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The relationship between mitochondrial respiration, resting metabolic rate and blood cell count in great tits

Thoral, Elisa LU ; Garcıá-Dıáz, Carmen C. ; Persson, Elin LU orcid ; Chamkha, Imen LU ; Elmér, Eskil LU orcid ; Ruuskanen, Suvi and Nord, Andreas LU (2024) In Biology Open 13(3).
Abstract

Although mitochondrial respiration is believed to explain a substantial part of the variation in resting metabolic rate (RMR), few studies have empirically studied the relationship between organismal and cellular metabolism. We therefore investigated the relationship between RMR and mitochondrial respiration of permeabilized blood cells in wild great tits (Parus major L.). We also studied the correlation between mitochondrial respiration traits and blood cell count, as normalizing mitochondrial respiration by the cell count is a method commonly used to study blood metabolism. In contrast to previous studies, our results show that there was no relationship between RMR and mitochondrial respiration in intact blood cells (i.e. with the... (More)

Although mitochondrial respiration is believed to explain a substantial part of the variation in resting metabolic rate (RMR), few studies have empirically studied the relationship between organismal and cellular metabolism. We therefore investigated the relationship between RMR and mitochondrial respiration of permeabilized blood cells in wild great tits (Parus major L.). We also studied the correlation between mitochondrial respiration traits and blood cell count, as normalizing mitochondrial respiration by the cell count is a method commonly used to study blood metabolism. In contrast to previous studies, our results show that there was no relationship between RMR and mitochondrial respiration in intact blood cells (i.e. with the ROUTINE respiration). However, when cells were permeabilized and interrelation re-assessed under saturating substrate availability, we found that RMR was positively related to phosphorylating respiration rates through complexes I and II (i.e. OXPHOS respiration) and to the mitochondrial efficiency to produce energy (i.e. net phosphorylation efficiency), though variation explained by the models was low (i.e. linear model: R2=0.14 to 0.21). However, unlike studies in mammals, LEAK respiration without [i.e. L(n)] and with [i.e. L(Omy)] adenylates was not significantly related to RMR. These results suggest that phosphorylating respiration in blood cells can potentially be used to predict RMR in wild birds, but that this relationship may have to be addressed in standardized conditions (permeabilized cells) and that the prediction risks being imprecise. We also showed that, in our conditions, there was no relationship between any mitochondrial respiration trait and blood cell count. Hence, we caution against normalising respiration rates using this parameter as is sometimes done. Future work should address the functional explanations for the observed relationships, and determine why these appear labile across space, time, taxon, and physiological state.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Basal metabolic rate, Erythrocyte, Great tit, Mitochondria, Oxidative metabolism, Resting metabolic rate
in
Biology Open
volume
13
issue
3
article number
bio060302
publisher
The Company of Biologists Ltd
external identifiers
  • scopus:85189696130
  • pmid:38385271
ISSN
2046-6390
DOI
10.1242/bio.060302
language
English
LU publication?
yes
id
6572ac98-d731-48ca-9e3e-7e72cafd4d92
date added to LUP
2024-04-23 15:01:53
date last changed
2024-06-18 20:04:20
@article{6572ac98-d731-48ca-9e3e-7e72cafd4d92,
  abstract     = {{<p>Although mitochondrial respiration is believed to explain a substantial part of the variation in resting metabolic rate (RMR), few studies have empirically studied the relationship between organismal and cellular metabolism. We therefore investigated the relationship between RMR and mitochondrial respiration of permeabilized blood cells in wild great tits (Parus major L.). We also studied the correlation between mitochondrial respiration traits and blood cell count, as normalizing mitochondrial respiration by the cell count is a method commonly used to study blood metabolism. In contrast to previous studies, our results show that there was no relationship between RMR and mitochondrial respiration in intact blood cells (i.e. with the ROUTINE respiration). However, when cells were permeabilized and interrelation re-assessed under saturating substrate availability, we found that RMR was positively related to phosphorylating respiration rates through complexes I and II (i.e. OXPHOS respiration) and to the mitochondrial efficiency to produce energy (i.e. net phosphorylation efficiency), though variation explained by the models was low (i.e. linear model: R<sup>2</sup>=0.14 to 0.21). However, unlike studies in mammals, LEAK respiration without [i.e. L(n)] and with [i.e. L(Omy)] adenylates was not significantly related to RMR. These results suggest that phosphorylating respiration in blood cells can potentially be used to predict RMR in wild birds, but that this relationship may have to be addressed in standardized conditions (permeabilized cells) and that the prediction risks being imprecise. We also showed that, in our conditions, there was no relationship between any mitochondrial respiration trait and blood cell count. Hence, we caution against normalising respiration rates using this parameter as is sometimes done. Future work should address the functional explanations for the observed relationships, and determine why these appear labile across space, time, taxon, and physiological state.</p>}},
  author       = {{Thoral, Elisa and Garcıá-Dıáz, Carmen C. and Persson, Elin and Chamkha, Imen and Elmér, Eskil and Ruuskanen, Suvi and Nord, Andreas}},
  issn         = {{2046-6390}},
  keywords     = {{Basal metabolic rate; Erythrocyte; Great tit; Mitochondria; Oxidative metabolism; Resting metabolic rate}},
  language     = {{eng}},
  number       = {{3}},
  publisher    = {{The Company of Biologists Ltd}},
  series       = {{Biology Open}},
  title        = {{The relationship between mitochondrial respiration, resting metabolic rate and blood cell count in great tits}},
  url          = {{http://dx.doi.org/10.1242/bio.060302}},
  doi          = {{10.1242/bio.060302}},
  volume       = {{13}},
  year         = {{2024}},
}