Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

Karine Salin, Eugenia M. Villasevil, Graeme J. Anderson, Sonya K. Auer, Colin Selman, Richard C. Hartley, William Mullen, C. Chinopoulos, Neil B. Metcalfe

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally-occurring periods of food deprivation may have long-term negative impacts on their subsequent life-history. In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade-off since studies of energy metabolism are generally conducted separately from those of oxidative stress. Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS). After a 2-week period of fasting, brown trout reduced their whole-liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two-fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe). The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade-off between the short-term energetic benefits of reducing metabolism in response to fasting and the potential long-term costs to subsequent life-history traits.

Original languageEnglish
JournalFunctional Ecology
DOIs
Publication statusAccepted/In press - Jan 1 2018

Fingerprint

fasting
Salmo trutta
liver
animal
cost
trade-off
breathing
reactive oxygen species
animals
respiration
oxidative stress
metabolism
life history
energy
food shortages
food
food deprivation
mitochondrion
life history trait
energy requirements

Keywords

  • High-resolution respirometry
  • In vivo
  • Liver atrophy
  • MitoB probe
  • Mitochondrial respiratory state

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

Salin, K., Villasevil, E. M., Anderson, G. J., Auer, S. K., Selman, C., Hartley, R. C., ... Metcalfe, N. B. (Accepted/In press). Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost. Functional Ecology. https://doi.org/10.1111/1365-2435.13125

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost. / Salin, Karine; Villasevil, Eugenia M.; Anderson, Graeme J.; Auer, Sonya K.; Selman, Colin; Hartley, Richard C.; Mullen, William; Chinopoulos, C.; Metcalfe, Neil B.

In: Functional Ecology, 01.01.2018.

Research output: Contribution to journalArticle

Salin, K, Villasevil, EM, Anderson, GJ, Auer, SK, Selman, C, Hartley, RC, Mullen, W, Chinopoulos, C & Metcalfe, NB 2018, 'Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost', Functional Ecology. https://doi.org/10.1111/1365-2435.13125
Salin, Karine ; Villasevil, Eugenia M. ; Anderson, Graeme J. ; Auer, Sonya K. ; Selman, Colin ; Hartley, Richard C. ; Mullen, William ; Chinopoulos, C. ; Metcalfe, Neil B. / Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost. In: Functional Ecology. 2018.
@article{d7311883d106491fb15b62bc26997c3d,
title = "Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost",
abstract = "Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally-occurring periods of food deprivation may have long-term negative impacts on their subsequent life-history. In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade-off since studies of energy metabolism are generally conducted separately from those of oxidative stress. Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS). After a 2-week period of fasting, brown trout reduced their whole-liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two-fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe). The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade-off between the short-term energetic benefits of reducing metabolism in response to fasting and the potential long-term costs to subsequent life-history traits.",
keywords = "High-resolution respirometry, In vivo, Liver atrophy, MitoB probe, Mitochondrial respiratory state",
author = "Karine Salin and Villasevil, {Eugenia M.} and Anderson, {Graeme J.} and Auer, {Sonya K.} and Colin Selman and Hartley, {Richard C.} and William Mullen and C. Chinopoulos and Metcalfe, {Neil B.}",
year = "2018",
month = "1",
day = "1",
doi = "10.1111/1365-2435.13125",
language = "English",
journal = "Functional Ecology",
issn = "0269-8463",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

AU - Salin, Karine

AU - Villasevil, Eugenia M.

AU - Anderson, Graeme J.

AU - Auer, Sonya K.

AU - Selman, Colin

AU - Hartley, Richard C.

AU - Mullen, William

AU - Chinopoulos, C.

AU - Metcalfe, Neil B.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally-occurring periods of food deprivation may have long-term negative impacts on their subsequent life-history. In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade-off since studies of energy metabolism are generally conducted separately from those of oxidative stress. Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS). After a 2-week period of fasting, brown trout reduced their whole-liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two-fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe). The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade-off between the short-term energetic benefits of reducing metabolism in response to fasting and the potential long-term costs to subsequent life-history traits.

AB - Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally-occurring periods of food deprivation may have long-term negative impacts on their subsequent life-history. In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade-off since studies of energy metabolism are generally conducted separately from those of oxidative stress. Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS). After a 2-week period of fasting, brown trout reduced their whole-liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two-fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe). The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade-off between the short-term energetic benefits of reducing metabolism in response to fasting and the potential long-term costs to subsequent life-history traits.

KW - High-resolution respirometry

KW - In vivo

KW - Liver atrophy

KW - MitoB probe

KW - Mitochondrial respiratory state

UR - http://www.scopus.com/inward/record.url?scp=85047664339&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85047664339&partnerID=8YFLogxK

U2 - 10.1111/1365-2435.13125

DO - 10.1111/1365-2435.13125

M3 - Article

AN - SCOPUS:85047664339

JO - Functional Ecology

JF - Functional Ecology

SN - 0269-8463

ER -