The relationship between membrane fatty acid content and mitochondrial efficiency differs within- and between- omega-3 dietary treatments

Type Article
Date 2021-01
Language English
Author(s) Salin KarineORCID1, Mathieu-Resuge Margaux2, Graziano Nicolas1, 3, Dubillot Emmanuel3, Le Grand Fabienne1, Soudant Philippe1, Vagner Marie1, 3
Affiliation(s) 1 : Univ Brest, Ifremer, CNRS, IRD, LEMAR, F-29280, Plouzané, France
2 : WasserCluster Lunz — Inter-University Centre for Aquatic Ecosystem Research, Dr. Carl Kupelwieser Promenade 5 A-3293 Lunz Am See, Austria
3 : UMR 7266 LIENSs, 2 Rue Olympe de Gouges 17000 La Rochelle, France
4 : Univ Brest, Ifremer, CNRS, IRD, LEMAR, F-29280, Plouzané, France
Source Marine Environmental Research (0141-1136) (Elsevier BV), 2021-01 , Vol. 163 , P. 105205 (8p.)
DOI 10.1016/j.marenvres.2020.105205
WOS© Times Cited 4
Keyword(s) ATP/O ratio, Docosahexaenoic acid (DHA), Eicosapentaenoic acid (EPA), Food quality, Chelon auratus, Global change
Abstract

An important, but underappreciated, consequence of climate change is the reduction in crucial nutrient production at the base of the marine food chain: the long-chain omega-3 highly unsaturated fatty acids (n-3 HUFA). This can have dramatic consequences on consumers, such as fish as they have limited capacity to synthesise n-3 HUFA de novo. The n-3 HUFA, such as docosahexaenoic acid (DHA, 22:6n-3) and eicosapentaenoic acid (EPA, 20:5n-3), are critical for the structure and function of all biological membranes. There is increasing evidence that fish will be badly affected by reductions in n-3 HUFA dietary availability, however the underlying mechanisms remain obscure. Hypotheses for how mitochondrial function should change with dietary n-3 HUFA availability have generally ignored ATP production, despite its importance to a cell's total energetics capacity, and in turn, whole-animal performance. Here we (i) quantified individual variation in mitochondrial efficiency (ATP/O ratio) of muscle and (ii) examined its relationship with content in EPA and DHA in muscle membrane of a primary consumer fish, the golden grey mullet Chelon auratus, receiving either a high or low n-3 HUFA diet. Mitochondria of fish fed on the low n-3 HUFA diet had higher ATP/O ratio than those of fish maintained on the high n-3 HUFA diet. Yet, mitochondrial efficiency varied up about 2-fold among individuals on the same dietary treatment, resulting in some fish consuming half the oxygen and energy substrate to produce the similar amount of ATP than conspecific on similar diet. This variation in mitochondrial efficiency among individuals from the same diet treatment was related to individual differences in fatty acid composition of the membranes: a high ATP/O ratio was associated with a high content in EPA and DHA in biological membranes. Our results highlight the existence of interindividual differences in mitochondrial efficiency and its potential importance in explaining intraspecific variation in response to food chain changes.

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Salin Karine, Mathieu-Resuge Margaux, Graziano Nicolas, Dubillot Emmanuel, Le Grand Fabienne, Soudant Philippe, Vagner Marie (2021). The relationship between membrane fatty acid content and mitochondrial efficiency differs within- and between- omega-3 dietary treatments. Marine Environmental Research, 163, 105205 (8p.). Publisher's official version : https://doi.org/10.1016/j.marenvres.2020.105205 , Open Access version : https://archimer.ifremer.fr/doc/00658/77013/