A Crude Awakening: Effects of Crude Oil on Lipid Metabolism in Calanoid Copepods Terminating Diapause

Abstract

Calanus finmarchicus and Calanus glacialis are keystone zooplankton species in North Atlantic and Arctic marine ecosystems because they form a link in the trophic transfer of nutritious lipids from phytoplankton to predators on higher trophic levels. These calanoid copepods spend several months of the year in deep waters in a dormant state called diapause, after which they emerge in surface waters to feed and reproduce during the spring phytoplankton bloom. Disruption of diapause timing could have dramatic consequences for marine ecosystems. In the present study, Calanus C5 copepodites were collected in a Norwegian fjord during diapause and were subsequently experimentally exposed to the water-soluble fraction of a naphthenic North Sea crude oil during diapause termination. The copepods were sampled repeatedly while progressing toward adulthood and were analyzed for utilization of lipid stores and for differential expression of genes involved in lipid metabolism. Our results indicate that water-soluble fraction exposure led to a temporary pause in lipid catabolism, suggested by (i) slower utilization of lipid stores in water-soluble fraction-exposed C5 copepodites and (ii) more genes in the b-oxidation pathway being downregulated in water-soluble fraction-exposed C5 copepodites than in the control C5 copepodites. Because lipid content and/or composition may be an important trigger for termination of diapause, our results imply that the timing of diapause termination and subsequent migration to the surface may be delayed if copepods are exposed to oil pollution during diapause or diapause termination. This delay could have detrimental effects on ecosystem dynamics.

Lipid metabolism in Calanus finmarchicus is sensitive to variations in predation risk and food availability

“…This downregulation of lipid catabolism genes in the presence of a predator cue could indicate that the copepods may cope with stress by reducing their overall metabolism. Downregulated lipid metabolism in response to petroleum oil components was recently reported in C. finmarchicus 32 , and predation risk has been linked to lower resting metabolic rates in the amphipod Gammarus minus 42 , and to decreased swimming speed in the marine copepod Temora longicornis 43 . Reduced activity, causing a reduced energy demand, is a common response to predation risk in aquatic and terrestrial prey 44 , and may explain the decreased lipid utilization in the copepods exposed to a predator cue.…”

“…Thus, a similar pattern in lipid catabolism seems to occur in the late life stages in Calanus copepods, perhaps regardless of activity level, but modulated by both food availability and predation risk. Exposure to oil pollution has been observed to disrupt lipid catabolism 32 , indicating additional sensitivity to anthropogenic disturbances. In Neocalanus flemingeri lipid catabolism genes were in contrast upregulated towards the end of diapause (which occurs in adults), and did not become reduced 41 .…”

“…Catabolism of fatty acids occurs primarily in mitochondria through the ß-oxidation pathway 36 , and 63 gene transcripts (henceforth called "genes") encoding the enzymes in this pathway were recently identified in the C. finmarchicus transcriptome 21,21 . We assessed catabolism of lipids by investigating expression patterns of these genes, an approach previously used in studies on Calanus copepods 21,32 . To facilitate interpretation, the ß-oxidation gene expression results are referred to as patterns of either up-or downregulation based on the number of genes that are differentially expressed between treatments.…”

“…Hi-P High food and no predator cue, Hi + P High food and predator cue, Lo-P Low food and no predator cue, Lo + P Low food and predator cue. www.nature.com/scientificreports/ have been observed in Calanus copepods exposed to petrogenic oil components 32 . It is likely that egg production rates differed between the treatments, as both food availability and predation risk can affect reproduction in copepods 14,[52][53][54] .…”

“…In pre-reproductive copepods, lipid catabolism can be expected to be low when sufficient food is available, but may increase due to stress 28 and insufficient food availability 29 . However, downregulation of lipid catabolism by crustaceans in the presence of stressors has also been reported [30][31][32] , illustrating that lipid metabolism is sensitive to external factors. Studying lipid metabolism on a gene expression level can provide detailed knowledge on how lipid accumulation and catabolism is altered in response to environmental cues, possibly before these changes become evident on a physiological level.…”