Infectious diseases of marine molluscs and host responses as revealed by genomic tools

Abstract

More and more infectious diseases affect marine molluscs. Some diseases have impacted commercial species including MSX and Dermo of the eastern oyster, QPX of hard clams, withering syndrome of abalone and ostreid herpesvirus 1 (OsHV-1) infections of many molluscs. Although the exact transmission mechanisms are not well understood, human activities and associated environmental changes often correlate with increased disease prevalence. For instance, hatcheries and large-scale aquaculture create high host densities, which, along with increasing ocean temperature, might have contributed to OsHV-1 epizootics in scallops and oysters. A key to understanding linkages between the environment and disease is to understand how the environment affects the host immune system. Although we might be tempted to downplay the role of immunity in invertebrates, recent advances in genomics have provided insights into host and parasite genomes and revealed surprisingly sophisticated innate immune systems in molluscs. All major innate immune pathways are found in molluscs with many immune receptors, regulators and effectors expanded. The expanded gene families provide great diversity and complexity in innate immune response, which may be key to mollusc's defence against diverse pathogens in the absence of adaptive immunity. Further advances in host and parasite genomics should improve our understanding of genetic variation in parasite virulence and host disease resistance.

Keywords: aquaculture; genomics; immune response; marine diseases; mollusc; parasites.

Figure 1.

Large-scale aquaculture production precedes outbreaks of OsHV-1 in Chinese scallop C. farreri in China (a) and in Pacific C. gigas cultured in France (b). Arrows point to first reports of OsHV-1 caused mortalities. Production statistics for Chinese scallop are estimated based on total scallop production data from Ministry of Agriculture of China and personal knowledge of regional production of Chinese scallop. Production of C. gigas in France is extracted from United Nations Food and Agriculture Organization's database.

Figure 2.

Hypothetical immune pathways in molluscs based on genes identified and their functions in model organisms. Genes shared in blue are receptors, genes in red are immune effectors, genes in green are transcriptional factors and genes in grey are suspected but have not been identified or confirmed in molluscs. IFN, interferon; IFNR, IFN receptor; IL-17, interleukin 17; IL-17R, IL-17 receptor; TNF, tissue necrosis factor; TNFR, TNF receptor; TLR, Toll-like receptor; MyD88, myeloid differentiation primary response gene 88; TRIF, TIR-domain-containing adapter-inducing interferon-β; ADAR, double-stranded RNA-specific adenosine deaminase; RIG-1, retinoic acid-inducible gene 1; MDA5, melanoma differentiation-associated protein 5; DCL, Dicer-like; AGO2, argonaute 2; Ribon, ribonucleases; PGRP, peptidoglycan recognition protein; GNBP, Gram-negative binding protein; FREP, fibrinogen-related protein; GPCR, G-protein-coupled receptor; SR, scavenger receptor; JAK, Janus kinase; STAT, signal transducer and activator of transcription; SOCS2, suppressor of cytokine signalling 2; IRF, interferon regulatory factor; BCL2, B-cell lymphoma 2; BAX, Bcl-2-associated X; C, cytochrome c; Casp, caspase; IAPs, inhibitors of apoptosis; FADD, Fas-associated protein with death domain; TRAF, TNF receptor-associated factors; JNK, c-Jun N-terminal kinases; NFκB, nuclear factor kappa B; IκB kinase (IKK); IKK, IκB kinase; TBK1, TANK-binding kinase 1; TAK1, transforming growth factor-beta-activated kinase 1; AP-1, activator protein 1; HSPs, heat shock proteins; CYP450, cytochrome P450; C1q, globular head C1q domain containing protein; IF44 L, interferon-induced protein 44-like; MCO, multi-copper oxidase; SO, spermidine oxidase; MP, metalloproteinase; SOD, superoxide dismutase; GPX, glutathione peroxidase; GST, glutathione S-transferase; CAT, catalase; AMP, antimicrobial peptide; TRIM, tripartite motif family; and ISGs, IFN-stimulated genes. (Adapted from [6].)