Divergences in the Control of Mitochondrial Respiration Are Associated With Life-Span Variation in Marine Bivalves

Abstract

The role played by mitochondrial function in the aging process has been a subject of intense debate in the past few decades, as part of the efforts to understand the mechanistic basis of longevity. The mitochondrial oxidative stress theory of aging (MOSTA) suggests that a progressive decay of this organelle’s function leads to an exacerbation of oxidative stress, with deleterious impact on mitochondrial structure and DNA, ultimately promoting aging. Among the traits suspected to be associated with longevity is the variation in regulation of oxidative phosphorylation, potentially impacting the management of oxidative stress. Longitudinal studies using the framework of metabolic control analysis have shown age-related differences in flux control of respiration, but this approach has seldom been taken on a comparative scale. Using four species of marine bivalves exhibiting a large range of maximum lifespans (from 28y to 507y), we report lifespan-related differences in flux control at different steps of the electron transfer system. Increased longevity was characterized by a lower control by NADH- (complex I-linked) and Succinate- (complex II- linked) pathways, while respiration was strongly controlled by complex IV when compared to shorter-lived species. Complex III exterted a strong control over respiration in all species. Furthermore, high longevity was associated with higher citrate synthase activity, and lower ATP synthase activity. Relieving the control exerted by the electron entry pathways could be advantageous for reaching a higher longevity, leading to an increased control by complex IV, the final electron acceptor in the electron transfer system.

The longest-lived metazoan, Arctica islandica, exhibits high mitochondrial H2O2 removal capacities

“…In the gills, RCR values were 1.66 (±0.29) for M.A., 1.62 (±0.23) for S.S, and 2.24 (±0.16) for A.I. The values following addition of cytochrome c during NADH-OXPHOS respiration for the three species studied, ranged from 11 to 20%, mirroring our previous results [11,18] and were not suggestive that mitochondria were adversely damaged during isolation.…”

“…They were fed a live microalgal diet (Nannochloropsis sp., Isochrysis galbana, Pavlova lutheri; 12% to 44% to 44% in cell numbers) at 1% body mass per day. Following our previous studies on these species, sexually mature adult individuals within the same narrow range of shell sizes were selected for the current experiment: all were estimated to be at or close to their middle age [11,17,18]. The average size (shell length) of individuals was 109 mm ± 4 for A.I., 66 mm ± 3 for M.A.…”

Mitonuclear Interactions Produce Diverging Responses to Mild Stress in Drosophila Larvae

“…In COX larvae, the single SN P difference in the COXII subunit of complex IV has been shown to slow electron transfer at higher temperatures, when metabolic demands are greater ( Patel et al, 2016 ). CIV passes on its electrons directly to oxygen, so it is not surprising that it exerts significant control over the overall rates of electron flow ( Rodriguez et al, 2021 ). While the maximal rates of both coupled and uncoupled respiration were similar in COX larvae and the other fly lines ( Figure 2B )—as well as complex IV activity itself ( Figure 3C )—the shift in substrate usage and respiratory architecture plainly drove reductive stress when subjected to mild redox stress from NAC.…”

High resolution respirometry of isolated mitochondria from adult Octopus maya (Class: Cephalopoda) systemic heart

“…Mitochondrial research has benefited from the availability of organelle preparations isolated from tissues, specifically those procedures to isolate mitochondria based on differential centrifugation [ 19 ], which allows separating cell constituents based on their different sedimentation characteristics after mechanical tissue homogenization [ 2 ]. Once isolated, the functionality of the mitochondria can be studied by adding different reagents or inhibitors that enhance or inhibit, step by step, the processes involved in mitochondrial respiration [ 20 , 21 ].…”

“…Despite the great progress in the development of mitochondrial isolation protocols in various tissues, vertebrates are the main animal model due to the interest in the mitochondrial physiology of various pathologies, even fish have been used as research models in neurodegenerative diseases such as Parkinson's [28,29]. Many other studies have been conducted in recent years to assess the relationship between mitochondrial energy production and environmental stressors in marine invertebrates to predict and understand how environmental changes affect performance and abundance in marine ecosystems and how mitochondrial adaptation may allow animals to live longer [20,21,[30][31][32][33].…”