostreidae family (Mollusca, Bivalvia, Lophotrochozoa). They are sessile filter-feeders living in shallow water from intertidal zones of bays, lagoons and estuaries. In these habitats, oysters are confronted and adapted to great changes in biotic and abiotic environmental conditions. Abiotic factors include temperatures and salinity fluctuations but also exposure to xenobiotics and water acidification due to human activities. Biotic factors include abundant and diverse populations of microbes. As filter feeders, oysters are in permanent contact and exchanges with microorganisms. Thus, they harbor on their surfaces and inside their body cavities and hemolymph a dense microbiota which has been shown to be greatly dominated by Vibrio species [1], [2]. Indeed, a large attention has been paid over the past years, to populations of vibrios as they are among the most abundant cultivable bacteria isolated from oyster tissues [3]. In healthy oyster, bacteria load, including vibrio, has been shown to vary over time according to individuals and to temperature, with hemolymph average concentrations of 5,7 colonies forming unit (CFU) per μL [2], [4]. Hence, oyster must be seen as an organism associated to a microbiota (including mutualistics, opportunists and pathogens), that has adapted effective cellular and molecular mechanisms for maintaining homeostasis and health status in stressful and changing environments. The multifactorial diseases affecting Crassostrea gigas oysters worldwide [5] are the outcome of an equilibrium collapse in the interplay between the biotic and abiotic environmental factors such as microorganisms and temperature [6], on the one hand, and the oyster physiology and immune responses on the other hand [7].

By focusing on C. gigas, we propose here to give cellular and molecular insights into the oyster antimicrobial defense system considering the genetic background of individuals.

Section snippets

Effectors of the antimicrobial defense

Oyster immunity involves not only hemolymph-mediated reactions, but also immune effectors produced by epithelial cells from various organs, including gills, mantle, digestive gland and intestine, which participate in the antimicrobial defense mechanisms.

The antimicrobial response to infection

The oyster antimicrobial response to infection needs to be reconsidered with the recent evidence that these bivalves naturally host diverse and abundant microbial communities [1] that may contribute to homeostasis, host protection and fitness in rapidly changing environments [75]. In a view similar to that of the interaction between the mammalian gut immune system and the abundant and diverse intestinal microbiota, the existence in oysters of an abundant microbiota associated to its epithelial

Unexplored functions of oyster AMPs

Until now, the main host defense function recognized for AMPs has been the direct killing of microorganisms. However, over the past years, an abundant literature has shown that AMPs from vertebrates support a broad series of immune functions. Indeed, there is new evidence that they also display immunomodulatory functions involving chemotactic activities, induction and/or inhibition of cytokine production, wound healing and modulation of immune cells responses (reviewed in Ref. [103]). Still,

Genomic structural organization

Whereas C. gigas genome has been recently sequenced [78], our knowledge about oyster AMP gene organization in oyster genome remains quite limited. Numerous DNA and RNA sequences have been characterized among the different AMP families (Table 3), revealing a great intra- and inter-individual diversity. Cg-Def family appears to be the most diversified with 89 different mRNA sequences and 25 gDNA ones, available on GenBank (Table 3). However, it is noteworthy that we failed to evidence in the

Conclusions

From the recent results and knowledge we reviewed here, the role of AMPs in the oyster immune system must be reconsidered taking into account that oysters must be seen as an organism associated to a microbiota. In such a context where the oyster can host an abundant and beneficial microbiota, AMPs cannot be considered only as repressive weapons. It is likely that in oyster, where AMPs are present at low concentrations [46], they are primarily involved in unexplored immune functions.

We have now

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    These authors contributed equally.

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