Membrane lipid metabolism, heat shock response, and energy costs mediate the interaction between acclimatization and heat hardening response

2021 ◽  
Author(s):  
Wenyi Zhang ◽  
Yunwei Dong
Keyword(s):  
Thermal Stress ◽  
Lipid Metabolism ◽  
Heat Shock ◽  
Thermal Tolerance ◽  
Global Climate ◽  
Membrane Lipid ◽  
Maximum Temperature ◽  
Energy Costs ◽  
Thermal Plasticity ◽  
Heat Hardening

Thermal plasticity on different timescales, including acclimation/acclimatization and heat hardening response – a rapid adjustment for thermal tolerance after nonlethal thermal stress, can interact to improve the resilience of organisms to thermal stress. However, little is known about physiological mechanisms mediating this interaction. To investigate underpinnings of heat hardening responses after acclimatization in warm seasons, we measured thermal tolerance plasticity, compared transcriptomic and metabolomic changes after heat hardening at 33 or 37oC followed by recovery of 3 h or 24 h in an intertidal bivalve Sinonovacula constricta. Clams showed explicit heat hardening responses after acclimatization in a warm season. The higher inducing temperature (37oC) caused less effective heat hardening effects than the inducing temperature that was closer to the seasonal maximum temperature (33oC). Metabolomic analysis highlighted the elevated contents of glyceropholipids in all heat-hardened clams, which may help to maintain the structure and function of the membrane. Heat shock proteins (HSPs) tended to be up-regulated after heat hardening at 37oC but not at 33oC, indicating that there was no complete dependency of heat hardening effects on up-regulated HSPs. Enhanced energy metabolism and decreased energy reserves were observed after heat hardening at 37oC, suggesting more energy costs during exposure to a higher inducing temperature which may restrict heat hardening effects. These results highlighted the mediating role of membrane lipid metabolism, heat shock responses, and energy costs in the interaction between heat hardening response and seasonal acclimatization, and benefit the mechanistic understanding of evolutionary change and thermal plasticity during global climate change.

scholarly journals Comparison of Static and Dynamic Assays When Quantifying Thermal Plasticity of Drosophilids

Insects ◽  
2020 ◽  
Vol 11 (8) ◽  
pp. 537
Author(s):  
Christian Winther Bak ◽  
Simon Bahrndorff ◽  
Natasja Krog Noer ◽  
Lisa Bjerregaard Jørgensen ◽  
Johannes Overgaard ◽  
...  
Keyword(s):  
Critical Temperature ◽  
Constant Temperature ◽  
Heat Tolerance ◽  
Thermal Tolerance ◽  
Physiological Trait ◽  
Thermal Plasticity ◽  
Heat Hardening ◽  
Temperature Interaction ◽  
Dynamic Assay ◽  
Species Specific

Numerous assays are used to quantify thermal tolerance of arthropods including dynamic ramping and static knockdown assays. The dynamic assay measures a critical temperature while the animal is gradually heated, whereas the static assay measures the time to knockdown at a constant temperature. Previous studies indicate that heat tolerance measured by both assays can be reconciled using the time × temperature interaction from “thermal tolerance landscapes” (TTLs) in unhardened animals. To investigate if this relationship remains true within hardened animals, we use a static assay to assess the effect of heat hardening treatments on heat tolerance in 10 Drosophila species. Using this TTL approach and data from the static heat knockdown experiments, we model the expected change in dynamic heat knockdown temperature (CTmax: temperature at which flies enter coma) and compare these predictions to empirical measurements of CTmax. We find that heat tolerance and hardening capacity are highly species specific and that the two assays report similar and consistent responses to heat hardening. Tested assays are therefore likely to measure the same underlying physiological trait and provide directly comparable estimates of heat tolerance. Regardless of this compliance, we discuss why and when static or dynamic assays may be more appropriate to investigate ectotherm heat tolerance.

scholarly journals Heat shock protein gene expression is higher and more variable with thermal stress and mutation accumulation in Daphnia

2021 ◽  
Author(s):  
Henry Scheffer ◽  
Jeremy Coate ◽  
Eddie K. H. Ho ◽  
Sarah Schaack
Keyword(s):  
Gene Expression ◽  
Thermal Stress ◽  
Heat Shock ◽  
De Novo ◽  
Global Climate ◽  
Mutation Accumulation ◽  
Integrative Approach ◽  
Expression Levels ◽  
Shock Proteins ◽  
Quantify Gene Expression

AbstractUnderstanding the genetic architecture of the stress response and its ability to evolve in response to different stressors requires an integrative approach. Here we quantify gene expression changes in response to two stressors associated with global climate change and habitat loss—heat shock and mutation accumulation. We measure expression levels for two Heat Shock Proteins (HSP90 and HSP60)—members of an important family of conserved molecular chaperones that have been shown to play numerous roles in the cell. While HSP90 assists with protein folding, stabilization, and degradation throughout the cell, HSP60 primarily localizes to the mitochondria and mediates de novo folding and stress-induced refolding of proteins. We perform these assays in Daphnia magna originally collected from multiple genotypes and populations along a latitudinal gradient, which differ in their annual mean, maximum, and range of temperatures. We find significant differences in overall expression between loci (10-fold), in response to thermal stress (~6x increase) and with mutation accumulation (~4x increase). Importantly, stressors interact synergistically to increase gene expression levels when more than one is applied (increasing, on average, >20x). While there is no evidence for differences among the three populations assayed, individual genotypes vary considerably in HSP90 expression. Overall, our results support previous proposals that HSP90 may act as an important buffer against not only heat, but also mutation, and expands this hypothesis to include another member of the gene family acting in a different domain of the cell.

scholarly journals Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies

2019 ◽  
Author(s):  
Jose Santinni Roma ◽  
Shaina D’Souza ◽  
Patrick J. Somers ◽  
Leah F. Cabo ◽  
Ruhan Farsin ◽  
...  
Keyword(s):  
Thermal Stress ◽  
Heat Shock ◽  
Stress Responses ◽  
Thermal Tolerance ◽  
Molecular Mechanisms ◽  
Symbiotic Bacteria ◽  
Tsetse Flies ◽  
African Trypanosomes ◽  
Sodalis Glossinidius ◽  
Insight Into

ABSTRACTTsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly within multiple tsetse tissues, has been implicated as a mediator of trypanosome infection establishment in the fly’s gut. Tsetse’s gut-associated population of Sodalis are subjected to marked temperature fluctuations each time their ectothermic fly host imbibes vertebrate blood. The molecular mechanisms that Sodalis employs to deal with this heat stress are unknown. In this study, we examined the thermal tolerance and heat shock response of Sodalis. When grown on BHI agar plates, the bacterium exhibited the most prolific growth at 25°C, and did not grow at temperatures above 30°C. Growth on BHI agar plates at 31°C was dependent on either the addition of blood to the agar or reduction in oxygen levels. Sodalis was viable in liquid cultures for 24 hours at 30°C, but began to die upon further exposure. The rate of death increased with increased temperature. Similarly, Sodalis was able to survive for 48 hours within tsetse flies housed at 30°C, while a higher temperature (37°C) was lethal. Sodalis’ genome contains homologues of the heat shock chaperone protein-encoding genes dnaK, dnaJ, and grpE, and their expression was up-regulated in thermally stressed Sodalis, both in vitro and in vivo within tsetse flies. Arrested growth of E. coli dnaK, dnaJ, or grpE mutants under thermal stress was reversed when the cells were transformed with a low copy plasmid that encoded the Sodalis homologues of these genes. The information contained in this study provides insight into how arthropod vector enteric commensals, many of which mediate their host’s ability to transmit pathogens, mitigate heat shock associated with the ingestion of a blood meal.AUTHOR SUMMARYMicroorganisms associated with insects must cope with fluctuating temperatures. Because symbiotic bacteria influence the biology of their host, how they respond to temperature changes will have an impact on the host and other microorganisms in the host. The tsetse fly and its symbionts represent an important model system for studying thermal tolerance because the fly feeds exclusively on vertebrate blood and is thus exposed to dramatic temperature shifts. Tsetse flies house a microbial community that can consist of symbiotic and environmentally acquired bacteria, viruses, and parasitic African trypanosomes. This work, which makes use of tsetse’s commensal symbiont, Sodalis glossinidius, is significance because it represents the only examination of thermal tolerance mechanisms in a bacterium that resides indigenously within an arthropod disease vector. A better understanding of the biology of thermal tolerance in Sodalis provides insight into thermal stress survival in other insect symbionts and may yield information to help control vector-borne disease.

Stress proteins and thermotolerance in psychrotrophic yeasts from arctic environments

1987 ◽  
Vol 33 (5) ◽  
pp. 383-389 ◽  
Author(s):  
Gary R. Berg ◽  
William E. Inniss ◽  
John J. Heikkila
Keyword(s):  
Thermal Stress ◽  
Heat Shock ◽  
Heat Shock Protein ◽  
Stress Proteins ◽  
The Arctic ◽  
Maximum Temperature ◽  
Maximum Heat ◽  
Physiological Range

The protein synthetic responses to heat shock of two psychrotrophic yeasts Trichosporon pullulans and Sporobolomyces salmonicolor, isolated from the Arctic, were examined. The temperature of maximum heat shock protein induction was above the maximum temperature for growth in Trichosporon pullulans, but was within the physiological range in Sporobolomyces salmonicolor. Heat shock protein synthetic rates remained elevated in both microorganisms for at least 4 h when the temperature used for heat shock was within the physiological growth range. Both of these nonfermentative yeasts showed a protein synthetic response to recovery from anaerobiosis similar to that shown to heat shock. Trichosporon pullulans failed to show any increased resistance to a lethal thermal stress concomitant with the induction of stress proteins due to heat shock or recovery from anoxia.

Extracellular Proteins as Enterobacterial Thermometers

2003 ◽  
Vol 86 (1-2) ◽  
pp. 139-156 ◽  
Author(s):  
Robin J. Rowbury
Keyword(s):  
Thermal Stress ◽  
Heat Shock ◽  
Stress Responses ◽  
Direct Evidence ◽  
Experimental Studies ◽  
Extracellular Proteins ◽  
Temperature Changes ◽  
Induction Components ◽  
Cellular Components ◽  
Thermal Stimuli

Biological thermometers are cellular components or structures which sense increasing temperatures, interaction of the thermometer and the thermal stress bringing about the switching-on of inducible responses, with gradually enhanced levels of response induction following gradually increasing temperatures. In enterobacteria, for studies of such thermometers, generally induction of heat shock protein (HSP) synthesis has been examined, with experimental studies aiming to establish (often indirectly) how the temperature changes which initiate HSP synthesis are sensed; numerous other processes and responses show graded induction as temperature is increased, and how the temperature changes which induce these are sensed is also of interest. Several classes of intracellular component and structure have been proposed as enterobacterial thermometers, with the ribosome and the DnaK chaperone being the most favoured, although for many of the proposed intracellular thermometers, most of the evidence for their functioning in this way is indirect. In contrast to the above, the studies reviewed here firmly establish that for four distinct stress responses, which are switched-on gradually as temperature increases, temperature changes are sensed by extracellular components (extracellular sensing components, ESCs) i.e. there is firm and direct evidence for the occurrence of extracellular thermometers. All four thermometers described here are proteins, which appear to be distinct and different from each other, and on sensing thermal stress are activated by it to four distinct extracellular induction components (EICs), which interact with receptors on the surface of organisms to induce the appropriate responses. It is predicted that many other temperature-induced processes, including the synthesis of HSPs, will be switched-on following the activation of similar extracellular thermometers by thermal stimuli.

scholarly journals Triple-Knockout, Synuclein-Free Mice Display Compromised Lipid Pattern

Molecules ◽  
2021 ◽  
Vol 26 (11) ◽  
pp. 3078
Author(s):  
Irina A. Guschina ◽  
Natalia Ninkina ◽  
Andrei Roman ◽  
Mikhail V. Pokrovskiy ◽  
Vladimir L. Buchman
Keyword(s):  
Fatty Acids ◽  
Lipid Metabolism ◽  
Family Members ◽  
Ether Lipid ◽  
Brain Regions ◽  
Membrane Lipid ◽  
Lipid Binding ◽  
Synaptic Functions ◽  
Ethanolamine Plasmalogens ◽  
Lipid Pattern

Recent studies have implicated synucleins in several reactions during the biosynthesis of lipids and fatty acids in addition to their recognised role in membrane lipid binding and synaptic functions. These are among aspects of decreased synuclein functions that are still poorly acknowledged especially in regard to pathogenesis in Parkinson’s disease. Here, we aimed to add to existing knowledge of synuclein deficiency (i.e., the lack of all three family members), with respect to changes in fatty acids and lipids in plasma, liver, and two brain regions in triple synuclein-knockout (TKO) mice. We describe changes of long-chain polyunsaturated fatty acids (LCPUFA) and palmitic acid in liver and plasma, reduced triacylglycerol (TAG) accumulation in liver and non-esterified fatty acids in plasma of synuclein free mice. In midbrain, we observed counterbalanced changes in the relative concentrations of phosphatidylcholine (PC) and cerebrosides (CER). We also recorded a notable reduction in ethanolamine plasmalogens in the midbrain of synuclein free mice, which is an important finding since the abnormal ether lipid metabolism usually associated with neurological disorders. In summary, our data demonstrates that synuclein deficiency results in alterations of the PUFA synthesis, storage lipid accumulation in the liver, and the reduction of plasmalogens and CER, those polar lipids which are principal compounds of lipid rafts in many tissues. An ablation of all three synuclein family members causes more profound changes in lipid metabolism than changes previously shown to be associated with γ-synuclein deficiency alone. Possible mechanisms by which synuclein deficiency may govern the reported modifications of lipid metabolism in TKO mice are proposed and discussed.

scholarly journals Lipid Remodeling Confers Osmotic Stress Tolerance to Embryogenic Cells during Cryopreservation

2021 ◽  
Vol 22 (4) ◽  
pp. 2174
Author(s):  
Liang Lin ◽  
Junchao Ma ◽  
Qin Ai ◽  
Hugh W. Pritchard ◽  
Weiqi Li ◽  
...  
Keyword(s):  
Lipid Metabolism ◽  
Technology Development ◽  
Membrane Lipids ◽  
Species Conservation ◽  
Membrane Lipid ◽  
Cell Integrity ◽  
Embryogenic Cells ◽  
Osmotic Stress Tolerance ◽  
Lipid Species ◽  
Magnolia Officinalis

Plant species conservation through cryopreservation using plant vitrification solutions (PVS) is based in empiricism and the mechanisms that confer cell integrity are not well understood. Using ESI-MS/MS analysis and quantification, we generated 12 comparative lipidomics datasets for membranes of embryogenic cells (ECs) of Magnolia officinalis during cryogenic treatments. Each step of the complex PVS-based cryoprotocol had a profoundly different impact on membrane lipid composition. Loading treatment (osmoprotection) remodeled the cell membrane by lipid turnover, between increased phosphatidic acid (PA) and phosphatidylglycerol (PG) and decreased phosphatidylcholine (PC) and phosphatidylethanolamine (PE). The PA increase likely serves as an intermediate for adjustments in lipid metabolism to desiccation stress. Following PVS treatment, lipid levels increased, including PC and PE, and this effectively counteracted the potential for massive loss of lipid species when cryopreservation was implemented in the absence of cryoprotection. The present detailed cryobiotechnology findings suggest that the remodeling of membrane lipids and attenuation of lipid degradation are critical for the successful use of PVS. As lipid metabolism and composition varies with species, these new insights provide a framework for technology development for the preservation of other species at increasing risk of extinction.

scholarly journals Heat shock factor 2 is required for maintaining proteostasis against febrile-range thermal stress and polyglutamine aggregation

2011 ◽  
Vol 22 (19) ◽  
pp. 3571-3583 ◽  
Author(s):  
Toyohide Shinkawa ◽  
Ke Tan ◽  
Mitsuaki Fujimoto ◽  
Naoki Hayashida ◽  
Kaoru Yamamoto ◽  
...  
Keyword(s):  
Thermal Stress ◽  
Heat Shock ◽  
Protein Misfolding ◽  
Reproductive Organs ◽  
Heat Shock Factors ◽  
Mild Heat ◽  
Promising Therapeutic Target ◽  
Αb Crystallin ◽  
Shock Proteins ◽  
Polyglutamine Protein

Heat shock response is characterized by the induction of heat shock proteins (HSPs), which facilitate protein folding, and non-HSP proteins with diverse functions, including protein degradation, and is regulated by heat shock factors (HSFs). HSF1 is a master regulator of HSP expression during heat shock in mammals, as is HSF3 in avians. HSF2 plays roles in development of the brain and reproductive organs. However, the fundamental roles of HSF2 in vertebrate cells have not been identified. Here we find that vertebrate HSF2 is activated during heat shock in the physiological range. HSF2 deficiency reduces threshold for chicken HSF3 or mouse HSF1 activation, resulting in increased HSP expression during mild heat shock. HSF2-null cells are more sensitive to sustained mild heat shock than wild-type cells, associated with the accumulation of ubiquitylated misfolded proteins. Furthermore, loss of HSF2 function increases the accumulation of aggregated polyglutamine protein and shortens the lifespan of R6/2 Huntington's disease mice, partly through αB-crystallin expression. These results identify HSF2 as a major regulator of proteostasis capacity against febrile-range thermal stress and suggest that HSF2 could be a promising therapeutic target for protein-misfolding diseases.

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