Into the deep: Exploring the molecular mechanisms of hyperactive behaviour induced by three rare earth elements in early life-stages of the deep-sea scavenging amphipod Tmetonyx cicada (Lysianassidae)

With increasing socio-economic importance of the rare earth elements and yttrium (REY), Norway has laid out plans for REY mining, from land-based to deep-sea mining, thereby enhancing REY mobility in the marine ecosystem. Little is known about associated environmental consequences, especially in the deep ocean. We explored the toxicity and modes of action of a light (Nd), medium (Gd) and heavy (Yb) REY-Cl₃ at four concentrations (3, 30, 300, and 3000 μg L^-1) in the Arcto-boreal deep-sea amphipod Tmetonyx cicada. At the highest concentration, REY solubility was limited and increased with atomic weight (Nd < Gd < Yb). Lethal effects were practically restricted to this treatment, with the lighter elements being more acutely toxic than Yb (from ∼50 % mortality in the Gd-group at dissolved 689-504 μg L^-1 to <20 % in the Yb-group at ca. 2000 μg L^-1), which could be a function of bioavailability. All three REY induced hyperactivity at the low-medium concentrations. Delving into the transcriptome of T. cicada allowed us to determine a whole array of potential (neurotoxic) mechanisms underlying this behaviour. Gd induced the vastest response, affecting serotonin-synthesis; sphingolipid-synthesis; the renin-angiotensin system; mitochondrial and endoplasmic reticulum functioning (Gd, Nd); and lysosome integrity (Gd, Yb); as well as the expression of hemocyanin, potentially governing REY-uptake (Gd, Yb). While Nd and Yb shared only few pathways, suggesting a link between mode of action and atomic weight/radius, almost all discussed mechanisms imply the disruption of organismal Ca-homeostasis. Despite only fragmental genomic information available for crustaceans to date, our results provide novel insight into the toxicophysiology of REY in marine biota. The neurotoxic/behavioural effects in T. cicada at concentrations with potential environmental relevance warn about the possibility of bottom-up ecological consequences in mining exposed fjords and deep-sea ecosystems, calling for follow-up studies and regulatory measures prior to the onset of REY mining in Norway.