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

Rodriguez-Armenta, Chrystian; Reyes-Zamora, Orlando; Re-Vega, Enrique De La; Sánchez‐Paz, Arturo; Mendoza–Cano, Fernando; Méndez-Romero, Ofelia; González‐Ríos, Humberto; Muhlia‐Almazán, Adriana

doi:10.1007/s00360-021-01369-7

Cited by 7 publications

(2 citation statements)

References 62 publications

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“…In Yarrowia lipolytica , it has been necessary to use ionophores and high Ca 2+ loads to force PT (Kovaleva et al., 2009 ). Also, in crustaceans such as Artemia franciscana , Litopenaeus vannamei , Lipidophtalmus louisianensis , Crangon crangon , and Palaemon serratus it has not been possible to induce PT by Ca 2+ overloading (Holman & Hand, 2009 ; Konrad et al., 2012 ; Menze et al., 2005 ; Rodriguez‐Armenta et al., 2021 ). In regard to structure, elimination of individual proteins has not led to conclusive results (Azzolin et al., 2010 ; Hurst et al., 2017 ; Izzo et al., 2016 ; Zoratti & Szabò, 1995 ).…”

Section: Discussionmentioning

confidence: 99%

Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Ricardez‐Garcia,

Reyes‐Becerril,

Mosqueda‐Martinez

et al. 2024

Physiological Reports

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Permeability transition pore (PTP) opening dissipates ion and electron gradients across the internal mitochondrial membrane (IMM), including excess Ca2+ in the mitochondrial matrix. After opening, immediate PTP closure must follow to prevent outer membrane disruption, loss of cytochrome c, and eventual apoptosis. Flickering, defined as the rapid alternative opening/closing of PTP, has been reported in heart, which undergoes frequent, large variations in Ca2+. In contrast, in tissues that undergo depolarization events less often, such as the liver, PTP would not need to be as dynamic and thus these tissues would not be as resistant to stress. To evaluate this idea, it was decided to follow the reversibility of the permeability transition (PT) in isolated murine mitochondria from two different tissues: the very dynamic heart, and the liver, which suffers depolarizations less frequently. It was observed that in heart mitochondria PT remained reversible for longer periods and at higher Ca2+ loads than in liver mitochondria. In all cases, Ca2+ uptake was inhibited by ruthenium red and PT was delayed by Cyclosporine A. Characterization of this phenomenon included measuring the rate of oxygen consumption, organelle swelling and Ca2+ uptake and retention. Results strongly suggest that there are tissue‐specific differences in PTP physiology, as it resists many more Ca2+ additions before opening in a highly active organ such as the heart than in an organ that seldom suffers Ca2+ loading, such as the liver.

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Section: Discussionmentioning

confidence: 99%

Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Ricardez‐Garcia,

Reyes‐Becerril,

Mosqueda‐Martinez

et al. 2024

Physiological Reports

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“…Mitochondria from oxyconformers such as the branchiopod A. fransciscana and the shrimp species Lepidophthalmus louisianensis , Crangon crangon , Palaemon serratus , and L. vannamei PTP opening is not induced by calcium overloads and these organelles can store high [Ca +2 ]. The absence of a calcium-regulated PTP in crustaceans has led to propose that other PUS such as UCPs and branched respiratory chains are critical for survival during stress ( Menze et al, 2005 ; Holman and Hand, 2009 ; Rodriguez-Armenta et al, 2021 ).…”

Section: Extrinsic Physiological Uncoupling Systems (Proton Sinks)mentioning

confidence: 99%

Thriving in Oxygen While Preventing ROS Overproduction: No Two Systems Are Created Equal

et al. 2022

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From 2.5 to 2.0 billion years ago, atmospheric oxygen concentration [O2] rose thousands of times, leading to the first mass extinction. Reactive Oxygen Species (ROS) produced by the non-catalyzed partial reduction of O2 were highly toxic eliminating many species. Survivors developed different strategies to cope with ROS toxicity. At the same time, using O2 as the final acceptor in respiratory chains increased ATP production manifold. Thus, both O2 and ROS were strong drivers of evolution, as species optimized aerobic metabolism while developing ROS-neutralizing mechanisms. The first line of defense is preventing ROS overproduction and two mechanisms were developed in parallel: 1) Physiological uncoupling systems (PUS), which increase the rate of electron fluxes in respiratory systems. 2) Avoidance of excess [O2]. However, it seems that as avoidance efficiency improved, PUSs became less efficient. PUS includes branched respiratory chains and proton sinks, which may be proton specific, the mitochondrial uncoupling proteins (UCPs) or unspecific, the mitochondrial permeability transition pore (PTP). High [O2] avoidance also involved different strategies: 1) Cell association, as in biofilms or in multi-cellularity allowed gas-permeable organisms (oxyconformers) from bacterial to arthropods to exclude O2. 2) Motility, to migrate from hypoxic niches. 3) Oxyregulator organisms: as early as in fish, and O2-impermeable epithelium excluded all gases and only exact amounts entered through specialized respiratory systems. Here we follow the parallel evolution of PUS and O2-avoidance, PUS became less critical and lost efficiency. In regard, to proton sinks, there is fewer evidence on their evolution, although UCPs have indeed drifted in function while in some species it is not clear whether PTPs exist.

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The branched mitochondrial respiratory chain from the jellyfish Stomolophus sp2 as a probable adaptive response to environmental changes

Nevarez-Lopez,

Muhlia-Almazan,

Gamero-Mora

et al. 2024

J Bioenerg Biomembr

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During their long evolutionary history, jelly sh have faced changes in multiple environmental factors, to which they may selectively x adaptations allowing some species to survive and inhabit diverse environments. Previous ndings have con rmed the jelly sh's ability to synthesize large ATP amounts, mainly produced by mitochondria, in response to environmental challenges. This study characterized the respiratory chain from the mitochondria of the jelly sh Stomolophus sp2 (previously misidenti ed as Stomolophus meleagris). The isolated mitochondrial oxygen consumption rates, multimeric complexes' in-gel activity, immunodetection, and mass spectrometry identi cation con rmed that the jelly sh mitochondrial respiratory chain contains the ve canonical complexes I to IV and F 0 F 1 -ATP synthase. In addition, our results con rmed the occurrence of four alternative enzymes integrated into a branched mitochondrial respiratory chain of Stomolophus sp2: an alternative oxidase and three dehydrogenases (two NADH type II enzymes and a mitochondrial glycerol-3-phosphate dehydrogenase). Signi cant differences in the transcript abundance of each alternative enzyme from jelly sh transcriptomes were detected after jelly sh were exposed to three different temperatures. These rst-time reported enzymes in cnidarians suggest the mitochondrial adaptative ability allowing jelly sh rapid metabolic responses to maintain energetic homeostasis and to face the temperature variations due to climate change.

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

Cited by 7 publications

References 62 publications

Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Thriving in Oxygen While Preventing ROS Overproduction: No Two Systems Are Created Equal

The branched mitochondrial respiratory chain from the jellyfish Stomolophus sp2 as a probable adaptive response to environmental changes

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

Cited by 7 publications

References 62 publications

Tissue‐specific differences in Ca2+ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Tissue‐specific differences in Ca2+ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Thriving in Oxygen While Preventing ROS Overproduction: No Two Systems Are Created Equal

The branched mitochondrial respiratory chain from the jellyfish Stomolophus sp2 as a probable adaptive response to environmental changes

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Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart

Tissue‐specific differences in Ca²⁺ sensitivity of the mitochondrial permeability transition pore (PTP). Experiments in male rat liver and heart