The cell origin of reactive oxygen species and its implication for evolutionary trade-offs

The allocation of resources in animals is shaped by adaptive trade-offs aimed at maximizing fitness. At the heart of these trade-offs, lies metabolism and the conversion of food resources into energy, a process mostly occurring in mitochondria. Yet, the conversion of nutrients to utilizable energy m...

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Main Authors: Maïly Kervella, Fabrice Bertile, Frédéric Bouillaud, François Criscuolo
Format: Article
Language:English
Published: The Royal Society 2025-04-01
Series:Open Biology
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Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.240312
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author Maïly Kervella
Fabrice Bertile
Frédéric Bouillaud
François Criscuolo
author_facet Maïly Kervella
Fabrice Bertile
Frédéric Bouillaud
François Criscuolo
author_sort Maïly Kervella
collection DOAJ
description The allocation of resources in animals is shaped by adaptive trade-offs aimed at maximizing fitness. At the heart of these trade-offs, lies metabolism and the conversion of food resources into energy, a process mostly occurring in mitochondria. Yet, the conversion of nutrients to utilizable energy molecules (adenosine triphosphate) inevitably leads to the by-production of reactive oxygen species (ROS) that may cause damage to important biomolecules such as proteins or lipids. The ‘ROS theory of ageing’ has thus proposed that the relationship between lifespan and metabolic rate may be mediated by ROS production. However, the relationship is not as straightforward as it may seem: not only are mitochondrial ROS crucial for various cellular functions, but mitochondria are also actually equipped with antioxidant systems, and many extra-mitochondrial sources also produce ROS. In this review, we discuss how viewing the mitochondrion as a regulator of cellular oxidative homeostasis, not merely a ROS producer, may provide new insights into the role of oxidative stress in the reproduction–survival trade-off. We suggest several avenues to test how mitochondrial oxidative buffering capacity might complement current bioenergetic and evolutionary studies.
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spelling doaj-art-e1496f69f8fe42a18c1b9fcca99cf14c2025-08-20T02:11:38ZengThe Royal SocietyOpen Biology2046-24412025-04-0115410.1098/rsob.240312The cell origin of reactive oxygen species and its implication for evolutionary trade-offsMaïly Kervella0Fabrice Bertile1Frédéric Bouillaud2François Criscuolo3EPE, IPHC, Strasbourg, Grand Est, FranceEPE, IPHC, Strasbourg, Grand Est, FranceInstitut Cochin Département EMD, Paris, Île-de-France, FranceEPE, IPHC, Strasbourg, Grand Est, FranceThe allocation of resources in animals is shaped by adaptive trade-offs aimed at maximizing fitness. At the heart of these trade-offs, lies metabolism and the conversion of food resources into energy, a process mostly occurring in mitochondria. Yet, the conversion of nutrients to utilizable energy molecules (adenosine triphosphate) inevitably leads to the by-production of reactive oxygen species (ROS) that may cause damage to important biomolecules such as proteins or lipids. The ‘ROS theory of ageing’ has thus proposed that the relationship between lifespan and metabolic rate may be mediated by ROS production. However, the relationship is not as straightforward as it may seem: not only are mitochondrial ROS crucial for various cellular functions, but mitochondria are also actually equipped with antioxidant systems, and many extra-mitochondrial sources also produce ROS. In this review, we discuss how viewing the mitochondrion as a regulator of cellular oxidative homeostasis, not merely a ROS producer, may provide new insights into the role of oxidative stress in the reproduction–survival trade-off. We suggest several avenues to test how mitochondrial oxidative buffering capacity might complement current bioenergetic and evolutionary studies.https://royalsocietypublishing.org/doi/10.1098/rsob.240312ageing theorybioenergeticslongevityoxidative metabolismoxidative stress
spellingShingle Maïly Kervella
Fabrice Bertile
Frédéric Bouillaud
François Criscuolo
The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
Open Biology
ageing theory
bioenergetics
longevity
oxidative metabolism
oxidative stress
title The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
title_full The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
title_fullStr The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
title_full_unstemmed The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
title_short The cell origin of reactive oxygen species and its implication for evolutionary trade-offs
title_sort cell origin of reactive oxygen species and its implication for evolutionary trade offs
topic ageing theory
bioenergetics
longevity
oxidative metabolism
oxidative stress
url https://royalsocietypublishing.org/doi/10.1098/rsob.240312
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