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PLoS One
2019 Jan 01;143:e0214373. doi: 10.1371/journal.pone.0214373.
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Temperature-induced aerobic scope and Hsp70 expression in the sea cucumber Holothuria scabra.
Kühnhold H
,
Steinmann N
,
Huang YH
,
Indriana L
,
Meyer A
,
Kunzmann A
.
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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 O2 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 (WTcrit) and cold (CTcrit) temperatures were reached, respectively. In addition, Hsp70 gene expression linked to respiration rates served as synergistic markers to confirm critical threshold temperatures. O2 consumption of H. scabra peaked distinctly at WTcrit of 38°C (TMMR = 33.2 ± 4.7 μgO2 g-1 h-1). A clear metabolic bottom line was reached at CTcrit of 22°C (TSMR = 2.2 ± 1.4 μgO2 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 μgO2 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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30901348
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Fig 1. Average (mean ± standard deviation) relative normalized Hsp70 gene expression, for the two temperature manipulation experiments with eight biological replicates (n = 8), (1) cold (17°C; n = 8; p = 0.34) and (2) warm (41°C; n = 8; p = 0.00086) compared to the pooled controls (29°C; n = 16).Differences between treatments were calculated using a Mann-Whitney test. Significant differences are indicated for P<0.05 (*) and P<0.01 (**).
Fig 2. O2 consumption rate of Holothuria scabra at different temperatures, obtained from four warm and cold experimental replications.Points represent means ± s.d. of eight biological replicates (n = 8). Upper red dotted line indicate temperature-induced maximal metabolic rate (TMMR), at the critical warm temperature (WTcrit; 38°C), lower red dotted line marks the start of the temperature-induced standard metabolic rate (TSMR), at critical cold temperature (CTcrit; 22°C). The difference between TMMR and TSMR define the temperature-induced aerobic scope (TAS) for H. scabra (black brace). Beyond CTcrit and WTcrit (22–38°C) progressively negative aerobic performance caused by growing dependency on energy reserves and declining aerobic capacity, respectively, indicate homeostatic disruption. Overexpression of Hsp70 occurs only at the warm temperature maximum (41°C).
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