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Review
. 2019 Mar:92:260-282.
doi: 10.1016/j.dci.2018.11.020. Epub 2018 Nov 29.

From the raw bar to the bench: Bivalves as models for human health

José A Fernández Robledo  1 , Raghavendra Yadavalli  2 , Bassem Allam  3 , Emmanuelle Pales Espinosa  3 , Marco Gerdol  4 , Samuele Greco  4 , Rebecca J Stevick  5 , Marta Gómez-Chiarri  6 , Ying Zhang  7 , Cynthia A Heil  2 , Adrienne N Tracy  8 , David Bishop-Bailey  9 , Michael J Metzger  10
Affiliations
Review

From the raw bar to the bench: Bivalves as models for human health

José A Fernández Robledo et al. Dev Comp Immunol. 2019 Mar.

Abstract

Bivalves, from raw oysters to steamed clams, are popular choices among seafood lovers and once limited to the coastal areas. The rapid growth of the aquaculture industry and improvement in the preservation and transport of seafood have enabled them to be readily available anywhere in the world. Over the years, oysters, mussels, scallops, and clams have been the focus of research for improving the production, managing resources, and investigating basic biological and ecological questions. During this decade, an impressive amount of information using high-throughput genomic, transcriptomic and proteomic technologies has been produced in various classes of the Mollusca group, and it is anticipated that basic and applied research will significantly benefit from this resource. One aspect that is also taking momentum is the use of bivalves as a model system for human health. In this review, we highlight some of the aspects of the biology of bivalves that have direct implications in human health including the shell formation, stem cells and cell differentiation, the ability to fight opportunistic and specific pathogens in the absence of adaptive immunity, as source of alternative drugs, mucosal immunity and, microbiome turnover, toxicology, and cancer research. There is still a long way to go; however, the next time you order a dozen oysters at your favorite raw bar, think about a tasty model organism that will not only please your palate but also help unlock multiple aspects of molluscan biology and improve human health.

Keywords: Disseminated neoplasia; HAB; Microbiome; Microplastics; Mucosal immunity; Myticalins.

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Conflict of interest statement

Declarations of interest: none.

Figures

Fig. 1.
Fig. 1.. Bivalves as models for human health.
Hemocytes are involved in multiple aspects from the biology of bivalves with a direct implication on human health. Keystone of the immune defense at the center against a broad variety of pathogens, we can learn how organism lacking adaptive immunity (as defined in vertebrates) deal with viruses, bacteria, and protozoan. Mucosal immunity, maintaining and turnover of the microbiome in an aquatic environment rich in bacteria and as source of antimicrobial peptides in a world where antibiotic resistance is on the rise, are only a few of the aspects where hemocytes and humoral factors are involved. Bivalves can to cope with detoxification during HABs and as a filter feeder can concentration of human viruses responsible for outbreaks and microplastics that are incorporated into the food chain. Shell formation is also an exciting biology aspect that has parallel mechanisms with bone formation. Contagious cancer is clams can bring some light into oncogenic mechanisms, including cancer evolution, metastasis, and the role of transposable elements in oncogenesis. Some drawings modified from IAN (http://ian.umces.edu/).
Fig. 2.
Fig. 2.. Mucosal immunity model.
Mucus covering pallial surfaces of bivalve plays an important role in immunity and homeostasis. Viruses, bacteria, and protozoans, but also particulate matter and microalgae present in seawater directly interact with innate immune effectors present in mucus. Mucosal hemocytes likely play a sentinel role (sensing and signaling) similar to that of dendritic cells in higher vertebrates. Based on (Allam and Pales Espinosa, 2015). Antimicrobial peptide (AMP); Crassostrea virginica Galectin 1 (CvGal1); vacuole (V).
Fig. 3.
Fig. 3.. Summary of the known antimicrobial peptides produced by mussels (Mytilus spp.).
Antimicrobial activity (defined as an experimentally determined Minimum Inhibitory Concentration <32 μM), tissue specificity and three-dimensional structure (whenever known) are indicated for each AMP family. The typical cysteine array and disulfide connectivity of cysteine-rich AMPs are also displayed. Different members of the mytimacin and mytimycin family are characterized by different cysteine arrays. The disulfide connectivity of mytimycin and myticusins has not been elucidated yet. MP: mature peptide; C-term: anionic C-terminal extension; Glyco 18: glycoside hydrolase, family 18, domain; L: linker region; C: chitinase-like domain of mytichitin.
Fig. 4.
Fig. 4.. Transfer routes and effects of toxins in bivalves.
HAB species containing biotoxins are ingested through the filter-feeding process. Some species are rejected in the pseudofeces. However, the ingestion of the HAB species may result in the concentration and modification of the toxins, resulting in genetic, pathological, physiological, and behavioral effects. Accumulated toxins are vectored to humans and/or bioaccumulated through the food chain. Interestingly, the bivalves also can eliminate (depurate) the toxins. Some drawings modified from IAN (http://ian.umces.edu/).
Fig. 5.
Fig. 5.. Overview of available resources towards a genetically tractable system in bivalves.
Most attempts to introducing genetic material in oysters date from two decades ago and focused on the Pacific oyster. With the genomes of commercial and non-commercial bivalves being sequenced, the minimum tools and resources for building a genetically tractable system are already available. Indeed, CRISPR/Cas9 has been recently achieved in the gastropod Crepidula fornicata (common slipper shell).
Fig. 6.
Fig. 6.. Genetic material delivery approaches in bivalves.
In the absence of cell lines of marine invertebrates, embryos are the only stage with proliferating cells necessary for testing knocking in genes using CRISPR/Cas9 approaches. Available all year round, hemocytes and mantle explants are useful to test plasmid constructs carrying fluorescence tags. For delivering the genetic material, microinjection, electroporation, and lipofection are techniques that have been successfully used in the past. Confocal microscopy, flow cytometry, enzymatic activity, and PCR/sequencing can be used to characterize the transfectants.
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