Abstract
In most eukaryotic organisms, mitochondrial uncoupling mechanisms control ATP synthesis and reactive oxygen species production. One such mechanism is the permeability transition of the mitochondrial inner membrane. In mammals, ischemia–reperfusion events or viral diseases may induce ionic disturbances, such as calcium overload; this cation enters the mitochondria, thereby triggering the permeability transition. This phenomenon increases inner membrane permeability, affects transmembrane potential, promotes mitochondrial swelling, and induces apoptosis. Previous studies have found that the mitochondria of some crustaceans do not exhibit a calcium-regulated permeability transition. However, in the whiteleg shrimp Litopenaeus vannamei, contradictory evidence has prevented this phenomenon from being confirmed or rejected. Both the ability of L. vannamei mitochondria to take up large quantities of calcium through a putative mitochondrial calcium uniporter with conserved characteristics and permeability transition were investigated in this study by determining mitochondrial responses to cations overload. By measuring mitochondrial swelling and transmembrane potential, we investigated whether shrimp exposure to hypoxia-reoxygenation events or viral diseases may induce mitochondrial permeability transition. The results of this study demonstrate that shrimp mitochondria take up large quantities of calcium through a canonical mitochondrial calcium uniporter. Neither calcium nor other ions were observed to promote permeability transition. This phenomenon does not depend on the life cycle stage of shrimp, and it is not induced during hypoxia/reoxygenation events or in the presence of viral diseases. The absence of the permeability transition phenomenon and its adaptive meaning are discussed as a loss with biological advantages, possibly enabling organisms to survive under harsh environmental conditions.
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All data generated and analyzed during this study are included in this published article and files. The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
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We thank Consejo Nacional de Ciencia y Tecnología (CONACyT) for funding and Sandra Araujo Bernal and M.Sc. Trinidad Encinas-Garcia for providing technical support.
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This research was supported by the Consejo Nacional de Ciencia y Tecnologia (CONACYT, National Council for Research and Technology, Mexico) [Grant 241670 to AMA, and 252979 to ERV, graduate scholarship to CRA).
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R-A: Conceptualization, methodology, investigation, validation, writing, review and editing; R-Z: Methodology, investigation, validation, formal analysis; DR-V: Funding acquisition, review and editing; S-P: WSSV inoculation, methodology, validation, writing, review and editing; M-C: methodology, viral infection assay, formal analysis; M-R: Methodology, validation; G-R: Writing, review and editing; M-A: Conceptualization, methodology, writing, review and editing, supervision, project administration and funding acquisition.
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Rodriguez-Armenta, C., Reyes-Zamora, O., De la Re-Vega, E. et al. Adaptive mitochondrial response of the whiteleg shrimp Litopenaeus vannamei to environmental challenges and pathogens. J Comp Physiol B 191, 629–644 (2021). https://doi.org/10.1007/s00360-021-01369-7
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DOI: https://doi.org/10.1007/s00360-021-01369-7