The Antimicrobial Defense of the Pacific Oyster, Crassostrea gigas. How Diversity may Compensate for Scarcity in the Regulation of Resident/Pathogenic Microflora

Abstract

Healthy oysters are inhabited by abundant microbial communities that vary with environmental conditions and coexist with immunocompetent cells in the circulatory system. In Crassostrea gigas oysters, the antimicrobial response, which is believed to control pathogens and commensals, relies on potent oxygen-dependent reactions and on antimicrobial peptides/proteins (AMPs) produced at low concentrations by epithelial cells and/or circulating hemocytes. In non-diseased oysters, hemocytes express basal levels of defensins (Cg-Defs) and proline-rich peptides (Cg-Prps). When the bacterial load dramatically increases in oyster tissues, both AMP families are driven to sites of infection by major hemocyte movements, together with bactericidal permeability/increasing proteins (Cg-BPIs) and given forms of big defensins (Cg-BigDef), whose expression in hemocytes is induced by infection. Co-localization of AMPs at sites of infection could be determinant in limiting invasion as synergies take place between peptide families, a phenomenon which is potentiated by the considerable diversity of AMP sequences. Besides, diversity occurs at the level of oyster AMP mechanisms of action, which range from membrane lysis for Cg-BPI to inhibition of metabolic pathways for Cg-Defs. The combination of such different mechanisms of action may account for the synergistic activities observed and compensate for the low peptide concentrations in C. gigas cells and tissues. To overcome the oyster antimicrobial response, oyster pathogens have developed subtle mechanisms of resistance and evasion. Thus, some Vibrio strains pathogenic for oysters are equipped with AMP-sensing systems that trigger resistance. More generally, the known oyster pathogenic vibrios have evolved strategies to evade intracellular killing through phagocytosis and the associated oxidative burst.

Antimicrobial Histones and DNA Traps in Invertebrate Immunity

“…This may be due to the intrinsic resistance of V. tasmaniensis LGP32 to antimicrobials (28) or to the low range of concentrations tested (0 -0.7 M). Because tissues of C. gigas oysters are poor in antimicrobial peptides/proteins (29), the isolation of histones as the only antimicrobials found in gills of challenged oysters strongly argues in favor of their role in the oyster antimicrobial defense.…”

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection

“…This also applies to the hemolymph (Olafsen et al, 1993;Garnier et al, 2007, Wendling et al, 2014-the functional analog of blood in vertebrates (Bachere et al, 2004). The presence of viable bacteria in the hemolymph of healthy oysters can influence the outcome of pathogen infections either by stimulating immunity or by competitive exclusion (Schmitt et al, 2012); isolation of antimicrobial compounds of bacterial origin from oyster hemolymph has provided support for the latter hypothesis (Defer et al, 2013). Yet oyster hemolymph microbiota have rarely been studied and so far only by means of culture-dependent methods (Olafsen et al, 1993;Garnier et al, 2007;Wendling et al, 2014).…”

The Galectin CvGal1 from the Eastern Oyster (Crassostrea virginica) Binds to Blood Group A Oligosaccharides on the Hemocyte Surface*

“…Therefore, the hemocytes provide not only the means of parasite uptake and entry but also an environment favorable for parasite proliferation and dissemination, leading to systemic infection and death of the oyster (14). The cell entry mechanisms of P. marinus have not been fully elucidated, but in a previous study, we identified a galectin (CvGal1) 3 of unique structure that plays a significant role in entering the host hemocytes (15).…”

“…Among the multiple factors involved in recognition of the potential infectious challenges, a diversified repertoire of soluble and cell-associated lectins mediate binding interactions with potential pathogens that usually result in their agglutination, immobilization, and phagocytosis or encapsulation by hemolymph cells (hemocytes) (2). The engulfed microbe is killed by oxidative stress resulting from the respiratory burst by the hemocytes upon particle uptake and is degraded in the phagosomal compartment (3).…”