An updated molecular basis for mussel immunity

Abstract

Non-self recognition with the consequent tolerance or immune reaction is a crucial process to succeed as living organisms. At the same time the interactions between host species and their microbiome, including potential pathogens and parasites, significantly contribute to animal life diversity. Marine filter-feeding bivalves, mussels in particular, can survive also in heavily anthropized coastal waters despite being constantly surrounded by microorganisms. Based on the first outline of the Mytilus galloprovincialis immunome dated 2011, the continuously growing transcript data and the recent release of a draft mussel genome, we explored the available sequence data and scientific literature to reinforce our knowledge on the main gene-encoded elements of the mussel immune responses, from the pathogen recognition to its clearance. We carefully investigated molecules specialized in the sensing and targeting of potential aggressors, expected to show greater molecular diversification, and outlined, whenever relevant, the interconnected cascades of the intracellular signal transduction. Aiming to explore the diversity of extracellular, membrane-bound and intracellular pattern recognition receptors in mussel, we updated a highly complex immune system, comprising molecules which are described here in detail for the first time (e.g. NOD-like receptors) or which had only been partially characterized in bivalves (e.g. RIG-like receptors). Overall, our comparative sequence analysis supported the identification of over 70 novel full-length immunity-related transcripts in M. galloprovincialis. Nevertheless, the multiplicity of gene functions relevant to immunity, the involvement of part of them in other vital processes, and also the lack of a refined mussel genome make this work still not-exhaustive and support the development of more specific studies.

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

“…TLRs and TLR pathways are activated by infections in molluscs [129,130]. In the Pacific oyster, four TLR-like and four MyD88-like genes along with several genes for downstream factors are highly upregulated by OsHV-1 infections [128].…”

“…C-type (calcium-dependent) lectin is the most common lectin found in molluscs. The C. gigas genome encodes 266 and the M. galloprovincialis transcriptome contains 154 C-type lectin genes, compared to 34 found in Drosophila melanogaster and 81 in Homo sapiens [115,129]. Molluscan C-type lectins agglutinate bacterial cells and are upregulated by bacterial challenges in several molluscs including C. farreri and C. virginica [130,138].…”

“…The classical pathway requires the activation of C1q by antigen : antibody complexes. Although molluscs do not produce antibodies, many C1q domain containing proteins (C1qDCs) have been found: 321 in C. gigas genome, 1274 in M. galloprovincialis genome and 187 in C. virginica transcriptome, compared with four in sea urchin and 31 in human [115,121,129]. The globular C1q domain recognizes a broad range of ligands, and its expansion in bivalve molluscs may provide great binding specificity to diverse pathogens.…”

Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus , involvement in symbiosis?

“…mussels, scallops, oysters, razor clams) and proved to play a key role in the defence against pathogenic bacteria (Itoh and Takahashi, 2008;Martins et al, 2014;Ni et al, 2007;Wei et al, 2012). Grippingly, only three paralogs of PGRPs were reported in mytilids (Mytilus galloprovinciallis), among which two are predicted to be bound to the membrane and one to be secreted (Gerdol and Venier, 2015) while in a cold seep symbiotic mussel eleven transcripts matching PGRP sequence were identified. These last can be clustered in three groups according to their sequence which suggest the presence in this specie of three paralogs of PGRPs with at least one predicted to have a signal peptide (Wong et al, 2015).…”

“…The high expression of the secreted paralogs Ba-PGRP 3 and 5 in natural population followed by their down-regulation in individuals that lost part of their symbionts raised our awareness and led to two main hypotheses. Due to the key role of PGRPs in the immune response of bivalves and invertebrates in general (Gerdol and Venier, 2015), we can suggest (i) that these two secreted paralogs are highly expressed in gills to defend the organism against pathogenic bacteria. As gills are one of the first barriers between the host and environment, the host to prevent an infection could produce Ba-PGRP 3 and 5.…”