Adaptive mitochondrial response of the whiteleg shrimp Litopenaeus vannamei to environmental challenges and pathogens

Chrystian Rodriguez-Armenta, Orlando Reyes-Zamora, Enrique De la Re-Vega, Arturo Sanchez-Paz, Fernando Mendoza-Cano, Ofelia Mendez-Romero, Humberto Gonzalez-Rios, Adriana Muhlia-Almazan*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Pages (from-to)629-644
Number of pages16
JournalJournal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology
Volume191
Issue number4
DOIs
StatePublished - Jul 2021
Externally publishedYes

Bibliographical note

Funding Information:
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.

Funding Information:
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).

Funding Information:
We thank Consejo Nacional de Ciencia y Tecnolog?a (CONACyT) for funding and Sandra Araujo Bernal and M.Sc. Trinidad Encinas-Garcia for providing technical support.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Keywords

  • Adaptation
  • Calcium
  • Crustaceans
  • Mitochondria
  • Permeability transition
  • Uncoupling mechanisms

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