Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold

Gaddiel Galarza-Munoz, Sonia I. Soto-Morales, Miguel Holmgren, Joshua J.C. Rosenthal

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Because enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90%. Enzymes embedded in the plasma membrane, such as the Na +/K+-ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na+/K+-ATPase α-subunits from an Antarctic (Pareledone sp.;-1.8°C) and a temperate octopus (Octopus bimaculatus; ∼18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97% identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25% higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na+/K+ pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na+/K+-ATPase.

Original languageEnglish (US)
Pages (from-to)2164-2174
Number of pages11
JournalJournal of Experimental Biology
Volume214
Issue number13
DOIs
StatePublished - Jul 2011
Externally publishedYes

Fingerprint

Physiological Adaptation
sodium-potassium-exchanging ATPase
pumps
pump
Octopodiformes
Temperature
Octopodidae
Enzymes
enzyme
Hot Temperature
enzymes
Lipid Bilayers
Xenopus
temperature
turnover
Oocytes
lipid
heat
lipid bilayers
Cell Membrane

Keywords

  • Antarctica
  • Ion channels
  • Ion transporters
  • Na/K -ATPase
  • Octopus
  • Temperature adaptation

ASJC Scopus subject areas

  • Medicine(all)
  • Physiology
  • Ecology, Evolution, Behavior and Systematics
  • Aquatic Science
  • Molecular Biology
  • Animal Science and Zoology
  • Insect Science

Cite this

Galarza-Munoz, G., Soto-Morales, S. I., Holmgren, M., & Rosenthal, J. J. C. (2011). Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold. Journal of Experimental Biology, 214(13), 2164-2174. https://doi.org/10.1242/jeb.048744

Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold. / Galarza-Munoz, Gaddiel; Soto-Morales, Sonia I.; Holmgren, Miguel; Rosenthal, Joshua J.C.

In: Journal of Experimental Biology, Vol. 214, No. 13, 07.2011, p. 2164-2174.

Research output: Contribution to journalArticle

Galarza-Munoz, G, Soto-Morales, SI, Holmgren, M & Rosenthal, JJC 2011, 'Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold', Journal of Experimental Biology, vol. 214, no. 13, pp. 2164-2174. https://doi.org/10.1242/jeb.048744
Galarza-Munoz G, Soto-Morales SI, Holmgren M, Rosenthal JJC. Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold. Journal of Experimental Biology. 2011 Jul;214(13):2164-2174. https://doi.org/10.1242/jeb.048744
Galarza-Munoz, Gaddiel ; Soto-Morales, Sonia I. ; Holmgren, Miguel ; Rosenthal, Joshua J.C. / Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold. In: Journal of Experimental Biology. 2011 ; Vol. 214, No. 13. pp. 2164-2174.
@article{a1c0703c0610404897e1827cf3d5b846,
title = "Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold",
abstract = "Because enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90{\%}. Enzymes embedded in the plasma membrane, such as the Na +/K+-ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na+/K+-ATPase α-subunits from an Antarctic (Pareledone sp.;-1.8°C) and a temperate octopus (Octopus bimaculatus; ∼18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97{\%} identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25{\%} higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na+/K+ pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na+/K+-ATPase.",
keywords = "Antarctica, Ion channels, Ion transporters, Na/K -ATPase, Octopus, Temperature adaptation",
author = "Gaddiel Galarza-Munoz and Soto-Morales, {Sonia I.} and Miguel Holmgren and Rosenthal, {Joshua J.C.}",
year = "2011",
month = "7",
doi = "10.1242/jeb.048744",
language = "English (US)",
volume = "214",
pages = "2164--2174",
journal = "Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists Ltd",
number = "13",

}

TY - JOUR

T1 - Physiological adaptation of an Antarctic Na+/K +-ATPase to the cold

AU - Galarza-Munoz, Gaddiel

AU - Soto-Morales, Sonia I.

AU - Holmgren, Miguel

AU - Rosenthal, Joshua J.C.

PY - 2011/7

Y1 - 2011/7

N2 - Because enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90%. Enzymes embedded in the plasma membrane, such as the Na +/K+-ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na+/K+-ATPase α-subunits from an Antarctic (Pareledone sp.;-1.8°C) and a temperate octopus (Octopus bimaculatus; ∼18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97% identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25% higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na+/K+ pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na+/K+-ATPase.

AB - Because enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90%. Enzymes embedded in the plasma membrane, such as the Na +/K+-ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na+/K+-ATPase α-subunits from an Antarctic (Pareledone sp.;-1.8°C) and a temperate octopus (Octopus bimaculatus; ∼18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97% identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25% higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na+/K+ pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na+/K+-ATPase.

KW - Antarctica

KW - Ion channels

KW - Ion transporters

KW - Na/K -ATPase

KW - Octopus

KW - Temperature adaptation

UR - http://www.scopus.com/inward/record.url?scp=79958795001&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79958795001&partnerID=8YFLogxK

U2 - 10.1242/jeb.048744

DO - 10.1242/jeb.048744

M3 - Article

C2 - 21653810

AN - SCOPUS:79958795001

VL - 214

SP - 2164

EP - 2174

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 13

ER -