Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Abstract

Cephalopods have evolved complex sensory systems and an active lifestyle to compete with fish for similar resources in the marine environment. Their highly active lifestyle and their extensive protein metabolism has led to substantial acid-base regulatory abilities enabling these organisms to cope with CO 2 induced acid-base disturbances. In convergence to teleost, cephalopods possess an ontogeny-dependent shift in ion-regulatory epithelia with epidermal ionocytes being the major site of embryonic acid-base regulation and ammonia excretion, while gill epithelia take these functions in adults. Although the basic morphology and excretory function of gill epithelia in cephalopods were outlined almost half a century ago, modern immunohistological and molecular techniques are bringing new insights to the mechanistic basis of acidbase regulation and excretion of nitrogenous waste products (e.g. NH 3 /NH 4 C ) across ion regulatory epithelia of cephalopods. Using cephalopods as an invertebrate model, recent findings reveal partly conserved mechanisms but also novel aspects of acid-base regulation and nitrogen excretion in these exclusively marine animals. Comparative studies using a range of marine invertebrates will create a novel and exciting research direction addressing the evolution of pH regulatory and excretory systems.

Impact of Short- and Long-Term Exposure to Elevated Seawater Pco2on Metabolic Rate and Hypoxia Tolerance inOctopus rubescens

“…Alternatively, the apparent increase in shortterm metabolic rate at 1,500 matm could, at least in part, be the result of increased activity in energy-dependent ion and acidbase regulation pathways. As with many aquatic metazoans, the primary site of ion regulation in cephalopods resides in the gills (Schipp et al 1979;Hu et al 2015b). Previous work has shown that V-type H 1 -ATPase activity and Na 1 /K 1 -ATPase activity increased after a 6-h ∼1,600-matm exposure in gill homogenates of squid Sepioteuthis lessoniana, along with mRNA transcript abundance of these enzymes (Hu et al 2014).…”

Development of Embryonic Market Squid, Doryteuthis opalescens, under Chronic Exposure to Low Environmental pH and [O2]

“…This difference in YV suggests these embryos may be allocating more energy towards maintaining their internal pH balance relative to embryos exposed to low [O 2 ]. Loliginid embryos exposed to acidified conditions have been shown to upregulate ATP-dependent ion pumps on the yolk epithelium to mediate extracellular pH regulation, suggesting a potential mechanism for elevated energy utilization in response to low pH [18, 43]. YV differences were not observed in Experiment 1.…”

Cuttlefish Early Development and Behavior Under Future High CO2 Conditions

“…Calcifying organisms, as well as those with minimal physiological buffering capacities (e.g., calcareous sponges, corals and most echinoderms) (Knoll et al, 2007) are expected to be particularly affected by OA. On the other hand, higher resilience is expected from organisms equipped with a more powerful capability to maintain their homeostasis and to compensate for extra and intracellular pH perturbations, such as teleosts and cephalopods (Hu et al, 2015). Nonetheless, an increasing number of studies have been reporting a myriad of OA-related impacts over these mollusks (Rosa et al, 2013; Pimentel et al, 2015, 2016; Spady et al, 2018).…”

“…All cephalopods’ hatchlings have a close-to-optimal central nervous system and most of them are strikingly similar to adults, both in morphology and basic behaviors, such as signaling and camouflage (Boyle, 1987). Additionally, cephalopods present a high level of plasticity to environmental changes (Fiorito et al, 2015; Doubleday et al, 2016), with very effective regulatory and excretory systems to that allow them to tolerate high CO 2 concentrations over long exposure times (Hu et al, 2015). However, there are differences within the cephalopods’ species, since active pelagic squids show higher sensitivity to elevated p CO 2 when compared with cuttlefish and octopods, which have a nekton-benthic and benthic lifestyles, respectively (Hu et al, 2014).…”