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The benefit of being still: energy savings during winter dormancy in fish come from inactivity and the cold, not from metabolic rate depression.

ABSTRACT: Winter dormancy is used by many animals to survive the cold and food-poor high-latitude winter. Metabolic rate depression, an active downregulation of resting cellular energy turnover and thus standard (resting) metabolic rate (SMR), is a unifying strategy underlying the persistence of organisms in such energy-limited environments, including hibernating endotherms. However, controversy exists about its involvement in winter-dormant aquatic ectotherms. To address this debate, we conducted simultaneous, multi-day measurements of whole-animal oxygen consumption rate (a proxy of metabolic rate) and spontaneous movement in a model winter-dormant marine fish, the cunner (Tautogolabrus adspersus). Winter dormancy in cunner involved a dampened diel rhythm of metabolic rate, such that a low and stable metabolic rate persisted throughout the 24 h day. Based on the thermal sensitivity (Q10) of SMR as well as correlations of metabolic rate and movement, the reductions in metabolic rate were not attributable to metabolic rate depression, but rather to reduced activity under the cold and darkness typical of the winter refuge among substrate. Previous reports of metabolic rate depression in cunner, and possibly other fish species, during winter dormancy were probably confounded by variation in activity. Unlike hibernating endotherms, and excepting the few fish species that overwinter in anoxic waters, winter dormancy in fishes, as exemplified by cunner, need not involve metabolic rate depression. Rather, energy savings come from inactivity combined with passive physico-chemical effects of the cold on SMR, demonstrating that thermal effects on activity can greatly influence temperature-metabolism relationships, and illustrating the benefit of simply being still in energy-limited environments.

SUBMITTER: Speers-Roesch B

PROVIDER: S-EPMC6158517 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The benefit of being still: energy savings during winter dormancy in fish come from inactivity and the cold, not from metabolic rate depression.

Speers-Roesch Ben B Norin Tommy T Driedzic William R WR

Proceedings. Biological sciences 20180905 1886

Winter dormancy is used by many animals to survive the cold and food-poor high-latitude winter. Metabolic rate depression, an active downregulation of resting cellular energy turnover and thus standard (resting) metabolic rate (SMR), is a unifying strategy underlying the persistence of organisms in such energy-limited environments, including hibernating endotherms. However, controversy exists about its involvement in winter-dormant aquatic ectotherms. To address this debate, we conducted simulta ...[more]

PMID: 30185640

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Project description:Winter dormancy is a seasonal survival strategy common among temperate ectotherms, characterized by inactivity, fasting and low metabolic rates. Previous reports of metabolic rate depression (MRD) in winter-dormant ectotherms, including many fishes, may have resulted from confounding influences of temperature-dependent variation in activity on metabolic rate measurements. We hypothesize that, as demonstrated recently in the winter-dormant cunner (Tautogolabrus adspersus), inactivity and the passive physicochemical (Arrhenius) effect of cold on standard metabolic rate (SMR) are the common primary mechanisms underlying the low metabolic rates among winter-dormant fishes. Using automated video tracking, we investigated threshold temperatures for winter dormancy onset (major reductions in activity, increased sheltering and fasting) in four phylogenetically diverse teleost species reported to be winter dormant: cunner, pumpkinseed sunfish (Lepomis gibbosus), American eel (Anguilla rostrata) and mummichog (Fundulus heteroclitus). All species showed large activity and feeding reductions, but the magnitude of change and dormancy threshold temperature was species-specific. We propose that a continuum of overwintering responses exists among fishes from dormant to lethargic to active. The relationship between activity and metabolic rate was then measured using video-recorded automated respirometry during acute cooling and following cold acclimation in pumpkinseed, mummichog and eel. In all species, activity and metabolic rate were strongly correlated at all temperatures, and cooling caused reduced activity and metabolic rate. When variation in activity was controlled for across temperatures spanning the dormancy thresholds, the thermal sensitivity of metabolic rate including SMR indicated the predominance of passive physicochemical influences (mean Q10<3.5), rather than active MRD. Activity reductions and physicochemical slowing of metabolism owing to cold appear to be the primary energy-saving mechanisms in overwintering fishes.

Project description:Main conclusionCold-acclimation genes in woody dicots without winter-dormancy, e.g., olive-tree, need investigation. Positive relationships between OeFAD8, OeOSM , and OeLIP19 and olive-tree cold-acclimation exist, and couple with increased lipid unsaturation and cutinisation. Olive-tree is a woody species with no winter-dormancy and low frost-tolerance. However, cold-tolerant genotypes were empirically selected, highlighting that cold-acclimation might be acquired. Proteins needed for olive-tree cold-acclimation are unknown, even if roles for osmotin (OeOSM) as leaf cryoprotectant, and seed lipid-transfer protein for endosperm cutinisation under cold, were demonstrated. In other species, FAD8, coding a desaturase producing α-linolenic acid, is activated by temperature-lowering, concomitantly with bZIP-LIP19 genes. The research was focussed on finding OeLIP19 gene(s) in olive-tree genome, and analyze it/their expression, and that of OeFAD8 and OeOSM, in drupes and leaves under different cold-conditions/developmental stages/genotypes, in comparison with changes in unsaturated lipids and cell wall cutinisation. Cold-induced cytosolic calcium transients always occurred in leaves/drupes of some genotypes, e.g., Moraiolo, but ceased in others, e.g., Canino, at specific drupe stages/cold-treatments, suggesting cold-acclimation acquisition only in the latter genotypes. Canino and Moraiolo were selected for further analyses. Cold-acclimation in Canino was confirmed by an electrolyte leakage from leaf/drupe membranes highly reduced in comparison with Moraiolo. Strong increases in fruit-epicarp/leaf-epidermis cutinisation characterized cold-acclimated Canino, and positively coupled with OeOSM expression, and immunolocalization of the coded protein. OeFAD8 expression increased with cold-acclimation, as the production of α-linolenic acid, and related compounds. An OeLIP19 gene was isolated. Its levels changed with a trend similar to OeFAD8. All together, results sustain a positive relationship between OeFAD8, OeOSM and OeLIP19 expression in olive-tree cold-acclimation. The parallel changes in unsaturated lipids and cutinisation concur to suggest orchestrated roles of the coded proteins in the process.

Project description:BackgroundFall dormancy and freezing tolerance characterized as two important phenotypic traits, have great effects on productivity and persistence of alfalfa (Medicago sativa L.). Despite the fact that one of the most limiting traits for alfalfa freezing tolerance in winter is fall dormancy, the interplay between fall dormancy and cold acclimation processes of alfalfa remains largely unknown. We compared the plant regrowth, winter survival, raffinose and amino acids accumulation, and genome-wide differentially expressed genes of fall-dormant cultivar with non-dormant cultivar under cold acclimation.ResultsAveraged over both years, the non-dormant alfalfa exhibited largely rapid regrowth compared with fall dormant alfalfa after last cutting in autumn, but the winter survival rate of fall dormant alfalfa was about 34-fold higher than that of non-dormant alfalfa. The accumulation of raffinose and amino acids were significantly increased in fall dormant alfalfa, whereas were decreased in non-dormant alfalfa under cold acclimation. Expressions of candidate genes encoding raffinose biosynthesis genes were highly up-regulated in fall dormant alfalfa, but down-regulated in non-dormant alfalfa under cold acclimation. In fall dormant alfalfa, there was a significantly down-regulated expression of candidate genes encoding the glutamine synthase, which is indirectly involved in the proline metabolism. A total of eight significantly differentially expressed transcription factors (TFs) related to CBF and ABRE-BFs were identified. The most up-regulated TFs in fall dormant alfalfa cultivar were ABF4 and DREB1C.ConclusionsFall dormant alfalfa drastically increased raffinose and amino acids accumulation under cold acclimation. Raffinose-associated and amino acid-associated genes involved in metabolic pathways were more highly expressed in fall dormant alfalfa than non-dormant alfalfa under cold acclimation. This global survey of transcriptome profiles provides new insights into the interplay between fall dormancy and cold acclimation in alfalfa.

Dataset Information

The benefit of being still: energy savings during winter dormancy in fish come from inactivity and the cold, not from metabolic rate depression.

Publications

The benefit of being still: energy savings during winter dormancy in fish come from inactivity and the cold, not from metabolic rate depression.

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