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Biology subjects

Matoo, O. B.

Publications and source records attributed to Matoo, O. B..

4 recordsLinked to original sources

Two Genomes, One Metabolome: Mitonuclear Incompatibility Remodels Developmental Metabolism and Fitness in Drosophila

Mitochondrial-nuclear (hereafter mitonuclear) genetic variation can alter cellular bioenergetics and metabolism via jointly encoding the subunits of oxidative phosphorylation (OXPHOS) system. Here we tested whether genetic variation in biochemical and bioenergetic phenotype can scale up across higher levels of biological organization to affect organismal development. We used a panel of (mtDNA); nDNA genotypes created by asymmetric substitution of divergent mtDNA between Drosophila melanogaster and its sister species D. simulans. Two genotypes - (ore); OreR and (ore); Aut - carry coevolved mitonuclear genomes from D. melanogaster, whereas the other two - (w501); Aut and (w501); OreR - harbor D. simulans mitochondrial DNA introgressed onto D. melanogaster nuclear backgrounds. We utilized untargeted metabolomics to track down the comprehensive biochemical footprint of the joint genomic architecture in the metabolome of these genotypes. We show that in (w501); OreR larvae with mitonuclear genome incompatibility there is extensive and coordinated metabolic remodeling of carbon, nitrogen, and redox balance, characterized by increased glycolysis, limited TCA cycle, amino acid scarcity, reduced nucleic acid balance, lipid remodeling, with compensatory activation of antioxidant pathways and possible epigenetic modulation by metabolites. This biochemical rewiring puts a physiological constraint that prioritizes maintenance metabolism over larval growth, leading to reduced body size, slow locomotion and delayed development, despite a compensatory increase in feeding in these larvae. These findings underscore the context dependency of mitonuclear interactions, which can uniquely scale up to influence organismal energy budget trade-offs, fitness and life-history evolution.

physiology↗

Mitochondrial-nuclear variation for metabolic plasticity with potential consequences for invasion success in New Zealand mud snails

Metabolic rate is an emergent organismal trait that integrates energetic costs of living and influences species distributions and response to climate change. For ectotherms, metabolic rate is likely shaped by interactions between mitochondrial and nuclear genomes and environmental temperature. Variation in reproductive mode (e.g., asexual vs. sexual reproduction) can enhance or interfere with cross-generational transmission of these interactions, with implications for evolutionary responses to selection on standing genetic variation for metabolism-related traits. We leveraged known patterns of mitochondrial-nuclear discordance in a global invader, the snail Potamopyrgus antipodarum, to measure thermal plasticity of metabolic rate in invasive vs. native asexual lineages that combined multiple mitochondrial haplotypes with nuclear genomic variation from distinct lake populations. Native lineages harbored significant mitochondrial-nuclear variation for metabolic plasticity, with some genotypes maintaining low metabolic rates at high temperature. Invasive lineages contained only a small subset of this variation, with non-plastic and lower metabolic rates relative to native lineages at high temperature. Together, these data indicate that mitochondrial-nuclear-environment interactions contribute to variation in the metabolic rate of asexual lineages. Our results also demonstrate that invasive lineages have metabolic phenotypes that could facilitate successful colonization of aquatic habitats via decreased maintenance metabolism under high temperatures.

ecology↗

Temperature but not ocean acidification affects energy metabolism and enzyme activities in the blue mussel, Mytilus edulis

O_LIIn mosaic marine habitats such as intertidal zones ocean acidification (OA) is exacerbated by high variability of pH, temperature, and biological CO2 production. The non-linear interactions among these drivers can be context-specific and their effect on organisms in these habitats remains largely unknown, warranting further investigation. C_LIO_LIWe were particularly interested in Mytilus edulis (the blue mussel) from intertidal zones of Gulf of Maine (GOM), USA for this study. GOM is a hot spot of global climate change (average SST increasing by > 0.2 {degrees}C y-1) with > 60% decline in mussel population over the past 40 years. C_LIO_LIHere, we utilize bioenergetic underpinnings to identify limits of stress tolerance in M. edulis from GOM exposed to warming and OA. We have measured whole-organism oxygen consumption rates and metabolic biomarkers in mussels exposed to control and elevated temperatures (10 vs. 15 {degrees}C) and moderate PCO2 levels (~ 400 vs. 800 atm). C_LIO_LIOur study demonstrates that adult M. edulis from GOM are metabolically resilient to the moderate OA scenario but responsive to warming as seen in changes in metabolic rate, energy reserves, metabolite profiles and enzyme activities. C_LIO_LIOur results are in agreement with recent literature that OA scenarios for the next 100-300 years do not affect this species, possibly as a consequence of maintaining its in vivo acid-base balance. C_LI

ecology↗

Genetic variation for ontogenetic shifts in metabolism underlies physiological homeostasis in Drosophila

Organismal physiology emerges from metabolic pathways and structures that can vary across development and among individuals. Here we tested whether genetic variation at one level of physiology can be buffered at higher levels during development by the inherent capacity for homeostasis in physiological systems. We found that the fundamental scaling relationship between mass and metabolic rate, as well as the oxidative capacity per mitochondria, differed significantly across development in the fruit fly Drosophila. However, mitochondrial respiration rate was maintained across development at similar levels. Furthermore, genotypes clustered into two types--those that switched to aerobic, mitochondrial ATP production before the second instar and those that relied on anaerobic production of ATP via glycolysis through the second instar. Despite genetic variation for the timing of this metabolic shift, second-instar metabolic rate was more robust to genetic variation than was the metabolic rate of other instars. We also found that a mitochondrial-nuclear genotype with disrupted mitochondrial function both increased aerobic capacity more through development and relied more heavily on anaerobic ATP production relative to wildtype genotypes. By taking advantage of both ways of making ATP, this genotype maintained mitochondrial respiratory capacity, but also generated more free radicals and had decreased mitochondrial membrane potential, potentially as a physiological-defense mechanism. Taken together, the data revealed that genetic defects in core physiology can be buffered at the organismal level via physiological compensation and that natural populations likely harbor genetic variation for distinct metabolic strategies in development that generate similar organismal outcomes.

genetics↗