Bioenergetics of Adaptation to a Salinity Transition in Euryhaline Teleost (Oreochromis mossambicus) Brain

Weng, Ching‐Feng; Chiang, Chia‐Chang; Gong, Hong‐Yi; Chen, Mark Hung‐Chih; Huang, Wei‐Tung; Cheng, Ching‐Yi; Wu, Jen‐Leih

doi:10.1177/153537020222700108

Cited by 11 publications

(9 citation statements)

References 24 publications

(20 reference statements)

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“…These changes are reflected in an increased energy demand based on the high glycolytic potential observed in BW-and HSW-acclimated fish, as suggested by changes displayed by PFK activity. This increased glycolysis may be related to the increase described by Weng et al (62) in both Na ϩ -K ϩ -ATPase and creatine kinase activities in brain of tilapia transferred from FW to SW. Another interesting finding was the increase in brain ATP and lactate levels in parallel with salinity, suggesting that the increased use of carbohydrates is higher than the energy demand of the brain, producing an accumulation of both lactate and ATP as a result. This accumulation also probably reflects that the energy demand of the brain decreases at lower salinities, since BW appears to be of a less stressor capacity than HSW.…”

Section: )mentioning

confidence: 92%

“…The absence of changes in the remaining parameters assessed may also lend support to the lower activation of kidney metabolism during osmotic acclimation and coincides with similar results obtained by Kelly et al (14) in kidneys of black sea bream in which no changes in parameters related to glycolysis, pentose phosphate shunt, and glucose export capacities in fish acclimated to SW and HSW were observed. Only one previous study (62) addressed metabolic changes in fish brain associated with osmotic adaptation, describing changes in ATP levels and creatine kinase activity in tilapia during the first hours of transfer from FW to SW. The results obtained in the present experiments demonstrate that acclimation of S. aurata to salinities either lower or higher than normal produces a mobilization of brain glycogen levels, which constitutes the major energy store of fish brain (49).…”

Section: )mentioning

confidence: 99%

“…In this way, a stressful situation such as adaptation to different osmotic conditions should produce effects similar to those of other stressors already evaluated in fish brain. Nevertheless, this possibility has received little attention to date (62).…”

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Acclimation ofS. auratato various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs

Sangiao‐Alvarellos¹,

Laiz‐Carrión²,

Guzmán³

et al. 2003

American Journal of Physiology-Regulatory, Integrative and Comp

133

107

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The impact of different environmental salinities on the energy metabolism of gills, kidney, liver, and brain was assessed in gilthead sea bream (Sparus aurata) acclimated to brackish water [BW, 12 parts/thousand (ppt)], seawater (SW, 38 ppt) and hyper saline water (HSW, 55 ppt) for 14 days. Plasma osmolality and levels of sodium and chloride presented a clear direct relationship with environmental salinities. A general activation of energy metabolism was observed under different osmotic conditions. In liver, an enhancement of glycogenolytic and glycolytic potential was observed in fish acclimated to BW and HSW compared with those in SW. In plasma, an increased availability of glucose, lactate, and protein was observed in parallel with the increase in salinity. In gills, an increased Na ϩ -K ϩ -ATPase activity, a clear decrease in the capacity for use of exogenous glucose and the pentose phosphate pathway, as well as an increased glycolytic potential were observed in parallel with the increased salinity. In kidney, Na ϩ -K ϩ -ATPase activity and lactate levels increased in HSW, whereas the capacity for the use of exogenous glucose decreased in BW-and HSWacclimated fish compared with SW-acclimated fish. In brain, fish acclimated to BW or HSW displayed an enhancement in their potential for glycogenolysis, use of exogenous glucose, and glycolysis compared with SW-acclimated fish. Also in brain, lactate and ATP levels decreased in parallel with the increase in salinity. The data are discussed in the context of energy expenditure associated with osmotic acclimation to different environmental salinities in fish euryhaline species.Gilthead sea bream; Sparus aurata; osmoregulation; energy metabolism ADAPTATION OF EURYHALINE FISH to different environmental salinities induces changes/activation of ion transport mechanisms. This adaptation is usually accompanied by changes in oxygen consumption, suggesting variations in the energetic demands for osmoregulation. Thus five patterns of metabolic response to altered environmental salinities have been suggested by Morgan and Iwama (37) in fish, including: 1) no change in metabolic rate, 2) metabolic rate is minimum in isotonic salinity and increased at lower and higher salinities, 3) metabolic rate increases linearly with salinity, 4) metabolic rates higher in freshwater (FW) that decrease in isotonic media [do not tolerate seawater (SW)], and 5) rate highest in SW and decreasing in other salinities. These changes in oxygen consumption can lead to variations in whole body metabolism. The metabolic response of the fish to different osmotic conditions undoubtedly includes both stress and osmoregulation components, but the relative energetic demands of these processes cannot be discerned from whole animal oxygen consumption. Thus, not unexpectedly, alterations in intermediary metabolism related to osmoregulation are not fully understood in fish (41). In addition, the influence of environmental salinities on the growth rate in fish is also poorly understood (4).Although the function...

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Section: )mentioning

confidence: 92%

Section: )mentioning

confidence: 99%

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Acclimation ofS. auratato various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs

Sangiao‐Alvarellos¹,

Laiz‐Carrión²,

Guzmán³

et al. 2003

American Journal of Physiology-Regulatory, Integrative and Comp

133

107

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“…The important increase observed in HK activity in HSW-and LSW-acclimated fish also suggests that at least part of the increased glucose within the brain is coming directly from the blood stream. An increased energy demand in brain during the first days of acclimation to HSW is also suggested by increased glycolytic capacity, which can be related to the increase observed in Na + ,K + -ATPase and creatine kinase activities in brain of tilapia transferred from FW to SW (Weng et al, 2002). Another interesting finding was the increase in lactate levels in HSW-acclimated fish, which indicate that the increased use of carbohydrates is higher than the energy demand of the brain, resulting in an accumulation of lactate.…”

Section: Brain Energy Metabolismmentioning

confidence: 99%

Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus

Sangiao‐Alvarellos

Arjona

Río

et al. 2005

Journal of Experimental Biology

160

103

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Changes in different osmoregulatory and metabolic parameters over time were assessed in gills, kidney, liver and brain of gilthead sea bream Sparus auratus transferred either from seawater (SW, 38 p.p.t.) to hypersaline water (HSW, 55 p.p.t.) or from SW to low salinity water (LSW, 6 p.p.t.) for 14 days. Changes displayed by osmoregulatory parameters revealed two stages during hyperosmotic and hypo-osmotic acclimation: (i) an adaptive period during the first days of acclimation (1-3 days), with important changes in these parameters, and (ii) a chronic regulatory period (after 3 days of transfer) where osmotic parameters reached homeostasis. From a metabolic point of view, two clear phases can also be distinguished during acclimation to hyperosmotic or hypo-osmotic conditions. The first one coincides with the adaptive period and is characterized by enhanced levels of plasma metabolites (glucose, lactate, triglycerides and protein), and use of these metabolites by different tissues in processes directly or indirectly involved in osmoregulatory work. The second stage coincides with the chronic regulatory period observed for the osmoregulatory parameters and is metabolically characterized in HSW-transferred fish by lower energy expenditure and a readjustment of metabolic parameters to levels returning to normality, indicative of reduced osmoregulatory work in this stage. In LSW-transferred fish, major changes in the second stage include: (i) decreased glycolytic potential, capacity for exporting glucose and potential for amino acid catabolism in liver; (ii) enhanced use of exogenous glucose through glycolysis, pentose phosphate and glycogenesis in gills; (iii) increased glycolytic potential in kidney; and (iv) increased glycogenolytic potential and capacity for use of exogenous glucose in brain.

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“…In particular, proteins involved in amino acid metabolism are consistently increased to a lesser extent during salinity stress than most other mitochondrial proteins. During severe salinity stress, activation of energy metabolism may have priority to produce ATP needed for fueling active transepithelial ion transport (65)(66)(67). In addition, activation of fatty acid metabolism may be essential to repair membrane damage and adjust the lipid composition/physicochemical properties of cell membranes in the face of altered salinity (68,69).…”

Section: Discussionmentioning

confidence: 99%

Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

Kültz

Gardell

et al. 2013

Molecular & Cellular Proteomics

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A two-tiered label-free quantitative (LFQ) proteomics workflow was used to elucidate how salinity affects the molecular phenotype, i.e. proteome, of gills from a cichlid fish, the euryhaline tilapia (Oreochromis mossambicus). The workflow consists of initial global profiling of relative tryptic peptide abundances in treated versus control samples followed by targeted identification (by MS/MS) and quantitation (by chromatographic peak area integration) of validated peptides for each protein of interest. Fresh water acclimated tilapia were independently exposed in separate experiments to acute short-term (34 ppt) and gradual long-term (70 ppt, 90 ppt) salinity stress followed by molecular phenotyping of the gill proteome. The severity of salinity stress can be deduced with high technical reproducibility from the initial global label-free quantitative profiling step alone at both peptide and protein levels. However, an accurate regulation ratio can only be determined by targeted label-free quantitative profiling because not all peptides used for protein identification are also valid for quantitation. Of the three salinity challenges, gradual acclimation to 90 ppt has the most pronounced effect on gill molecular phenotype. Known salinity effects on tilapia gills, including an increase in the size and number of mitochondria-rich ionocytes, activities of specific ion transporters, and induction of specific molecular chaperones are reflected in the regulation of abundances of the corresponding proteins. Moreover, specific protein isoforms that are responsive to environmental salinity change are resolved and it is revealed that salinity effects on the mitochondrial proteome are nonuniform. Furthermore, protein NDRG1 has been identified as a novel key component of molecular phenotype restructuring during salinity-induced gill remodeling. In conclusion, besides confirming known effects of salinity on gills of euryhaline fish, molecular phenotyping reveals novel insight into proteome changes that underlie the remodeling of tilapia gill epithelium in response to environmental salinity change. Molecular & Cellular Proteomics 12: 10.1074/ mcp.M113.029827, 3962-3975, 2013.Euryhaline fish are capable of living in fresh water (FW), 1 brackish water (BW), seawater (SW), and hypersaline water (ϾSW). They adjust transepithelial ion transport across gill epithelium when challenged by an environmental salinity change (1). Acclimation from hyposmotic (relative to plasma, e.g. FW) to hyperosmotic (relative to plasma, e.g. SW) environments is accompanied by extensive remodeling of gill epithelium, the most prominent feature of which is an increase in the number and size of salt-secretory, mitochondria-rich ionocytes (2). In addition, molecular chaperones and distinct sets of transport proteins are activated when euryhaline fish are challenged by increasing environmental salinity (3)(4)(5). A euryhaline fish species in which these physiological responses have been observed is the Mozambique tilapia, Oreochromis mossambicus (6 -8). Tilapi...

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Bioenergetics of Adaptation to a Salinity Transition in Euryhaline Teleost (Oreochromis mossambicus) Brain

Cited by 11 publications

References 24 publications

Acclimation ofS. auratato various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs

Acclimation ofS. auratato various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs

Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus

Quantitative Molecular Phenotyping of Gill Remodeling in a Cichlid Fish Responding to Salinity Stress

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