Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

Abstract

The Pacific oyster Crassostrea gigas lives in microbe-rich marine coastal systems subjected to rapid environmental changes. It harbours a diversified and fluctuating microbiota that cohabits with immune cells expressing a diversified immune gene repertoire. In the early stages of oyster development, just after fertilization, the microbiota plays a key role in educating the immune system. Exposure to a rich microbial environment at the larval stage leads to an increase in immune competence throughout the life of the oyster, conferring a better protection against pathogenic infections at later juvenile/adult stages. This beneficial effect, which is intergenerational, is associated with epigenetic remodelling. At juvenile stages, the educated immune system participates in the control of the homeostasis. In particular, the microbiota is fine-tuned by oyster antimicrobial peptides acting through specific and synergistic effects. However, this balance is fragile, as illustrated by the Pacific Oyster Mortality Syndrome, a disease causing mass mortalities in oysters worldwide. In this disease, the weakening of oyster immune defences by OsHV-1 µVar virus induces a dysbiosis leading to fatal sepsis. This review illustrates the continuous interaction between the highly diversified oyster immune system and its dynamic microbiota throughout its life, and the importance of this cross-talk for oyster health. This article is part of the theme issue 'Sculpting the microbiome: how host factors determine and respond to microbial colonization'.

Keywords: holobiont; homeostasis; immune priming; immunity; microbiome; ontogeny.

Figure 1.

Immune–microbiota interplay at an oyster epithelium: homeostasis versus dysbiosis. The left panel (health) illustrates a homeostatic context. The microbiota is kept away from epithetial cells (brown cells) by a thick mucus layer (green) secreted by mucocytes (blue cells), which covers the oyster body surfaces. Lectins, hydrolases, copper and zinc contribute to limit penetration of microorganisms. It is assumed that amidase peptidoglycan recognition proteins (PGRPs) prevent peptidoglycan from activating immune receptors. Bacteria circulate in the haemolymph (pink) without inducing a measurable immune response. They are kept under control by functional immune cells (purple) and the AMPs, hydrolases, reactive oxygen species (ROS) and nitric oxide synthase (NOS) they produce. Bacteriocins mediate competition. The right panel (disease) shows a context of dysbiosis. Pathogens alter immune cell functions (pink cells), which no longer control the microbiota. AMP expression is altered. Bacteria invade the conjunctive tissues. Tissues lose their integrity and their barrier functions. Figure created using biorender.com.

Figure 2.

Environmental factors acting on the cross-talk between the oyster immune sytem and its microbiota. Healthy microbiota is diverse and plastic (left panel). Its structure is influenced by environmental factors; for instance, some communities can be favoured by given abiotic factors (pH, temperature or salinity). Microbiota plays a key role in the education of the immune system. In parallel, the immune system relying on haemocytes, mucus production and secreted molecular effectors (e.g. AMPs) participates in the control of the homeostasis of the oyster microbiota. In the presence of pathogens, which can alter immune defences, loss of control of oyster microbiota results in dysbiosis and leads to fatal sepsis (right panel).