The Role of the Cephalopod Digestive Gland in the Storage and Detoxification of Marine Pollutants

Abstract

The relevance of cephalopods for fisheries and even aquaculture, is raising concerns on the relationship between these molluscs and environmental stressors, from climate change to pollution. However, how these organisms cope with environmental toxicants is far less understood than for other molluscs, especially bivalves, which are frontline models in aquatic toxicology. Although, sharing the same basic body plan, cephalopods hold distinct adaptations, often unique, as they are active predators with high growth and metabolic rates. Most studies on the digestive gland, the analog to the vertebrate liver, focused on metal bioaccumulation and its relation to environmental concentrations, with indication for the involvement of special cellular structures (like spherulae) and proteins. Although the functioning of phase I and II enzymes of detoxification in molluscs is controversial, there is evidence for CYP-mediated bioactivation, albeit with lower activity than vertebrates, but this issue needs yet much research. Through novel molecular tools, toxicology-relevant genes and proteins are being unraveled, from metallothioneins to heat-shock proteins and phase II conjugation enzymes, which highlights the importance of increasing genomic annotation as paramount to understand toxicant-specific pathways. However, little is known on how organic toxicants are stored, metabolized and eliminated, albeit some evidence from biomarker approaches, particularly those related to oxidative stress, suggesting that these molluscs' digestive gland is indeed responsive to chemical aggression. Additionally, cause-effect relationships between pollutants and toxicopathic effects are little understood, thus compromising, if not the deployment of these organisms for biomonitoring, at least understanding how they are affected by anthropogenically-induced global change.

High cadmium and mercury concentrations in the tissues of the orange-back flying squid, Sthenoteuthis pteropus, from the tropical Eastern Atlantic

“…This proliferation is likely a result of global climate change, overfishing of apex predators, or a combination of both (Doubleday et al 2016). They are also known to rapidly accumulate both organic and inorganic contaminants in their tissues (Penicaud et al 2017;Rodrigo and Costa, 2017).…”

Temporal Variability of Polycyclic Aromatic Hydrocarbons in Deep-Sea Cephalopods of the Northern Gulf of Mexico

“…Also, biological parameters such as lipid metabolism may have an essential role in the variability of PAH bioaccumulation among cephalopod species. It seems that in some shallowerliving cephalopod species, the digestive gland has an important role in detoxification of organic pollutants, including PAHs (Rodrigo and Costa, 2017). The physiological and molecular mechanisms involved in detoxification processes for organic pollutants in deep-sea cephalopod species are not known.…”

“…These toxic compounds are highly lipid-soluble and therefore can cross lipid membranes and bioaccumulate in marine organisms. Mollusks, including cephalopods, have a reduced capacity to metabolize PAHs with higher bioaccumulation potential than other aquatic organisms (Lacoue-Labarthe et al, 2016;Rodrigo and Costa, 2017). In addition, cephalopods have high growth rates, short life spans, and high sensitivity to environmental changes (Rodrigo and Costa, 2017).…”

“…Mollusks, including cephalopods, have a reduced capacity to metabolize PAHs with higher bioaccumulation potential than other aquatic organisms (Lacoue-Labarthe et al, 2016;Rodrigo and Costa, 2017). In addition, cephalopods have high growth rates, short life spans, and high sensitivity to environmental changes (Rodrigo and Costa, 2017). Cephalopods have a high capacity to bioaccumulate and concentrate contaminants at higher levels than other aquatic groups, thus are potentially useful bioindicators of aquatic contamination over short periods (Gomes et al, 2013;Semedo et al, 2014).…”

18S rRNA, a potential reference gene in the qRT-PCR measurement of bisphenol A contamination in green mussels (Perna viridis) collected from the Gulf of Thailand

“…In bivalves, the digestive gland plays a central role like that of the liver in vertebrates, in the metabolism and detoxification of xenobiotic agents (Cocci et al, 2017;Rodrigo and Costa, 2017). Cyp4, the target gene in this study, encodes the CYP4 enzyme which is mainly involved in xenobiotic metabolisms (Hardwick, 2008;Lewis and Ito, 2008).…”