Mitochondrial plasticity in response to changing abiotic factors in Antarctic fish and cephalopods

Antarctic species possess very low metabolic rates and poor capacities to change their physiological state, thus making them extremely vulnerable to changing environmental conditions. Mitochondria are a key element in shaping whole organism energy turnover and functional capacity. In my study, the effects of rising temperature and increased seawater PCO2 on the energy metabolism were compared between various nototheniids from sub-Antarctic and cold-temperate and Antarctic waters, and between cephalopods from the Antarctic and temperate latitudes. I determined extra- and intracellular blood carbonate parameters, enzymatic capacities and oxygen consumption at whole animal and mitochondrial level and mitochondrial lipid composition and proton leak as a measure for routine metabolic rate, in order to compare their abilities for metabolic compensation towards climate change. My results showed limited aerobic capacities of high-Antarctic fish mitochondria towards the warmth and higher CO2-levels. The mitochondrial responses of cephalopods to an acute temperature rise suggest that they possess similar mitochondrial flexibilities and capacities towards the warmth as fish. Nevertheless, generally more effective capacities for acid-base regulation and larger energy reserves (lipids) in fish compared to cephalopods will putatively make them win the competition for resources over longer time-scales, when seawater temperatures and PCO2 continue to rise

Influence of Temperature, Hypercapnia, and Development on the Relative Expression of Different Hemocyanin Isoforms in the Common Cuttlefish Sepia officinalis

The cuttlefish Sepia officinalis expresses several hemocyanin isoforms with potentially different pH optima, indicating their reliance on efficient pH regulation in the blood. Ongoing ocean warming and acidification could influence the oxygen-binding properties of respiratory pigments in ectothermic marine invertebrates. This study examined whether S. officinalis differentially expresses individual hemocyanin isoforms to maintain optimal oxygen transport during development and acclimation to elevated seawater pCO2 and temperature. Using quantitative PCR, we measured relative mRNA expression levels of three different hemocyanin isoforms in several ontogenetic stages (embryos, hatchlings, juveniles, and adults), under different temperatures and elevated seawater pCO2. Our results indicate moderately altered hemocyanin expression in all embryonic stages acclimated to higher pCO2, while hemocyanin expression in hatchlings and juveniles remained unaffected. During the course of development, total hemocyanin expression increased independently of pCO2 or thermal acclimation status. Expression of isoform 3 is reported for the first time in a cephalopod in this study and was found to be generally low but highest in the embryonic stages (0.2% of total expression). Despite variable hemocyanin expression, hemolymph total protein concentrations remained constant in the experimental groups. Our data provide first evidence that ontogeny has a stronger influence on hemocyanin isoform expression than the environmental conditions chosen, and they suggest that hemocyanin protein abundance in response to thermal acclimation is regulated by post-transcriptional/translational rather than by transcriptional modifications

Xenobiotic metabolism and its physiological consequences in high-Antarctic Notothenioid fishes.

The Antarctic ecosystem is progressively exposed to anthropogenic contaminants, such as polycyclic aromatic hydrocarbons (PAHs). So far, it is largely unknown if PAHs leave a mark in the physiology of high-Antarctic fish. We approached this issue via two avenues: first, we examined the functional response of the aryl hydrocarbon receptor (Ahr), which is a molecular initiating event of many toxic effects of PAHs in biota. Chionodraco hamatus and Trematomus loennbergii served as representatives for high-Antarctic Notothenioids, and Atlantic cod, Gadus morhua as non-polar reference species. We sequenced and cloned the Ahr ligand binding domain (LBD) of the Notothenioids and deployed a GAL4-based luciferase reporter gene assay expressing the Ahr LBD. Benzo[a]pyrene (BaP), beta-naphthoflavone and chrysene were used as ligands for the reporter gene assay. Second, we investigated the energetic costs of Ahr activation in isolated liver cells of the Notothenioids during acute, non-cytotoxic BaP exposure. In the reporter assay, the Ahr LBD of Atlantic cod and the Antarctic Notothenioids were activated by the ligands tested herein. In the in vitro assays with isolated liver cells of high-Antarctic Notothenioids, BaP exposure had no effect on overall respiration, but caused shifts in the respiration dedicated to protein synthesis. Thus, our study demonstrated that high-Antarctic fish possess a functional Ahr that can be ligand-activated in a concentration-dependent manner by environmental contaminants. This is associated with altered cost for cellular protein synthesis. Future studies have to show if the toxicant-induced activation of the Ahr pathway may lead to altered organism performance of Antarctic fish. Supplementary Information The online version contains supplementary material available at 10.1007/s00300-021-02992-4

ACUTE VS. DEVELOPMENTAL ACCLIMATION SHAPES PARENTAL AND GRANDPARENTAL EFFECTS OF OCEAN WARMING ON MARINE STICKLEBACKS

Transgenerational plasticity (TGP) can buffer populations against rapid environmental change, yet little is known about the underlying mechanisms or how long these effects persist. We tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks, and investigated mitochondrial respiration capacity (MRC) as a potential mechanism underlying growth responses. Acute exposure to elevated temperature during reproductive conditioning led to strong maternal TGP benefits on F1 offspring growth, with a matching pattern for MRC, providing an intuitive mechanistic basis for maternal acclimation persisting into adulthood. Developmental acclimation to elevated temperature, however, led to negative maternal effects on F2 offspring growth and no detectable maternal effects on MRC. But, maternal grandmother TGP benefits were still present for both growth and MRC, perhaps resulting from epigenetic marks on mitochondrial genes acquired during acute exposure. In summary, both parental and grandparental TGP will play a role in mediating some of the impacts of climate change, but the mechanisms underlying offspring phenotype plasticity may differ depending on whether mothers experience acute or developmental acclimation

Persistent organic pollutants in tissues of the white-blooded Antarctic fish Champsocephalus gunnari and Chaenocephalus aceratus

The global occurrence of persistent organic pollutants (POPs) continuously contributes to their accumulation also in remote areas such as the Antarctic Ocean. Antarctic fish , which hold high trophic positions but appear to possess low endogenous elimination rates for chemicals, are expected to bioaccumulate POPs with rising anthropogenic pollution. Using a chemical-analytical method, we measured concentrations of PCBs, PBDEs, HCBs, HCH and DDTs and determined toxic equivalents (TEQs) and bioanalytical equivalents (BEQs) in muscle and ovaries of Antarctic icefish caught in the Southern Ocean around Elephant Island. We used two species with different feeding habits and trophic web positions: the planktivorous Champsocephalus gunnari and the piscivorous Chaenocephalus aceratus . Our results revealed higher contaminant levels in ovary than in muscle tissues of both species. Most analytes concentrations and the TEQs (0.2-0.5) and BEQs (0.2) were lower as in temperate species. Comparison with literature data points to higher PCB (20-22 ng g(-1) lipid weight (lw)) and DDT (7 19.5 ng g(-1) lw) concentrations than those measured in icefish in the 90's. For the other contaminants, we could not identify temporal trends. We found a higher bioaccumulation of contaminants, particularly HCB and DDTs, in C. aceratus (6.2 & 19.5 ng g(-1) lw, respectively) than in C. gunnari (3.8 & 7.0 ng g(-1) lw, respectively). However, there was no general species-specific accumulation pattern of the different toxicant classes between the two icefish. Thus, the expected link between contaminant burdens of C aceratus and C gunnari and their ecological traits was only weakly supported for these species

Mitochondrial Function in Antarctic Nototheniids with ND6 Translocation

Fish of the suborder Notothenioidei have successfully radiated into the Southern Ocean and today comprise the dominant fish sub-order in Antarctic waters in terms of biomass and species abundance. During evolution in the cold and stable Antarctic climate, the Antarctic lineage of notothenioids developed several unique physiological adaptations, which make them extremely vulnerable to the rapid warming of Antarctic waters currently observed. Only recently, a further phenomenon exclusive to notothenioid fish was reported: the translocation of the mitochondrial gene encoding the NADH Dehydrogenase subunit 6 (ND6), an indispensable part of complex I in the mitochondrial electron transport system

Mitochondriale Anpassungsfähigkeit antarktischer Fische und Cephalopoden bei sich ändernden abiotischen Faktoren

Antarctic species possess very low metabolic rates and poor capacities to change their physiological state, thus making them extremely vulnerable to changing environmental conditions. Mitochondria are a key element in shaping whole organism energy turnover and functional capacity. In my study, the effects of rising temperature and increased seawater PCO2 on the energy metabolism were compared between various nototheniids from sub-Antarctic and cold-temperate and Antarctic waters, and between cephalopods from the Antarctic and temperate latitudes. I determined extra- and intracellular blood carbonate parameters, enzymatic capacities and oxygen consumption at whole animal and mitochondrial level and mitochondrial lipid composition and proton leak as a measure for routine metabolic rate, in order to compare their abilities for metabolic compensation towards climate change. My results showed limited aerobic capacities of high-Antarctic fish mitochondria towards the warmth and higher CO2-levels. The mitochondrial responses of cephalopods to an acute temperature rise suggest that they possess similar mitochondrial flexibilities and capacities towards the warmth as fish. Nevertheless, generally more effective capacities for acid-base regulation and larger energy reserves (lipids) in fish compared to cephalopods will putatively make them win the competition for resources over longer time-scales, when seawater temperatures and PCO2 continue to rise

Physiological response and mitochondrial adaptations to changing abiotic factors in Antarctic fish and cephalopods

Antarctic species possess very low metabolic rates and poor capacities to change their physiological state, thus making them extremely vulnerable to changing environmental conditions. Mitochondria are a key element in shaping whole organism energy turnover and functional capacity. In my study, the effects of rising temperature and increased seawater PCO2 on the energy metabolism were compared between various nototheniids from sub-Antarctic and cold-temperate and Antarctic waters, and between cephalopods from the Antarctic and temperate latitudes. I determined extra- and intracellular blood carbonate parameters, enzymatic capacities and oxygen consumption at whole animal and mitochondrial level and mitochondrial lipid composition and proton leak as a measure for routine metabolic rate, in order to compare their abilities for metabolic compensation towards climate change. My results showed limited aerobic capacities of high-Antarctic fish mitochondria towards the warmth and higher CO2-levels. The mitochondrial responses of cephalopods to an acute temperature rise suggest that they possess similar mitochondrial flexibilities and capacities towards the warmth as fish. Nevertheless, generally more effective capacities for acid-base regulation and larger energy reserves (lipids) in fish compared to cephalopods will putatively make them win the competition for resources over longer time-scales, when seawater temperatures and PCO2 continue to rise

Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2

Introduction: Ongoing ocean warming and acidification increasingly affect marine ecosystems, in particular around the Antarctic Peninsula. Yet little is known about the capability of Antarctic notothenioid fish to cope with rising temperature in acidifying seawater. While the whole animal level is expected to be more sensitive towards hypercapnia and temperature, the basis of thermal tolerance is set at the cellular level, with a putative key role for mitochondria. This study therefore investigates the physiological responses of the Antarctic Notothenia rossii after long-term acclimation to increased temperatures (7°C) and elevated PCO2 (0.2 kPa CO2) at different levels of physiological organisation. Results: For an integrated picture, we analysed the acclimation capacities of N. rossii by measuring routine metabolic rate (RMR), mitochondrial capacities (state III respiration) as well as intra- and extracellular acid–base status during acute thermal challenges and after long-term acclimation to changing temperature and hypercapnia. RMR was partially compensated during warm- acclimation (decreased below the rate observed after acute warming), while elevated PCO2 had no effect on cold or warm acclimated RMR. Mitochondrial state III respiration was unaffected by temperature acclimation but depressed in cold and warm hypercapnia-acclimated fish. In both cold- and warm-exposed N. rossii, hypercapnia acclimation resulted in a shift of extracellular pH (pHe) towards more alkaline values. A similar overcompensation was visible in muscle intracellular pH (pHi). pHi in liver displayed a slight acidosis after warm normo- or hypercapnia acclimation, nevertheless, long-term exposure to higher PCO2 was compensated for by intracellular bicarbonate accumulation. Conclusion: The partial warm compensation in whole animal metabolic rate indicates beginning limitations in tissue oxygen supply after warm-acclimation of N. rossii. Compensatory mechanisms of the reduced mitochondrial capacities under chronic hypercapnia may include a new metabolic equilibrium to meet the elevated energy demand for acid–base regulation. New set points of acid–base regulation under hypercapnia, visible at the systemic and intracellular level, indicate that N. rossii can at least in part acclimate to ocean warming and acidification. It remains open whether the reduced capacities of mitochondrial energy metabolism are adaptive or would impair population fitness over longer timescales under chronically elevated temperature and PCO2