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Ectotherms Metabolism: Plasticity and Adaptation

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A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Environmental Metabolomics".

Deadline for manuscript submissions: closed (15 October 2021) | Viewed by 19260

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Special Issue Editors

Prof. Pierre Blier

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Guest Editor

Department of Biology, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC G5L 3A1, Canada
Interests: temperature; global change; mitochondria; energy metabolism; omics; evolution; oxygen

Dr. Hélène Lemieux

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Guest Editor

Faculty Saint-Jean, Dept. of Medicine, Women and Children's Health Research Institute, 576 Medical Science Building, University of Alberta, Edmonton, AB T6G 2H7, Canada
Interests: mitochondrial physiology related to health and diseases

Special Issue Information

Dear Colleagues,

Since pioneer work on metabolism in first half of twentieth century, metabolic organization (enzyme activities, pathways and network regulation) has been shown to be quite variable among tissues and organisms. The first observations of the impact of environmental conditions (for example temperature or water osmolarity) on metabolism established ectotherms animals as convenient models to reveal adaptations of metabolic phenotypes. The comparative approach allowed highlighting key responses or adjustments to face the wide range of environments occupied by animals, thus ensuring cellular bioenergetic requirements for life history. While this approach contributed to draw big pictures of metabolic and bioenergetic strategies, the development of the fields of “evolutionary physiology” and “conservation physiology” in the 90s along with appearance of new omic tools and refinement of traditional tools (microscopy, high resolution respirometry etc.) led to questioning the plasticity and evolvability of metabolic organization. In this new context, the ectotherms organisms are still champion models to scrutinize the range and mode of adaptation of cellular metabolism. This topic is of paramount importance in the context of global climate changes. We are therefore seeking, in this special issue, for original contributions on the responses of cellular bioenergetic metabolism of ectotherms to environmental gradient or perturbations as well as on putative acclimatory or adaptive responses to these environmental factors.

Prof. Pierre Blier
Dr. Hélène Lemieux
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Metabolites is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

temperature
global change
mitochondria
energy metabolism
omics
evolution
oxygen

Published Papers (5 papers)

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Research

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29 pages, 4377 KiB

Open AccessArticle

Tolerant Larvae and Sensitive Juveniles: Integrating Metabolomics and Whole-Organism Responses to Define Life-Stage Specific Sensitivity to Ocean Acidification in the American Lobster

by Fanny Noisette, Piero Calosi, Diana Madeira, Mathilde Chemel, Kayla Menu-Courey, Sarah Piedalue, Helen Gurney-Smith, Dounia Daoud and Kumiko Azetsu-Scott

Metabolites 2021, 11(9), 584; https://doi.org/10.3390/metabo11090584 - 30 Aug 2021

Cited by 13 | Viewed by 3598

Abstract

Bentho-pelagic life cycles are the dominant reproductive strategy in marine invertebrates, providing great dispersal ability, access to different resources, and the opportunity to settle in suitable habitats upon the trigger of environmental cues at key developmental moments. However, free-dispersing larvae can be highly sensitive to environmental changes. Among these, the magnitude and the occurrence of elevated carbon dioxide (CO₂) concentrations in oceanic habitats is predicted to exacerbate over the next decades, particularly in coastal areas, reaching levels beyond those historically experienced by most marine organisms. Here, we aimed to determine the sensitivity to elevated pCO₂ of successive life stages of a marine invertebrate species with a bentho-pelagic life cycle, exposed continuously during its early ontogeny, whilst providing in-depth insights on their metabolic responses. We selected, as an ideal study species, the American lobster Homarus americanus, and investigated life history traits, whole-organism physiology, and metabolomic fingerprints from larval stage I to juvenile stage V exposed to different pCO₂ levels. Current and future ocean acidification scenarios were tested, as well as extreme high pCO₂/low pH conditions that are predicted to occur in coastal benthic habitats and with leakages from underwater carbon capture storage (CCS) sites. Larvae demonstrated greater tolerance to elevated pCO₂, showing no significant changes in survival, developmental time, morphology, and mineralisation, although they underwent intense metabolomic reprogramming. Conversely, juveniles showed the inverse pattern, with a reduction in survival and an increase in development time at the highest pCO₂ levels tested, with no indication of metabolomic reprogramming. Metabolomic sensitivity to elevated pCO₂ increased until metamorphosis (between larval and juvenile stages) and decreased afterward, suggesting this transition as a metabolic keystone for marine invertebrates with complex life cycles. Full article

(This article belongs to the Special Issue Ectotherms Metabolism: Plasticity and Adaptation)

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17 pages, 3017 KiB

Open AccessArticle

Emersion and Relative Humidity Modulate Stress Response and Recovery Dynamics in Juvenile Mussels (Perna canaliculus)

by Natalí J. Delorme, David J. Burritt, Norman L. C. Ragg and Paul M. South

Metabolites 2021, 11(9), 580; https://doi.org/10.3390/metabo11090580 - 27 Aug 2021

Cited by 13 | Viewed by 2300

Abstract

The early stages of intertidal mussels, including the green-lipped mussel, Perna canaliculus, face both direct and indirect environmental threats. Stressors may influence physiological status and, ultimately, survival. An understanding of the nature of stress experienced is critical to inform conservation and aquaculture efforts. Here, we investigated oxidative stress dynamics in juvenile P. canaliculus in relation to emersion duration (1–20 h) and relative humidity (RH, 29–98%) by quantifying oxidative damage (protein carbonyls, lipid hydroperoxides, 8-hydroxydeoxyguanosine) and enzymatic antioxidants (superoxide dismutase, catalase, glutathione peroxidase and reductase). Mussels held in low RH during emersion experienced severe water loss (>70%), high mortality (>80%) and increased oxidative damage (35–45% increase compared to control conditions), while mussels held at high RH were not impacted, even after 20 h of air exposure. Following re-immersion, reoxygenation stress resulted in further increases in damage markers in mussels that had experienced dryer emersion conditions; protective action of antioxidants increased steadily during the 10 h re-immersion period, apparently supporting a reduction in damage markers after 1–5 h of immersion. Clearly, conditions during emersion, as well as duration, substantially influence physiological performance and recovery of juvenile mussels. Successful recruitment to intertidal beds or survival in commercial aquaculture operations may be mediated by the nature of emersion stress experienced by these vulnerable juveniles. Full article

(This article belongs to the Special Issue Ectotherms Metabolism: Plasticity and Adaptation)

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13 pages, 1542 KiB

Open AccessEditor’s ChoiceArticle

Proline as a Sparker Metabolite of Oxidative Metabolism during the Flight of the Bumblebee, Bombus impatiens

by Nadia Stec, Ammar Saleem and Charles-A. Darveau

Metabolites 2021, 11(8), 511; https://doi.org/10.3390/metabo11080511 - 4 Aug 2021

Cited by 10 | Viewed by 2566

Abstract

Several insect species use the amino acid proline as a major energy substrate. Although initially thought to be limited to blood-feeding dipterans, studies have revealed this capability is more widespread. Recent work with isolated flight muscle showed that the bumblebee Bombus impatiens can oxidize proline at a high rate. However, its role as a metabolic fuel to power flight is unclear. To elucidate the extent to which proline is oxidized to power flight and how its contribution changes during flight, we profiled 14 metabolites central to energy and proline metabolism at key time points in flight muscle and abdominal tissues. Ultra-high performance liquid chromatography-electrospray ionization-quadrupole time of flight mass spectrometry (UPLC-ESI-QTOF MS) analysis revealed that proline is likely used as a sparker metabolite of the tricarboxylic acid cycle at the onset of flight, whereby it supplements the intermediates of the cycle. Carbohydrates are the major energy substrates, which is evidenced by marked decreases in abdominal glycogen stores and a lack of alanine accumulation to replenish flight muscle proline. The time course of fuel stores and metabolites changes during flight highlights homeostatic regulation of energy substrates and patterns of changes in metabolic intermediates within pathways. This study clarifies the role of proline and carbohydrate metabolism during flight in hymenopterans, such as B. impatiens. Full article

(This article belongs to the Special Issue Ectotherms Metabolism: Plasticity and Adaptation)

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17 pages, 1341 KiB

Open AccessFeature PaperEditor’s ChoiceArticle

Goldfish Response to Chronic Hypoxia: Mitochondrial Respiration, Fuel Preference and Energy Metabolism

by Elie Farhat, Hang Cheng, Caroline Romestaing, Matthew Pamenter and Jean-Michel Weber

Metabolites 2021, 11(3), 187; https://doi.org/10.3390/metabo11030187 - 22 Mar 2021

Cited by 27 | Viewed by 5633

Abstract

Hypometabolism is a hallmark strategy of hypoxia tolerance. To identify potential mechanisms of metabolic suppression, we have used the goldfish to quantify the effects of chronically low oxygen (4 weeks; 10% air saturation) on mitochondrial respiration capacity and fuel preference. The responses of key enzymes from glycolysis, β-oxidation and the tricarboxylic acid (TCA) cycle, and Na⁺/K⁺-ATPase were also monitored in various tissues of this champion of hypoxia tolerance. Results show that mitochondrial respiration of individual tissues depends on oxygen availability as well as metabolic fuel oxidized. All the respiration parameters measured in this study (LEAK, OXPHOS, Respiratory Control Ratio, CCCP-uncoupled, and COX) are affected by hypoxia, at least for one of the metabolic fuels. However, no common pattern of changes in respiration states is observed across tissues, except for the general downregulation of COX that may help metabolic suppression. Hypoxia causes the brain to switch from carbohydrates to lipids, with no clear fuel preference in other tissues. It also downregulates brain Na⁺/K⁺-ATPase (40%) and causes widespread tissue-specific effects on glycolysis and beta-oxidation. This study shows that hypoxia-acclimated goldfish mainly promote metabolic suppression by adjusting the glycolytic supply of pyruvate, reducing brain Na⁺/K⁺-ATPase, and downregulating COX, most likely decreasing mitochondrial density. Full article

(This article belongs to the Special Issue Ectotherms Metabolism: Plasticity and Adaptation)

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Review

Jump to: Research

20 pages, 684 KiB

Open AccessReview

Exploring Thermal Sensitivities and Adaptations of Oxidative Phosphorylation Pathways

by Hélène Lemieux and Pierre U. Blier

Metabolites 2022, 12(4), 360; https://doi.org/10.3390/metabo12040360 - 17 Apr 2022

Cited by 6 | Viewed by 3770

Abstract

Temperature shifts are a major challenge to animals; they drive adaptations in organisms and species, and affect all physiological functions in ectothermic organisms. Understanding the origin and mechanisms of these adaptations is critical for determining whether ectothermic organisms will be able to survive when faced with global climate change. Mitochondrial oxidative phosphorylation is thought to be an important metabolic player in this regard, since the capacity of the mitochondria to produce energy greatly varies according to temperature. However, organism survival and fitness depend not only on how much energy is produced, but, more precisely, on how oxidative phosphorylation is affected and which step of the process dictates thermal sensitivity. These questions need to be addressed from a new perspective involving a complex view of mitochondrial oxidative phosphorylation and its related pathways. In this review, we examine the effect of temperature on the commonly measured pathways, but mainly focus on the potential impact of lesser-studied pathways and related steps, including the electron-transferring flavoprotein pathway, glycerophosphate dehydrogenase, dihydroorotate dehydrogenase, choline dehydrogenase, proline dehydrogenase, and sulfide:quinone oxidoreductase. Our objective is to reveal new avenues of research that can address the impact of temperature on oxidative phosphorylation in all its complexity to better portray the limitations and the potential adaptations of aerobic metabolism. Full article

(This article belongs to the Special Issue Ectotherms Metabolism: Plasticity and Adaptation)

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