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Human alterations to the marine environment such as an oil spill can induce oxidative stress in phytoplankton. Exposure to oil has been shown to be lethal to most phytoplankton species, but some are able to survive and grow at unaffected or reduced growth rates, which appears to be independent of the class and phylum of the phytoplankton and their ability to consume components of oil heterotrophically. The goal of this article is to test the role of core metabolism plasticity in the oil‐resisting ability of phytoplankton. Experiments were performed on the oil‐ resistant chlorophyte, Dunaliella tertiolecta, in control and water accommodated fractions of oil, with and without metabolic inhibitors targeting the core metabolic pathways. We observed that inhibiting pathways such as photosynthetic electron transport (PET) and pentose‐phosphate pathway were lethal; however, inhibition of pathways such as mitochondrial electron transport and cyclic electron transport caused growth to be arrested. Pathways such as photorespiration and Kreb's cycle appear to play a critical role in the oil‐tolerating ability of D. tertiolecta. Analysis of photo‐physiology revealed reduced PET under inhibition of photorespiration but not Kreb's cycle. Further studies showed enhanced flux through Kreb's cycle suggesting increased energy production and photorespiration counteract oxidative stress. Lastly, reduced extracellular carbohydrate secretion under oil exposure indicated carbon and energy conservation, which together with enhanced flux through Kreb's cycle played a major role in the survival of D. tertiolecta under oil exposure by meeting the additional energy demands. Overall, we present data that suggest the role of phenotypic plasticity of multiple core metabolic pathways in accounting for the oxidative stress tolerating ability of certain phytoplankton species. [ABSTRACT FROM AUTHOR]