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Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra

The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SM...

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Autores principales: Kühnhold, Holger, Steinmann, Nuri, Huang, Yi-Hsuan, Indriana, Lisa, Meyer, Achim, Kunzmann, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6430385/
https://www.ncbi.nlm.nih.gov/pubmed/30901348
http://dx.doi.org/10.1371/journal.pone.0214373
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author Kühnhold, Holger
Steinmann, Nuri
Huang, Yi-Hsuan
Indriana, Lisa
Meyer, Achim
Kunzmann, Andreas
author_facet Kühnhold, Holger
Steinmann, Nuri
Huang, Yi-Hsuan
Indriana, Lisa
Meyer, Achim
Kunzmann, Andreas
author_sort Kühnhold, Holger
collection PubMed
description The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SMR) and maximal- (MMR) metabolic rates, especially in sluggish marine invertebrates with low oxygen consumption rates, such as sea cucumbers. In this study the AS concept was modified to define a Temperature-induced Aerobic Scope (TAS), based on metabolic rate changes due to temperature adjustments rather than traditionally used physical activity patterns. Consequentially, temperature dependent peak and bottom O(2) consumption rates, defined as Temperature-induced Maximal- (TMMR) and Standard Metabolic Rates (TSMR), respectively, served as MMR and SMR alternatives for the sea cucumber Holothuria scabra. TMMR and TSMR were induced through acute temperature change (2°C per hour; 17–41°C) until critical warm (WT(crit)) and cold (CT(crit)) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O(2) consumption of H. scabra peaked distinctly at WT(crit) of 38°C (TMMR = 33.2 ± 4.7 μgO(2) g(-1) h(-1)). A clear metabolic bottom line was reached at CT(crit) of 22°C (TSMR = 2.2 ± 1.4 μgO(2) g(-1) h(-1)). Within the thermal window of 22–38°C H. scabra sustained positive aerobic capacity, with assumed optimal performance range between 29–31.5°C (13.85–18.7 μgO(2) g(-1) h(-1)). Between 39–41°C H. scabra decreased respiration progressively, while gene expression levels of Hsp70 increased significantly at 41°C, indicating prioritization of heat shock response (HSR) and homeostatic disruption. At the cold end (17–22°C) homeostatic disruption was visible through incrementally increasing energetic expenses to fuel basal maintenance costs, but no Hsp70 overexpression occurred. TMMR, TSMR and TAS proved to be reliable metrics, similar to the traditional energetic key parameters MMR, SMR and AS, to determine a specific aerobic performance window for the sluggish bottom dwelling species H. scabra. In addition, the linkage between respiration physiology and molecular defense mechanisms showed valuable analytical synergies in terms of mechanistic prioritization as response to thermal stress. Overall, this study will help to define lethal temperatures for aquaculture and to predict the effects of environmental stress, such as ocean warming, in H. scabra.
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spelling pubmed-64303852019-04-01 Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra Kühnhold, Holger Steinmann, Nuri Huang, Yi-Hsuan Indriana, Lisa Meyer, Achim Kunzmann, Andreas PLoS One Research Article The Aerobic Scope (AS), which reflects the functional capacity for biological fitness, is a highly relevant proxy to determine thermal tolerance in various taxa. Despite the importance of this method, its implementation is often hindered, due to lacking techniques to accurately measure standard- (SMR) and maximal- (MMR) metabolic rates, especially in sluggish marine invertebrates with low oxygen consumption rates, such as sea cucumbers. In this study the AS concept was modified to define a Temperature-induced Aerobic Scope (TAS), based on metabolic rate changes due to temperature adjustments rather than traditionally used physical activity patterns. Consequentially, temperature dependent peak and bottom O(2) consumption rates, defined as Temperature-induced Maximal- (TMMR) and Standard Metabolic Rates (TSMR), respectively, served as MMR and SMR alternatives for the sea cucumber Holothuria scabra. TMMR and TSMR were induced through acute temperature change (2°C per hour; 17–41°C) until critical warm (WT(crit)) and cold (CT(crit)) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O(2) consumption of H. scabra peaked distinctly at WT(crit) of 38°C (TMMR = 33.2 ± 4.7 μgO(2) g(-1) h(-1)). A clear metabolic bottom line was reached at CT(crit) of 22°C (TSMR = 2.2 ± 1.4 μgO(2) g(-1) h(-1)). Within the thermal window of 22–38°C H. scabra sustained positive aerobic capacity, with assumed optimal performance range between 29–31.5°C (13.85–18.7 μgO(2) g(-1) h(-1)). Between 39–41°C H. scabra decreased respiration progressively, while gene expression levels of Hsp70 increased significantly at 41°C, indicating prioritization of heat shock response (HSR) and homeostatic disruption. At the cold end (17–22°C) homeostatic disruption was visible through incrementally increasing energetic expenses to fuel basal maintenance costs, but no Hsp70 overexpression occurred. TMMR, TSMR and TAS proved to be reliable metrics, similar to the traditional energetic key parameters MMR, SMR and AS, to determine a specific aerobic performance window for the sluggish bottom dwelling species H. scabra. In addition, the linkage between respiration physiology and molecular defense mechanisms showed valuable analytical synergies in terms of mechanistic prioritization as response to thermal stress. Overall, this study will help to define lethal temperatures for aquaculture and to predict the effects of environmental stress, such as ocean warming, in H. scabra. Public Library of Science 2019-03-22 /pmc/articles/PMC6430385/ /pubmed/30901348 http://dx.doi.org/10.1371/journal.pone.0214373 Text en © 2019 Kühnhold et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Kühnhold, Holger
Steinmann, Nuri
Huang, Yi-Hsuan
Indriana, Lisa
Meyer, Achim
Kunzmann, Andreas
Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title_full Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title_fullStr Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title_full_unstemmed Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title_short Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra
title_sort temperature-induced aerobic scope and hsp70 expression in the sea cucumber holothuria scabra
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6430385/
https://www.ncbi.nlm.nih.gov/pubmed/30901348
http://dx.doi.org/10.1371/journal.pone.0214373
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