High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

Jakob Michaelsen; Angela Fago; Amanda Bundgaard

doi:10.1242/jeb.242382

High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

Jakob Michaelsen, Angela Fago, Amanda Bundgaard^*

^*Corresponding author af dette arbejde

Institut for Biologi - Zoofysiologi

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

26 Citationer (Scopus)

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Abstract

Mitochondria provide cellular energy through oxidative phosphorylation, and thus temperature-induced constraints on mitochondrial function may be crucial to animal aerobic scope and thermal tolerance. Here, we report the effect of temperature in the range 5-30 degrees C on respiration rates of isolated cardiac mitochondria from rainbow trout (Oncorhynchus mykiss) studied by high-resolution respirometry and spectrophotometric enzyme activity assays. Arrhenius breakpoint temperature analysis indicated that mitochondrial respiration rates under phosphorylating and fully uncoupled conditions increased exponentially up to 20 degrees C, but stopped increasing at higher temperatures. In contrast, respiration rates measured under non-phosphorylating leak conditions continued to increase up to 30 degrees C. The decrease in the ratio between phosphorylating and uncoupled respiration at high temperature indicated that phosphorylation was gradually impaired with increasing temperature, possibly because of the steadily increasing proton leak across the membrane. In addition, we found that complex I (NADH dehydrogenase) activity decreased above 20 degrees C, similarly to mitochondrial respiration, and that complex I was unstable in the presence of detergents, suggesting that it may be particularly sensitive to changes in its interaction with membrane phospholipids. In contrast, complex II (succinate dehydrogenase) maintained activity at temperatures above 20 degrees C, although succinate oxidation was insufficient to compensate for the loss of complex I activity in intact mitochondria. Together, these results indicate that the temperature-induced decrease in cardiac mitochondrial function coincides with the temperature at which trout aerobic scope peaks, and is largely due to impaired phosphorylation and complex I activity.

Originalsprog	Engelsk
Artikelnummer	jeb242382
Tidsskrift	Journal of Experimental Biology
Vol/bind	224
Nummer	9
Antal sider	7
ISSN	0022-0949
DOI	https://doi.org/10.1242/jeb.242382
Status	Udgivet - maj 2021

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10.1242/jeb.242382

High temperature impairs mitochondrial function in rainbow trout cardiac mitochondriaForlagets udgivne version, 1,08 MBLicens: Andet

Citationsformater

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title = "High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria",

abstract = "Mitochondria provide cellular energy through oxidative phosphorylation, and thus temperature-induced constraints on mitochondrial function may be crucial to animal aerobic scope and thermal tolerance. Here, we report the effect of temperature in the range 5-30 degrees C on respiration rates of isolated cardiac mitochondria from rainbow trout (Oncorhynchus mykiss) studied by high-resolution respirometry and spectrophotometric enzyme activity assays. Arrhenius breakpoint temperature analysis indicated that mitochondrial respiration rates under phosphorylating and fully uncoupled conditions increased exponentially up to 20 degrees C, but stopped increasing at higher temperatures. In contrast, respiration rates measured under non-phosphorylating leak conditions continued to increase up to 30 degrees C. The decrease in the ratio between phosphorylating and uncoupled respiration at high temperature indicated that phosphorylation was gradually impaired with increasing temperature, possibly because of the steadily increasing proton leak across the membrane. In addition, we found that complex I (NADH dehydrogenase) activity decreased above 20 degrees C, similarly to mitochondrial respiration, and that complex I was unstable in the presence of detergents, suggesting that it may be particularly sensitive to changes in its interaction with membrane phospholipids. In contrast, complex II (succinate dehydrogenase) maintained activity at temperatures above 20 degrees C, although succinate oxidation was insufficient to compensate for the loss of complex I activity in intact mitochondria. Together, these results indicate that the temperature-induced decrease in cardiac mitochondrial function coincides with the temperature at which trout aerobic scope peaks, and is largely due to impaired phosphorylation and complex I activity.",

keywords = "Complex I, Fish, Heart, Mitochondria, Respiration, Temperature, THERMAL TOLERANCE, OXIDATIVE CAPACITIES, ONCORHYNCHUS-MYKISS, HEART-MITOCHONDRIA, SENSITIVITY, PHOSPHOLIPIDS, ACCLIMATION, RESPIRATION, MECHANISM, EVOLUTION",

author = "Jakob Michaelsen and Angela Fago and Amanda Bundgaard",

note = "Publisher Copyright: {\textcopyright} 2021. Published by The Company of Biologists Ltd.",

year = "2021",

month = may,

doi = "10.1242/jeb.242382",

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journal = "Journal of Experimental Biology",

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T1 - High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

AU - Michaelsen, Jakob

AU - Fago, Angela

AU - Bundgaard, Amanda

PY - 2021/5

Y1 - 2021/5

N2 - Mitochondria provide cellular energy through oxidative phosphorylation, and thus temperature-induced constraints on mitochondrial function may be crucial to animal aerobic scope and thermal tolerance. Here, we report the effect of temperature in the range 5-30 degrees C on respiration rates of isolated cardiac mitochondria from rainbow trout (Oncorhynchus mykiss) studied by high-resolution respirometry and spectrophotometric enzyme activity assays. Arrhenius breakpoint temperature analysis indicated that mitochondrial respiration rates under phosphorylating and fully uncoupled conditions increased exponentially up to 20 degrees C, but stopped increasing at higher temperatures. In contrast, respiration rates measured under non-phosphorylating leak conditions continued to increase up to 30 degrees C. The decrease in the ratio between phosphorylating and uncoupled respiration at high temperature indicated that phosphorylation was gradually impaired with increasing temperature, possibly because of the steadily increasing proton leak across the membrane. In addition, we found that complex I (NADH dehydrogenase) activity decreased above 20 degrees C, similarly to mitochondrial respiration, and that complex I was unstable in the presence of detergents, suggesting that it may be particularly sensitive to changes in its interaction with membrane phospholipids. In contrast, complex II (succinate dehydrogenase) maintained activity at temperatures above 20 degrees C, although succinate oxidation was insufficient to compensate for the loss of complex I activity in intact mitochondria. Together, these results indicate that the temperature-induced decrease in cardiac mitochondrial function coincides with the temperature at which trout aerobic scope peaks, and is largely due to impaired phosphorylation and complex I activity.

AB - Mitochondria provide cellular energy through oxidative phosphorylation, and thus temperature-induced constraints on mitochondrial function may be crucial to animal aerobic scope and thermal tolerance. Here, we report the effect of temperature in the range 5-30 degrees C on respiration rates of isolated cardiac mitochondria from rainbow trout (Oncorhynchus mykiss) studied by high-resolution respirometry and spectrophotometric enzyme activity assays. Arrhenius breakpoint temperature analysis indicated that mitochondrial respiration rates under phosphorylating and fully uncoupled conditions increased exponentially up to 20 degrees C, but stopped increasing at higher temperatures. In contrast, respiration rates measured under non-phosphorylating leak conditions continued to increase up to 30 degrees C. The decrease in the ratio between phosphorylating and uncoupled respiration at high temperature indicated that phosphorylation was gradually impaired with increasing temperature, possibly because of the steadily increasing proton leak across the membrane. In addition, we found that complex I (NADH dehydrogenase) activity decreased above 20 degrees C, similarly to mitochondrial respiration, and that complex I was unstable in the presence of detergents, suggesting that it may be particularly sensitive to changes in its interaction with membrane phospholipids. In contrast, complex II (succinate dehydrogenase) maintained activity at temperatures above 20 degrees C, although succinate oxidation was insufficient to compensate for the loss of complex I activity in intact mitochondria. Together, these results indicate that the temperature-induced decrease in cardiac mitochondrial function coincides with the temperature at which trout aerobic scope peaks, and is largely due to impaired phosphorylation and complex I activity.

KW - Complex I

KW - Fish

KW - Heart

KW - Mitochondria

KW - Respiration

KW - Temperature

KW - THERMAL TOLERANCE

KW - OXIDATIVE CAPACITIES

KW - ONCORHYNCHUS-MYKISS

KW - HEART-MITOCHONDRIA

KW - SENSITIVITY

KW - PHOSPHOLIPIDS

KW - ACCLIMATION

KW - RESPIRATION

KW - MECHANISM

KW - EVOLUTION

U2 - 10.1242/jeb.242382

DO - 10.1242/jeb.242382

M3 - Journal article

C2 - 33758025

SN - 0022-0949

VL - 224

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

IS - 9

M1 - jeb242382

ER -

High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

Abstract

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