Osmoregulatory capacity at low temperature is critical for insect cold tolerance

Overgaard, Johannes; Gerber, Lucie; Andersen, Mads Kuhlmann

doi:10.1016/j.cois.2021.02.015

Cited by 48 publications

(42 citation statements)

References 81 publications

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“…Considering the central role of the Na + /K + -ATPase in regulating extracellular ion homeostasis in the insect central nervous system it is perhaps not surprising that its activity is essential for preventing SD when exposed to stressful cold. Nonetheless, our findings support a key role of the Na + /K + -ATPase in modulating SD susceptibility, and adaptations promoting maintained active ion transport capacity therefore appear to be a key pathway by which cold tolerance can be improved at multiple levels of biological organization (see Overgaard et al (2021)). The molecular and/or cellular mechanism by which the Na + /K + -ATPase of cold-acclimated flies is able to maintain activity at low temperature remains unknown, but we suggest that future research should focus on investigating the roles of phosphorylation, transcript expression, sequence variation, cellular localization, and the membrane environment.…”

Section: Discussionsupporting

confidence: 54%

“…Cold-induced SD and chill coma are plastic traits that can vary greatly. This is also true for Drosophila, where the chill coma and SD temperatures cover a range of more than 10°C among species (Mellanby, 1954;Kellermann et al, 2012;Andersen et al, 2015b;MacMillan et al, 2015b) and by several degrees within a species depending on thermal history (Kelty and Lee Jr, 1999;Overgaard et al, 2011;Ransberry et al, 2011;Armstrong et al, 2012;MacMillan et al, 2015a;Schou et al, 2017;Andersen et al, 2018). This makes drosophilids, such as Drosophila melanogaster, excellent model systems for studying the physiological mechanisms underlying variation in cold tolerance.…”

Section: Introductionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted September 3, 2022. ; https://doi.org/10. 1101 this clade to make great progress in describing the processes that underlie improved organismal cold tolerance (see reviews by Overgaard and MacMillan (2017) and Overgaard et al (2021)).…”

Section: Introductionmentioning

confidence: 99%

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Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Andersen

Robertson

MacMillan

2022

Preprint

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The majority of insects can acclimate to changes in their thermal environment and counteract temperature effects on neuromuscular function. At the critical thermal minimum a spreading depolarization (SD) event silences central neurons, but the temperature at which this event occurs can be altered through acclimation. SD is triggered by an inability to maintain ion homeostasis in the extracellular space in the brain and is characterized by a rapid surge in extracellular K+ concentration, implicating ion pump and channel function. Here, we focused on the role of the Na+/K+-ATPase specifically in lowering the SD temperature in cold-acclimated Drosophila melanogaster. After first confirming cold acclimation altered SD onset, we investigated the dependency of the SD event on Na+/K+-ATPase activity by injecting an inhibitor, ouabain, into the head of the flies to induce SD over a range of temperatures. Latency to SD followed the pattern of a thermal performance curve, but cold acclimation resulted in a left-shift of the curve to an extent similar to its effect on the SD temperature. With Na+/K+-ATPase activity assays and immunoblots, we found that cold-acclimated flies have ion pumps that are less sensitive to temperature, but do not differ in their overall abundance in the brain. Combined, these findings suggest a key role for plasticity in Na+/K+-ATPase thermal sensitivity in maintaining central nervous system function in the cold, and more broadly highlight that a single ion pump can be an important determinant of whether insects can respond to their environment to remain active at low temperatures.

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Section: Discussionsupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

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Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Andersen

Robertson

MacMillan

2022

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“…The combination of cold and hyperkalemia leads to loss of membrane polarization which triggers calcium influx into cells, activating signaling pathways that initiate cell death (MacMillan et al 2015c; Bayley et al 2018; Carrington et al 2020). The increasingly well-resolved physiological basis of chilling injury (see for example (Overgaard et al 2021)) makes it possible to test both the extent of plastic and evolved changes and also to determine whether any changes in complex phenotypes have similar physiological underpinnings.…”

Section: Introductionmentioning

confidence: 99%

Elemental stoichiometry and insect chill tolerance: Evolved and plastic changes in organismal Na⁺ and K⁺ content in Drosophila

Chalmer

Rudman

Andersen

et al. 2022

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Acclimation and evolutionary adaptation can produce phenotypic change that allows organisms to cope with challenges like those associated with climate change. Determining the relative contributions of acclimation and adaptation is of central importance to understanding animal responses to change. Rates of evolution have traditionally been considered slow relative to ecological processes that shape biodiversity. Many organisms nonetheless show patterns of spatial genetic variation suggestive of adaptation and some evidence is emerging that adaptation can act sufficiently fast to allow phenotypic tracking in response to environmental change (adaptive tracking). In Drosophila, both plastic and evolved differences in chill tolerance are associated with ionoregulation. Here we combine acclimation, latitudinal field collections, and a replicated field experiment to assess the effects of acclimation and adaptation on chill coma recovery and elemental (Na and K) stoichiometry in both sexes of Drosophila melanogaster. Acclimation and spatial adaptation both shape chill coma recovery, with acclimation producing the greatest magnitude response. Leveraging knowledge on the physiological mechanisms that underlie variation in chill tolerance traits, we find that the relationship between K content and chill tolerance differs among flies acclimated vs. adapted to cold. Taken together, these data reinforce the importance of acclimation in responses to abiotic challenges and illustrate that the mechanisms of phenotypic change can differ between acclimation and basal tolerance adaptation.

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“…Low temperatures are detrimental to a chill-susceptible insect, in part, because they slow the rate of active ion transport in the gut and Malpighian tubules. As a cold exposure continues, active transport rates pass a critical threshold where they cannot counterbalance the passive leak of solutes and water (Overgaard et al, 2021). Ion and water homeostasis then become disrupted when a net leak of Na + and water into the gut lumen occurs, reducing hemolymph volume (MacMillan and Sinclair, 2011b).…”

Section: The Insect Gut and Malpighian Tubulesmentioning

confidence: 99%

Investigating a Link Between Cold Stress and Bacterial Leak from the Gut of Locusta Migratoria

El-Saadi¹

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Following prolonged low temperature exposure, chill-susceptible insects can incur chilling injuries that manifest as motor deficits and tissue damage. This tissue damage is thought to be driven by a loss of ion and water homeostasis, characterized by elevated potassium concentration in the hemolymph (hyperkalemia). The insect gut plays a major role in the maintenance of ion and water balance, and gut epithelial barrier function is compromised during chilling, which can contribute to the leak of water and solutes across the gut wall. The insect gut also houses an abundant bacterial population which can contribute to the host's cold tolerance. In recent years, however, a growing number of studies have reported increased activation of the insect immune system following a cold stress, suggesting that cold stress may cause bacterial infection. For my research, I hypothesized that prolonged cold stresses result in the leak of bacteria from the gut into the surrounding hemolymph as a possible explanation for the immune activation. With locusts as my model insect, I used an E. coli strain that expresses a fluorescent marker (GFPmut3) to track bacterial leak from the gut. After a period of feeding on wheat that was soaked in a concentrated solution of the bacteria, locusts were exposed to -2°C for varying lengths of time before hemolymph was extracted and plated on agar media to facilitate bacterial colony growth. Surprisingly, I found no evidence of bacterial leak as no colonies were observed regardless of cold exposure length. My research strongly suggests that gut barrier integrity is well maintained even after severe cold stresses and is sufficient enough to prevent the leak of whole bacteria across the gut wall, which opens up other possible explanations as to why immune activation occurs following cold exposures in insects.iii AcknowledgementsMy graduate school experience here at Carleton was a very fulfilling and enriching one.The people I've met, the opportunities I've been given, and the lessons I've learned may be innumerable, but they all mean a great deal to me.Thank you, Heath, for all your support and mentorship over the past four years, especially through a pandemic! A large part of my growth as a scientist has been, in large part, because of you going above and beyond for us. From publishing a paper to attending conferences, I can definitely say that I've become a lot better at communicating research to others and, more importantly, become even better at thinking independently as a researcher. I can certainly look back now and see how far I've come, so thank you once more. I'd also like to extend this thanks to Jeff Dawson. Thank you for your monumental help and support at the beginning of my MSc.

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Osmoregulatory capacity at low temperature is critical for insect cold tolerance

Cited by 48 publications

References 81 publications

Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Elemental stoichiometry and insect chill tolerance: Evolved and plastic changes in organismal Na⁺ and K⁺ content in Drosophila

Investigating a Link Between Cold Stress and Bacterial Leak from the Gut of Locusta Migratoria

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Osmoregulatory capacity at low temperature is critical for insect cold tolerance

Cited by 48 publications

References 81 publications

Plasticity in Na+/K+-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Plasticity in Na+/K+-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Elemental stoichiometry and insect chill tolerance: Evolved and plastic changes in organismal Na+ and K+ content in Drosophila

Investigating a Link Between Cold Stress and Bacterial Leak from the Gut of Locusta Migratoria

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Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Plasticity in Na⁺/K⁺-ATPase thermal kinetics drives variation in the critical thermal minimum of adult Drosophila melanogaster

Elemental stoichiometry and insect chill tolerance: Evolved and plastic changes in organismal Na⁺ and K⁺ content in Drosophila