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1. Keystone predation: trait‐based or driven by extrinsic processes? Assessment using a comparative‐experimental approach

   https://doi.org/10.1002/ecm.1436  

   Menge, Bruce A. ; Foley, Melissa M. ; Robart, Matthew J. ; Richmond, Erin ; Noble, Mae ; Chan, Francis ( December 2020 , Ecological Monographs)

   Keystone predation can be a determinant of community structure, including species diversity, but factors underlying “keystoneness” have been minimally explored. Using the system in which the original keystone, the sea starPisaster ochraceus, was discovered, we focused on two potential (but overlapping) determinants of keystoneness: intrinsic traits or state variables of the species (e.g., size, density), and extrinsic environmental parameters (e.g., prey productivity) that may provide conditions favorable for keystone predator evolution. Using a comparative‐experimental approach, with repeated field experiments at multiple sites across a variable coastal environment, we tested predation rates, or how quickly predators consumed prey, and predation effects, or community response to predator presence or absence. We tested five hypotheses: (H₁) predation rates and effects will vary in space but not time; (H₂) per population predation rates will vary primarily with individual traits and population variables; (HJHH₃) per capita predation rates will vary only with individual traits; (H₄) predation effects will vary with traits, variables, and external drivers; and (H₅) as predicted by the keystone predation hypothesis, diversity will vary unimodally with predation pressure. As hypothesized, predation rates differed among sites but not over time (H₁), and in caging exclusion experiments, predation effect varied with both intrinsicmore »and extrinsic factors (H₄). Unexpectedly, predation rates varied with both intrinsic and extrinsic (H₂, per population), or only with extrinsic (H₃, per capita) factors. Further, in large‐plot exclusion experiments, predation effect was most closely associated with individual traits (contraH₄). Finally, taxon diversity varied unimodally with proxies of predation pressure (sessile prey abundance) and was sensitive to extrinsic factors (mussel growth, temperature, and upwelling,H₅). Hence, keystoneness depended on predator individual traits, predator population variables, and environmental parameters. However, temporal differences in caging experiments suggested that environmental characteristics underlying prey dynamics may be preeminent. Compared to prior experiments, predation was weaker with low prey input compared to periods with high prey input. Collectively, our results suggest that keystone predator evolution depends on the coalescence of species‐specific characteristics, and environmental parameters favoring high prey productivity. Our approach may be a model for future studies exploring the generality of keystoneness.

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2. Metabolic rates of Neomysis americana (Smith, 1873) (Mysida: Mysidae) from a temperate estuary vary in response to summer temperature and salinity conditions

   https://doi.org/10.1093/jcbiol/ruaa031  

   Chapina, Rosaura J ; Rowe, Christopher L ; Woodland, Ryan J ( June 2020 , Journal of Crustacean Biology)

   Abstract The mysid Neomysis americana (Smith, 1873) is native to shallow shelf waters and estuaries of the western Atlantic coast of North America. Despite the important role mysids such as N. americana play in estuarine ecosystems as both consumers and as prey for higher trophic levels, there is limited information on how metabolism influences their spatial ecology and habitat requirements. In tributaries of Chesapeake Bay, MD, USA, previous research has shown that summer water temperatures can approach the lethal upper tolerance limit for N. americana. We measured the per capita metabolic rate (µgO2 min–1) of N. americana from the upper Patuxent River near Benedict, MD, a tributary of Chesapeake Bay in the laboratory to evaluate the metabolic response to salinity and temperature conditions that mysids experience in natural habitats. Sex-specific and diel patterns in metabolic rate were quantified. Metabolic rates did not differ between night and day and there was no significant difference in metabolic rate between males and females, exclusive of gravid females. Metabolic rates were lowest in salinity treatments of 2 and 8 at 29 °C, and highest in the salinity 2 treatment at 22 °C. Only temperature had a statistically significant, albeit unexpected, effect. This study showsmore »that the metabolic response of N. americana to temperature and salinity conditions is complex and plastic, and that metabolic rates can vary 3–4 fold within realistic summer temperature and salinity conditions. As environmental conditions continue to change, understanding metabolic response of mysids to realistic salinity and temperature conditions is necessary for understanding their distributions in temperate estuaries.« less
3. Induction of lysosomal and mitochondrial biogenesis by AMPK phosphorylation of FNIP1

   https://doi.org/10.1126/science.abj5559  

   Malik, Nazma ; Ferreira, Bibiana I. ; Hollstein, Pablo E. ; Curtis, Stephanie D. ; Trefts, Elijah ; Weiser Novak, Sammy ; Yu, Jingting ; Gilson, Rebecca ; Hellberg, Kristina ; Fang, Lingjing ; et al ( April 2023 , Science)

   INTRODUCTION Eukaryotes contain a highly conserved signaling pathway that becomes rapidly activated when adenosine triphosphate (ATP) levels decrease, as happens during conditions of nutrient shortage or mitochondrial dysfunction. The adenosine monophosphate (AMP)–activated protein kinase (AMPK) is activated within minutes of energetic stress and phosphorylates a limited number of substrates to biochemically rewire metabolism from an anabolic state to a catabolic state to restore metabolic homeostasis. AMPK also promotes prolonged metabolic adaptation through transcriptional changes, decreasing biosynthetic genes while increasing expression of genes promoting lysosomal and mitochondrial biogenesis. The transcription factor EB (TFEB) is a well-appreciated effector of AMPK-dependent signals, but many of the molecular details of how AMPK controls these processes remain unknown. RATIONALE The requirement of AMPK and its specific downstream targets that control aspects of the transcriptional adaptation of metabolism remain largely undefined. We performed time courses examining gene expression changes after various mitochondrial stresses in wild-type (WT) or AMPK knockout cells. We hypothesized that a previously described interacting protein of AMPK, folliculin-interacting protein 1 (FNIP1), may be involved in how AMPK promotes increases in gene expression after metabolic stress. FNIP1 forms a complex with the protein folliculin (FLCN), together acting as a guanosine triphosphate (GTP)–activating protein (GAP)more »for RagC. The FNIP1-FLCN complex has emerged as an amino acid sensor to the mechanistic target of rapamycin complex 1 (mTORC1), involved in how amino acids control TFEB activation. We therefore examined whether AMPK may regulate FNIP1 to dominantly control TFEB independently of amino acids. RESULTS AMPK was found to govern expression of a core set of genes after various mitochondrial stresses. Hallmark features of this response were activation of TFEB and increases in the transcription of genes specifying lysosomal and mitochondrial biogenesis. AMPK directly phosphorylated five conserved serine residues in FNIP1, suppressing the function of the FLCN-FNIP1 GAP complex, which resulted in dissociation of RagC and mTOR from the lysosome, promoting nuclear translocation of TFEB even in the presence of amino acids. FNIP1 phosphorylation was required for AMPK to activate TFEB and for subsequent increases in peroxisome proliferation–activated receptor gamma coactivator 1-alpha (PGC1α) and estrogen-related receptor alpha (ERRα) mRNAs. Cells in which the five serines in FNIP1 were mutated to alanine were unable to increase lysosomal and mitochondrial gene expression programs after treatment with mitochondrial poisons or AMPK activators despite the presence and normal regulation of all other substrates of AMPK. By contrast, neither AMPK nor its control of FNIP1 were needed for activation of TFEB after amino acid withdrawal, illustrating the specificity to energy-limited conditions. CONCLUSION Our data establish FNIP1 as the long-sought substrate of AMPK that controls TFEB translocation to the nucleus, defining AMPK phosphorylation of FNIP1 as a singular event required for increased lysosomal and mitochondrial gene expression programs after metabolic stresses. This study also illuminates the larger biological question of how mitochondrial damage triggers a temporal response of repair and replacement of damaged mitochondria: Within early hours, AMPK-FNIP1–activated TFEB induces a wave of lysosome and autophagy genes to promote degradation of damaged mitochondria, and a few hours later, TFEB–up-regulated PGC1⍺ and ERR⍺ promote expression of a second wave of genes specifying mitochondrial biogenesis. These insights open therapeutic avenues for several common diseases associated with mitochondrial dysfunction, ranging from neurodegeneration to type 2 diabetes to cancer. Mitochondrial damage activates AMPK to phosphorylate FNIP1, stimulating TFEB translocation to the nucleus and sequential waves of lysosomal and mitochondrial biogenesis. After mitochondrial damage, activated AMPK phosphorylates FNIP1 (1), causing inhibition of FLCN-FNIP1 GAP activity (2). This leads to accumulation of RagC in its GTP-bound form, causing dissociation of RagC, mTORC1, and TFEB from the lysosome (3). TFEB is therefore not phosphorylated and translocates to the nucleus, inducing transcription of lysosomal or autophagy genes, with parallel increases in NT-PGC1α mRNA (4), which, in concert with ERRα (5), subsequently induces mitochondrial biogenesis (6). CCCP, carbonyl cyanide m-chlorophenylhydrazone; CLEAR, coordinated lysosomal expression and regulation; GDP, guanosine diphosphate; P, phosphorylation. [Figure created using BioRender]« less
4. Reconstruction and Analysis of Thermodynamically Constrained Models Reveal Metabolic Responses of a Deep-Sea Bacterium to Temperature Perturbations

   https://doi.org/10.1128/msystems.00588-22  

   Dufault-Thompson, Keith ; Nie, Chang ; Jian, Huahua ; Wang, Fengping ; Zhang, Ying ( August 2022 , mSystems)

   Mackelprang, Rachel (Ed.)

   ABSTRACT Microbial acclimation to different temperature conditions can involve broad changes in cell composition and metabolic efficiency. A systems-level view of these metabolic responses in nonmesophilic organisms, however, is currently missing. In this study, thermodynamically constrained genome-scale models were applied to simulate the metabolic responses of a deep-sea psychrophilic bacterium, Shewanella psychrophila WP2, under suboptimal (4°C), optimal (15°C), and supraoptimal (20°C) growth temperatures. The models were calibrated with experimentally determined growth rates of WP2. Gibbs free energy change of reactions (Δ r G ′), metabolic fluxes, and metabolite concentrations were predicted using random simulations to characterize temperature-dependent changes in the metabolism. The modeling revealed the highest metabolic efficiency at the optimal temperature, and it suggested distinct patterns of ATP production and consumption that could lead to lower metabolic efficiency under suboptimal or supraoptimal temperatures. The modeling also predicted rearrangement of fluxes through multiple metabolic pathways, including the glycolysis pathway, Entner-Doudoroff pathway, tricarboxylic acid (TCA) cycle, and electron transport system, and these predictions were corroborated through comparisons to WP2 transcriptomes. Furthermore, predictions of metabolite concentrations revealed the potential conservation of reducing equivalents and ATP in the suboptimal temperature, consistent with experimental observations from other psychrophiles. Taken together, the WP2 models providedmore »mechanistic insights into the metabolism of a psychrophile in response to different temperatures. IMPORTANCE Metabolic flexibility is a central component of any organism’s ability to survive and adapt to changes in environmental conditions. This study represents the first application of thermodynamically constrained genome-scale models in simulating the metabolic responses of a deep-sea psychrophilic bacterium to various temperatures. The models predicted differences in metabolic efficiency that were attributed to changes in metabolic pathway utilization and metabolite concentration during growth under optimal and nonoptimal temperatures. Experimental growth measurements were used for model calibration, and temperature-dependent transcriptomic changes corroborated the model-predicted rearrangement of metabolic fluxes. Overall, this study highlights the utility of modeling approaches in studying the temperature-driven metabolic responses of an extremophilic organism.« less
5. Social Brain Energetics: Ergonomic Efficiency, Neurometabolic Scaling, and Metabolic Polyphenism in Ants

   https://doi.org/10.1093/icb/icac048  

   Coto, Zach N. ; Traniello, James F. A. ( May 2022 , Integrative and Comparative Biology)

   Metabolism, a metric of the energy cost of behavior, plays a significant role in social evolution. Body size and metabolic scaling are coupled, and a socioecological pattern of increased body size is associated with dietary change and the formation of larger and more complex groups. These consequences of the adaptive radiation of animal societies beg questions concerning energy expenses, a substantial portion of which may involve the metabolic rates of brains that process social information. Brain size scales with body size, but little is understood about brain metabolic scaling. Social insects such as ants show wide variation in worker body size and morphology that correlates with brain size, structure, and worker task performance, which is dependent on sensory inputs and information-processing ability to generate behavior. Elevated production and maintenance costs in workers may impose energetic constraints on body size and brain size that are reflected in patterns of metabolic scaling. Models of brain evolution do not clearly predict patterns of brain metabolic scaling, nor do they specify its relationship to task performance and worker ergonomic efficiency, two key elements of social evolution in ants. Brain metabolic rate is rarely recorded and, therefore, the conditions under which brain metabolism influencesmore »the evolution of brain size are unclear. We propose that studies of morphological evolution, colony social organization, and worker ergonomic efficiency should be integrated with analyses of species-specific patterns of brain metabolic scaling to advance our understanding of brain evolution in ants.

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