Mitochondrial physiology and responses to elevated hydrogen sulphide in two isogenic lineages of an amphibious mangrove fish

Abstract

Hydrogen sulphide (H2S) is toxic and can act as a selective pressure on aquatic organisms facilitating a wide range of adaptations for life in sulphidic environments. Rivulus (Kryptolebias marmoratus) inhabit mangrove swamps and have developed high tolerance to environmental H2S. Rivulus are hermaphroditic and can self-fertilize, producing distinct isogenic lineages with different sensitivity to H2S. Here, we tested the hypothesis that observed differences in responses to H2S are the result of differences in mitochondrial functions. For this purpose, we performed two experimental series testing 1) the overall mitochondrial oxidizing capacities and 2) the kinetics of apparent H2S mitochondrial oxidation and inhibition in two distinct lineages of mangrove Rivulus, originally collected from Belize and Honduras. We used permeabilized livers from both lineages, measured mitochondrial oxidation, and monitored changes during gradual increases of sulphide. Ultimately, we determined that each lineage has a distinct strategy for coping with elevated H2S, indicating divergences in mitochondrial function and metabolism. The Honduras lineage has higher anaerobic capacity substantiated by higher LDH activity and higher apparent H2S oxidation rates, likely enabling them to tolerate H2S by escaping aquatic H2S in a terrestrial environment. However, Belize fish have increased cytochrome c oxidase (COX) and citrate synthase activities as well as increased succinate contribution to mitochondrial respiration, allowing them to tolerate higher levels of aquatic H2S without inhibition of mitochondrial oxygen consumption. Our study reveals distinct physiological strategies in genetic lineages of a single species indicating possible genetic and/or functional adaptations to sulphidic environments at the mitochondrial level.

Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species

“…Another example is the amino acid proline that can be used as an anaplerotic donor of electrons to complex I in some species ( Sacktor and Childress, 1967 ; Micheu et al, 2000 ; Suarez et al, 2005 ; Soares et al, 2015 ), or as a direct donor of electron to the proline dehydrogenase (ProDH) in other species ( Bursell, 1963 ; Bursell, 1981 ; Soares et al, 2015 ; Teulier et al, 2016 ; McDonald et al, 2018 ). Succinate is another oxidative substrate that can act as an electron donor to the ETS via complex II, and its importance has also recently been put forward in several organisms during challenging environmental conditions such as hypoxia/anoxia and reoxygenation stresses ( Bundgaard et al, 2018 ; Cox and Gillis, 2020 ; Martin et al, 2021 ; Adzigbli et al, 2022 ). These substrates are thus an important part of the oxidative capacity of mitochondria and must be systematically taken into account when evaluating mitochondrial thermal sensitivity.…”

Regulation of Mitochondrial Respiration by Hydrogen Sulfide

“…A low concentration of GYY4137 (a slow-releasing H 2 S donor) enhances mitochondrial oxygen consumption, ATP production, and spare respiratory capacity, induces the S -sulfhydration of Cys163 in lactate dehydrogenase, and stimulates enzyme activity [ 80 ]. Under H 2 S stress, Belize fish increase cytochrome c oxidase and citrate synthase activities to tolerate higher levels of aquatic H 2 S without inhibiting mitochondrial oxygen consumption [ 81 ]. NaHS upregulates the activities of pyruvate dehydrogenase, malate dehydrogenase, isocitrate dehydrogenase, succinyl-CoA ligase, fumarate hydratase, succinate dehydrogenase of TCA cycle in db/db mice [ 82 ].…”