France

As poikilotherms, fish exposed to environmental extremes temperatures experience a stressful metabolic challenge, which elicits physiological responses required to maintain cellular homeostasis. These responses include modified glucose or lipid metabolism, altered gene expression and alternative splicing, and endocrine and immune system activity. Additionally, heat seeking may not resolve the homeostatic needs of tropical poikilotherms under unpredictable extreme cold events, which occur frequently due to global climate changes. In spite of the physiological responses that occur in poikilothermic vertebrates, the prevailing notion is that their reduction in metabolic rate is passive. Here, we explored molecular hypothalamic and physiological responses to cold stress in the tropical cichlid, Nile tilapia (Oreochromis niloticus). When exposed to low temperatures, tilapia exhibited complex homeostatic responses, including increased plasma glucose and cortisol concomitant with reduced plasma lactate and metabolic rate. Hypothalamic transcriptome analysis revealed increased oxytocin expression. Blockage of oxytocin signaling using zebrafish CRISPR-knockout lines for oxytocin or its receptors, and pharmacological antagonist in tilapia, further affected temperature-dependent metabolic rate in two cold-exposed tropical fish species. This indicates that oxytocin, a known thermoregulator in homeotherms, actively regulates temperature-related homeostasis in fish. Overall, our findings show that the fish brain actively responds to cold temperature by regulating metabolic physiology. Moreover, we identify oxytocin signaling as an adaptive and evolutionarily conserved metabolic regulator of temperature-related homeostasis. 

SEB Annual Conference 2022

Oxytocin centrally regulates temperature-dependent metabolism in fish

Discover the art of creating extraordinary science at SEB’s Annual Conference at Le Corum Conference Center     in Montpellier, France from 5 to  8 July 2022.

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2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France

technical paper

Land plants cover their epidermis with a specialised protective layer called the cuticle, a feature which is crucial for surviving the perils of a terrestrial environment, including desiccation, UV damage and pathogen attack, dangers which may worsen with our escalating climate crisis. Several cereal staples such as barley and wheat show further epidermal specialisation with a distinctive, glaucous wax bloom on reproductive stage tissues, a feature associated with improved drought tolerance. Understanding the mechanisms underpinning wax bloom development may help breed more climate resilient varieties. To date, studies on barley eceriferum mutants have identified several enzymes involved in cuticular wax biosynthesis. However, little is known about the upstream regulation of this process. My research addresses this knowledge gap by exploiting genetic resources to identify a key regulatory player in barley cuticle development. Here, I will discuss how I used high density genotyping, comparative gene expression and wax compositional analyses to identify a gene essential for wax bloom formation and the expression of cuticular metabolic genes in barley.

Identification of a key regulator controlling cuticular wax in barley

Animals respond to environmental challenges with a suite of physiological responses – the stress response. As high temperatures become more frequent and intense globally, determining whether and how individuals vary in their stress response to heat is urgent. While there is an emerging interest in understanding avian stress response to heat, very often, only glucocorticoids are quantified. Here, we tested whether early-life conditions affect multiple traits of nestling stress physiology in response to heat. In the arid-adapted zebra finch, parents emit “heat-calls” when incubating under high temperatures, which adaptively alter offspring growth. We exposed nestlings to prenatal heat-calls or control-calls, and manipulated postnatal nest temperatures. At 13-day old, we collected blood samples in two experiments: under undisturbed “in-nest” conditions, or following a 2.5-hour heat-challenge. As biomarkers of acute, cellular and chronic stress, we measured, respectively, levels of corticosterone (CORT), constitutive heat-shock cognate 70 (HSC70) and stress-inducible heat-shock protein 90 (HSP90), and, the heterophil to lymphocyte (H/L) ratio. We found that none of the stress biomarkers co-varied in either experiment, likely due to distinct time-courses. After the heat-challenge, only the H/L ratio was higher than in the in-nest experiment. Furthermore, in the in-nest experiment, control-call nestlings had a marginally higher H/L ratio than heat-calls nestlings, and both HSPs increased with nest temperatures, in control-call individuals only. These results suggest a higher sensitivity of control-calls nestlings to summer nest temperatures. Overall, our study shows for the first time that a prenatal acoustic signal for heat affects physiological stress responses to postnatal thermal conditions. 

Prenatal acoustic signals and postnatal heat shape nestling stress physiology

Many pesticides are endocrine-active, even if the intended mechanism of action is not specified to directly interfere with outcomes such as development, reproduction, or sex determination. Pyrethroid pesticides, which are commonly used in both North America and the European Union, are based on toxins naturally produced by the chrysanthemum plant, but are chemically enhanced to increase persistence and toxicity to target organisms. These modifications make pyrethroids more likely to interact with endocrine targets such as the nuclear and membrane estrogen receptors, to modify downstream responses like the activity of steroidogenic enzymes, and to ultimately induce organismal responses indicative of endocrine disruption in fish (e.g. changes in gonad size, sex ratio). Previous work from our group confirmed these interactions for specific pyrethroid types, demonstrating that early life exposure can result in impacts that span multiple generations, and that increased temperature can exacerbate these effects. Recent findings indicate that other abiotic factors, such as salinity, can influence the direction and degree of endocrine-related responses, likely due to a combination of osmoregulatory modulation and differential chemical behavior that is dependent upon aqueous salinity. These observations are highly relevant in terms of predicted changes in temperature and salinity regimes over the coming decades, and our findings underscore the importance of understanding responses to endocrine-active compounds in the context of altered environmental conditions.

Endocrine disruption in the context of climate change: understanding responses in fish

On the upper surface of its leafs salvinia molesta has pillar shaped structures which are hydrophilic at the tip and hydrophobic at the shaft. When submerged under water, air is retained between the surface structure. Beside the storage of oxygen this feature enables a variety of further applications. The air layer could serve as barrier to prevent the settlement of biological organisms (antifouling) and reduce wall shear stress if water flows along the surface. These phenomena are from higher interest in case of ships or liquid transport in pipes. If an air retaining structure could be realised on such surfaces, a reduction of frictional drag, fuel consumption and CO2 production could follow. A requirement for this is the understanding of the physics and the influence of fundamental parameters such as structure geometry, size, contact angle of the structure material, pressure, or air saturation of the liquid. In this work the effect of different parameters is presented and discussed using numerical simulation, analytical approaches and experiments.

Air Retaining Surface Structure of Salvinia molesta - Physics, Applications and Challenges1

Muscles perform a number of roles, acting as motor, brakes and shock absorbers. Tendons also perform several roles, acting as transmission and/or elastic springs. But a distinct and perhaps largely overlooked role of isometric muscles and tendons is as functional tension bicycle spokes, becoming loaded in turn through simple geometry, and enabling horizontal translation during vertical weight support without high mechanical power demand. Here, quadrupedal mammal leg structure and function is considered in the context of enabling low mechanical demand at the level of the limb by maintain forces perpendicular to velocity, at the same time as providing low power supply by keeping muscles isometric when loaded, or unloaded when changing in length. These principles provide a simple account for the general structure of the scapula, serratus ventralis and triceps brachii of the forelimb, and the biceps femoris (curiously crossing across the femur), vastus, rectus femoris and tensor fasciae latae of the hindlimb. Different muscles experience tension at different stages in stance, each resulting in linkages where the links are isometric, and the limb supports predominantly vertical forces during horizontal translation.

Legs as linkages: thinking of isometric muscles and tendons as bicycle spokes

Cereal grains are among the most important sources of energy for humans and domestic animals, owing to large and nutritious endosperm tissues. We study nuclear organization and chromatin in seeds of cereals using cultivated barley (Hordeum vulgare subsp. vulgare) - a diploid temperate zone model cereal used for both food and feed. Barley has a large genome (2n = 2x = 14, 1C = 5.1 Gbp) with interphase chromosomes organized in Rabl configuration with centromeres and telomeres clustering at opposite nuclear poles. Though considered to be typical for large cereal genomes, observations of Rabl configuration are based mostly on nuclei from meristematic tissues. We explored interphase chromosome organization in different tissues of developing barley grains and will show that Rabl chromosome organization is not a general rule in barley and it diminishes with the increasing nuclear DNA content and seed age. Furthermore, we performed transcriptome profiling of different barley grain tissues that allowed determining roles of different biological processes and also chromatin regulatory pathways during this critical stage of development. In summary, all these facets of our barley chromatin research create a fruitful environment for future functional analyses of nuclear organization and epigenetic regulation of gene expression in this agriculturally important species.

The dynamics of chromatin changes during barley seed development

Reactive oxygen species (ROS) are by-products of oxidative metabolism, and while low levels contribute to cell signalling, high levels can be toxic. In mammals, ischaemia-reperfusion leads to production of toxic levels of ROS, which cause oxidative tissue damage. In contrast, anoxia-tolerant species, such as the freshwater turtle, do not sustain oxidative tissue damage after anoxia and reoxygenation. How anoxia-tolerant animals are able to prevent ROS dysregulation and oxidative damage with anoxia is unclear. We investigated ROS production and antioxidant capacity in the turtle heart upon anoxia-reoxygenation. Using the in vivo mass-spectrometric H2O2-probe MitoB, we found that there is no excessive production of ROS in the turtle heart after whole animal anoxia-reoxygenation. We hypothesized that this was due to the fact that turtles avoid large accumulation of succinate in the heart and preserve energy levels. This would prevent reverse electron transfer and extensive ROS production from complex I after anoxia. However, addition of exogenous succinate and manipulation of membrane potential with oligomycin did not induce excessive ROS production in turtle heart strips in vitro. This suggests that other factors, such as S-nitrosation of complex I, supercomplex stability or high antioxidant capacity may also be involved in preventing ROS after anoxia in the turtle heart. Together, this study shows that turtles are able to avoid toxic levels of ROS in the heart and oxidative tissue damage after anoxia and reoxygenation. 

Low in vivo production of reactive oxygen species after anoxia and reoxygenation prevents oxidative damage in the turtle heart

Surviving in low oxygen environments requires complex and integrated physiological responses, many of which center on economizing energy budgets. At the cellular level, significant reductions in protein synthesis and even translational arrest (in anoxia) can save as much as 90% of routine ATP demand. This suggests strategic investment in the protein complement of essential tissues, like the heart, that must maintain some level of function for the animal to survive through and recover from a hypoxic bout. The use of quantitative proteomics in animal models of hypoxia tolerance has unveiled new ideas about how the cardiac proteome is influenced by hypoxia exposure, as well as the ontogenic constraints on this aspect of cardiac plasticity. For example, developmental hypoxia exposure of American alligators (Alligator mississippiensis) induces persistent shifts in the cardiac proteome that, paradoxically, reflect an increased capacity for translation, proteolysis, and metabolic capacity. Concomitant with these changes was an equitable down-regulation of seemingly random cardiac proteins, which may offset the cellular energy budget. In Western painted turtles (Chrysemys picta bellii), the cold acclimation required to prepare tissues for chronic anoxia during winter dormancy induced general down-regulation of electron transport system proteins in adult but not hatchling turtles. Interestingly, both studies revealed 
‘age’ as a key explanatory variable in the cardiac proteome. This suggests a robust developmental program in the ectotherm heart that is resilient even to potent environmental stressors like oxygen and temperature, and warrants further investigations into the developmental thresholds of hypoxia tolerance.






Proteomes & Juveniles: A synthesis of ideas on the ontogeny of hypoxia tolerance

There are several pre- and post-natal routes whereby the adverse effect of parental age on offspring longevity (the Lansing effect) could occur, and the nature and magnitude of the effects could also be influenced by environmental factors that affect parent or offspring state. Furthermore, we know little about the extent to which any such effects persist beyond the first generation. In this talk we will describe experiments in which female zebra finches lived in a mildly stressful environment other when they were not breeding. In both young and old age these females bred with young males, thereby controlling for effects of old father age. The telomere length of their offspring at 30 days after hatching was compared with those produced by females that always lived in a benign environment. When the mothers were young, those that had lived in the more stressful environment had sons (but not daughters) with significantly shorter telomere lengths than those of mothers living in the benign environment. Offspring of both sexes had substantially shorter telomere lengths when the mother was old than when she was young. This effect of maternal age on F1 offspring persisted into the F2 generation, with grandmother (F0) age at the time of producing the mother (F1) having a substantial effect on telomere length in the F2 offspring. In contrast, no effect of grandmother environment was evident in the F2 generation. Such maternal and grand-maternal age effects on early life telomere length could underpin the Lansing effect.

Effects of maternal and grandmaternal age at breeding on a biomarker of ageing

It is clear that the age of parents at the time of conception can affect the phenotype of the next generation. The most commonly observed adverse trend is for old parents to produce offspring that have a shorter lifespan (the Lansing effect). Effects such as this are important to our understanding of the selective forces shaping life history evolution, yet we rarely understand the underlying mechanisms, nor whether they actually reduce offspring fitness. For instance, is a shorter lifespan due to greater frailty ( = greater likelihood of dying, even at younger ages) or an earlier onset of senescence, and is it offset (or even caused by) a greater investment by the offspring in early reproduction? In this talk I will outline the potential routes whereby a Lansing effect can occur, and discuss how these might be teased apart through carefully designed experimental studies. I will stress that parental age effects such as the Lansing effect can arise via routes that have nothing to do with biological ageing of the parents or their offspring, since there can be indirect effects of parental age such as changes in investment patterns by their mates. We also need to be aware that there may be compensatory responses by the offspring themselves that obscure the underlying effects of parental age. Consideration of these issues should reveal why phenomena such as the Lansing effect are seen in some contexts and not others.  

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Oxytocin centrally regulates temperature-dependent metabolism in fish

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Identification of a key regulator controlling cuticular wax in barley

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