Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
PLoS One
2019 Jan 01;143:e0214373. doi: 10.1371/journal.pone.0214373.
Show Gene links
Show Anatomy links
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
.
???displayArticle.abstract???
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.
???displayArticle.pubmedLink???
30901348
???displayArticle.pmcLink???PMC6430385 ???displayArticle.link???PLoS One
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).
Airaksinen,
Heat- and cold-inducible regulation of HSP70 expression in zebrafish ZF4 cells.
2003, Pubmed
Airaksinen,
Heat- and cold-inducible regulation of HSP70 expression in zebrafish ZF4 cells.
2003,
Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Beere,
Stress management - heat shock protein-70 and the regulation of apoptosis.
2001,
Pubmed
Clark,
Exceptional aerobic scope and cardiovascular performance of pink salmon (Oncorhynchus gorbuscha) may underlie resilience in a warming climate.
2011,
Pubmed
Collard,
Acid-base physiology response to ocean acidification of two ecologically and economically important holothuroids from contrasting habitats, Holothuria scabra and Holothuria parva.
2014,
Pubmed
,
Echinobase
Dahlhoff,
Biochemical indicators of stress and metabolism: applications for marine ecological studies.
2004,
Pubmed
Dong,
Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress.
2017,
Pubmed
Eliason,
Differences in thermal tolerance among sockeye salmon populations.
2011,
Pubmed
Ern,
Oxygen dependence of upper thermal limits in fishes.
2016,
Pubmed
FRY,
The relation of temperature to oxygen consumption in the goldfish.
1948,
Pubmed
Falfushynska,
Long-Term Acclimation to Different Thermal Regimes Affects Molecular Responses to Heat Stress in a Freshwater Clam Corbicula Fluminea.
2016,
Pubmed
Farrell,
Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations.
2008,
Pubmed
Feder,
The consequences of expressing hsp70 in Drosophila cells at normal temperatures.
1992,
Pubmed
Frederich,
Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado.
2000,
Pubmed
Fujikake,
Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress.
2005,
Pubmed
Giomi,
Improved heat tolerance in air drives the recurrent evolution of air-breathing.
2014,
Pubmed
Giomi,
A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs.
2013,
Pubmed
Giomi,
The importance of thermal history: costs and benefits of heat exposure in a tropical, rocky shore oyster.
2016,
Pubmed
Huang,
CAP3: A DNA sequence assembly program.
1999,
Pubmed
Jolly,
Role of the heat shock response and molecular chaperones in oncogenesis and cell death.
2000,
Pubmed
Kozera,
Reference genes in real-time PCR.
2013,
Pubmed
Leung,
Heatwaves diminish the survival of a subtidal gastropod through reduction in energy budget and depletion of energy reserves.
2017,
Pubmed
Melzner,
Temperature-dependent oxygen extraction from the ventilatory current and the costs of ventilation in the cephalopod Sepia officinalis.
2006,
Pubmed
Nguyen,
Upper temperature limits of tropical marine ectotherms: global warming implications.
2011,
Pubmed
Overgaard,
Validity of thermal ramping assays used to assess thermal tolerance in arthropods.
2012,
Pubmed
Owczarzy,
IDT SciTools: a suite for analysis and design of nucleic acid oligomers.
2008,
Pubmed
Priede,
Natural selection for energetic efficiency and the relationship between activity level and mortality.
1977,
Pubmed
Purcell,
The cost of being valuable: predictors of extinction risk in marine invertebrates exploited as luxury seafood.
2014,
Pubmed
,
Echinobase
Pörtner,
Ecology. Physiology and climate change.
2008,
Pubmed
Pörtner,
Climate change affects marine fishes through the oxygen limitation of thermal tolerance.
2007,
Pubmed
Pörtner,
Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals.
2001,
Pubmed
Rummer,
Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures.
2014,
Pubmed
Schramm,
A simple and reliable 5'-RACE approach.
2000,
Pubmed
Sejerkilde,
Effects of cold- and heat hardening on thermal resistance in Drosophila melanogaster.
2003,
Pubmed
Sokolova,
Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates.
2012,
Pubmed
Song,
Molecular characteristics of the HSP70 gene and its differential expression in female and male golden apple snails (Pomacea canaliculata) under temperature stimulation.
2014,
Pubmed
Srivastava,
Roles of heat-shock proteins in innate and adaptive immunity.
2002,
Pubmed
Stothard,
The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences.
2000,
Pubmed
Sunday,
Global analysis of thermal tolerance and latitude in ectotherms.
2011,
Pubmed
Sylvestre,
Thermal sensitivity of metabolic rates and swimming performance in two latitudinally separated populations of cod, Gadus morhua L.
2007,
Pubmed
Terblanche,
Critical thermal limits depend on methodological context.
2007,
Pubmed
Tewksbury,
Ecology. Putting the heat on tropical animals.
2008,
Pubmed
Vandesompele,
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.
2002,
Pubmed
Vazzana,
Cellular responses and HSP70 expression during wound healing in Holothuria tubulosa (Gmelin, 1788).
2015,
Pubmed
,
Echinobase
Verberk,
Can respiratory physiology predict thermal niches?
2016,
Pubmed
Vinagre,
Effect of warming rate on the critical thermal maxima of crabs, shrimp and fish.
2015,
Pubmed
Ye,
Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction.
2012,
Pubmed
