Effects of actin remodeling inhibitors on cellular energy metabolism of a model marine bivalve, the Pacific oyster

TL;DR

This study investigates how actin remodeling affects energy use in oyster cells and finds that it contributes little to overall energy costs, but some inhibitors cause unexpected mitochondrial changes.

Contribution

The study experimentally quantifies actin remodeling energy costs in a marine ectotherm and reveals a novel link between actin disruption and mitochondrial proton leak.

Findings

Actin remodeling contributes less than 5% to cellular energy budget in oyster gill and mantle cells.

Cytochalasin D increases mitochondrial proton leak, suggesting a link between actin disorganization and mitochondrial maintenance costs.

Jasplakinolide and latrunculin B do not affect mitochondrial respiration, indicating different disruption mechanisms.

Abstract

Actin, the most abundant cellular protein, is essential for maintaining structural organization, mechanical stability and cellular motility. The actin cytoskeleton undergoes continuous ATP-dependent reorganization, incurring significant energy costs through treadmilling. However, experimental quantifications of these energy expenditures, especially in ectotherms, remain scarce. In this study, we assessed the energy costs of actin remodeling in the Pacific oyster Crassostrea [also Magallana] gigas, a marine bivalve, by measuring oxygen consumption in the presence of inhibitors of actin treadmilling (latrunculin B, jasplakinolide and cytochalasin D). Our results indicate that under normal physiological conditions, actin remodeling contributes less than 5% to the cellular energy budget in gill and mantle cells of oysters. Unexpectedly, cytochalasin D induced a marked increase in mitochondrial proton leak, observed both in intact cells and isolated mitochondria, suggesting a connection between actin disorganization and increased mitochondrial maintenance costs. Notably, jasplakinolide and latrunculin B, which inhibit actin treadmilling through different mechanisms from those of cytochalasin D, had no effect on mitochondrial respiration. This suggests that different mechanisms of actin cytoskeleton disruption can lead to distinct cellular outcomes. Given the significant role of proton leak in cellular respiration, these findings suggest that actin dynamics may play a crucial role in regulating mitochondrial metabolism, with broad implications for cellular energy costs. Further studies are needed to elucidate the underlying mechanisms of actin–mitochondria interactions and their broader relevance to the regulation of cellular metabolism in ectothermic species.

Summary: Actin treadmilling constitutes a minor energy cost in differentiated gill and mantle tissues of adult oysters.

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