The molecular arsenal of the key coastal bioturbator Hediste diversicolor faced with changing oceans

The importance of infaunal bioturbators for the functioning of marine ecosystems cannot be overstated. Inhabitants of estuarine and coastal habitats are expected to show resilience to fluctuations in seawater temperature and pH, which adds complexity to our understanding of the effects of global change drivers. Further, stress responses may be propagated through chemical cues within and across species, which may amplify the costs of life and alter species interactions. Research into the molecular mechanisms underlying this resilience has been limited by a lack of annotated genomes and associated molecular tools. In this study, we present the first chromosome-level, annotated draft genome of the marine ragworm Hediste diversicolor, specifically mapping genes important for chemical communication, sensing and pH homeostasis. Using these resources, we then evaluate the transcriptomic and behavioural responses of two distinct populations -- one field-sampled from Portugal (Ria Formosa) and one laboratory-acclimated and -bred from the United Kingdom (Humber) -- to changes in seawater pH, temperature, and odour cues from a low pH-stressed predator. Both populations displayed adaptive responses to future oceanic conditions, with targeted acid-base regulation in the Ria Formosa population experiment, and broader changes in metabolism and growth genes in the Humber population experiment. Chemical cues from stressed fish predators induced genes related to Schreckstoff biosynthesis in ragworms. Additionally, under future ocean conditions including increased temperature, the Humber population exhibited signs of cellular stress and damage. Our findings using the new annotated genome offer novel insights into the molecular arsenal of acid-base regulation which aids in predicting the impacts of an increasingly acidified and unstable ocean, and to transfer this knowledge to investigate these mechanisms in species with less tolerance.