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Oil spill events in the marine environment can have a deleterious impact on the affected ecosystems, such as coral reefs, with direct consequences for their socioeconomic value. The mutualistic relationship between tropical corals and their dinoflagellate symbionts (Symbiodiniaceae) provide structural and nutritional basis for a high local biodiversity in oligotrophic waters. Here, we investigated effects of crude oil water-accommodated fraction on the competitive fitness of the model zooxanthellae species Symbiodinium glynnii. Results of laboratory essays demonstrate that crude oil carbon is incorporated into the cellular biomass with a concomitant change of δ13C isotopic value. Carcinogenic/mutagenic polycyclic aromatic hydrocarbons were identified in the culture media and were responsible for a linear reduction in population growth of S. glynnii, presumably related to energy relocation for DNA repair. Additionally, the experiments revealed that physiological effects induced by crude oil compounds are genetically inherited by the following generations under non-contaminated growth conditions, and induce a reduction in the competitive fitness to cope with other environmental parameters, such as low salinity. We suggest that the effects of crude oil contamination represent an imparing factor for S. glynnii coping with anthropogenic drivers (e.g. warming and acidification) and interfere with the delicate symbiont-host relationship of tropical corals. This is especially relevant in the coastal areas of northeastern Brazil where an oil spill event deposited crude oil on shallow water sediments with the potential to be resuspended to the water column by physical and/or biological activity, enhancing the risk of future coral bleaching events.