The response of a boreal deep-sea sponge holobiont to an acute crude oil exposure: a mesocosm experiment

Abstract

Exploration and extraction of petroleum reserves in deep-sea marine ecosystems are ongoing activities world-wide and are continuously expanding with the identification of new reservoirs. Whilst a wealth of knowledge is known on the effects of oil spills on fish and other organisms in shallow water environments, there is a dearth of studies on the effects of subsurface oil spills (blowout events like the Deepwater Horizon) on deep-sea ecosystems. With exploration activities in deep-sea ecosystems predicted to increase, there are concerns regarding the accidental release of hydrocarbons into deep-sea ecosystems and the subsequent cascading effects on associated fauna. Sponges are abundant and ecologically valuable, known to be highly efficient filter feeders, contributing significantly to benthic pelagic coupling and providing habitat for a suite of organisms. However, sponges, which are sessile in nature, accumulate contaminants present in their ambient environment, potentially making them vulnerable to oil spills. Surprisingly, the impacts of oil on deep-sea sponges remain unexplored, despite sponges being particularly dominant around oil and gas exploration locations in the Northern Atlantic. Here are presented the findings from a mesocosm study, where the locally abundant deep-sea sponge Geodia barretti was exposed to three ecologically relevant oil concentrations for a duration of 8 days, followed by a recovery period of 30 days. A holistic approach elucidating the effects of oil on G. barretti focused on measuring changes in physiology (respiration rates), cellular stress (lysosomal membrane stability), and the structure of the sponge-associated microbiome using high-throughput sequencing of 16s rRNA gene amplicons. G. barretti did not demonstrate strong sub-lethal stress effects in response to an acute crude oil exposure. Respiration showed varying patterns of increased and decreased rates with no significant effect from the treatments while lysosomes were significantly impacted by oil, displaying destabilisation of lysosomal membranes. A 30 day recovery period allowed the sponges to recover to control levels. G. barretti’s microbiome was stable at the phylum and class level across all treatments and days of exposure. Some evidence suggest that this high microbial abundance sponge could naturally host microorganisms which play a role in oil degradation / detoxification. Further research should investigate the effects of a long-term oil exposure on G. barretti’s physiology, cellular stress, metabolism and associated microbial community. Of particular interest is the uncovering of the functions of the sponge microbiome in relation to oil contamination. Such studies enhance our understanding of the vulnerability and / or resilience of deep-sea sponges to hydrocarbon exposure, providing useful data for managing risks associated with oil and gas exploration in the Northern Atlantic.