Core metabolism plasticity in phytoplankton: Response of Dunaliella tertiolecta to oil exposure

Abstract

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.

Field study on natural phytoplankton throughout “Bizerte City” oil spill on the south-western coast of the Mediterranean Sea

“…However, prymnesiophyceae can be a dominant group after an oil spill (Brussaard et al 2016). In fact, the sensitivity of phytoplankton to oil is largely species dependent, since toxic oil compounds can affect different cellular and molecular targets Kamalanathan et al 2021Kamalanathan et al , 2022. Furthermore, species can have differential core metabolism plasticity to counteract oil-induced oxidative stress and can modulate their tolerance to oil exposure (Kamalanathan et al 2021(Kamalanathan et al , 2022.…”

“…Oil exposure can be lethal for some species, but others can survive and grow at an unaffected or reduced rate. The oil-resisting ability of some phytoplankton species is related to the plasticity of their core metabolism, i.e., reduced extracellular carbohydrate secretion and enhanced ux through the Krebs cycle to conserve and increase energy production and counteract the oxidative stress caused by oil exposure (Kamalanathan et al 2021(Kamalanathan et al , 2022. Physiological traits such as cell size, motility and mixotrophy, are also important in determining the ability of species to survive oil exposure (Bretherton et al 2020).…”