Adaptation of teleosts to very high salinity

Laverty, Gary; Skadhauge, Erik

doi:10.1016/j.cbpa.2012.05.203

Cited by 67 publications

(38 citation statements)

References 66 publications

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“…from para-to trans-cellular routes) to accommodate the decreased osmotic permeability ( junctional leakiness) of branchial epithelia. Although I am not aware of any direct evidence for this conjecture it is indirectly supported by osmotic permeability and water balance studies on teleosts acclimated to hyperhalinity (Motais et al, 1966(Motais et al, , 1969Gonzalez et al, 2005;Laverty and Skadhauge, 2012). Interestingly, many species of euryhaline fish have upper salinity tolerance thresholds of about 2× seawater (Schultz and McCormick, 2013), which suggests that only the most euryhaline species that tolerate salinities well above 2× seawater have evolved the capacity for qualitatively changing their osmoregulatory strategy when encountering extremely hyperhaline conditions.…”

Section: −1mentioning

confidence: 97%

“…The main challenge in this case is that active transepithelial ion transport and water retention demands are increased greatly, which comes at the price of disproportionately large energetic costs, as reflected, for instance, in Na + /K + -ATPase activity (Karnaky et al, 1976;Kültz et al, 1992;Laverty and Skadhauge, 2012). Increased water retention is achieved by increasing drinking rates, intestinal reabsorption of water via solute-linked transport, and decreased osmotic permeability of gill epithelium (Laverty and Skadhauge, 2012).…”

Section: Evolution Of High Salinity Tolerance In Euryhaline Fishesmentioning

confidence: 99%

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Physiological mechanisms used by fish to cope with salinity stress

Kültz

2015

Journal of Experimental Biology

298

161

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Salinity represents a critical environmental factor for all aquatic organisms, including fishes. Environments of stable salinity are inhabited by stenohaline fishes having narrow salinity tolerance ranges. Environments of variable salinity are inhabited by euryhaline fishes having wide salinity tolerance ranges. Euryhaline fishes harbor mechanisms that control dynamic changes in osmoregulatory strategy from active salt absorption to salt secretion and from water excretion to water retention. These mechanisms of dynamic control of osmoregulatory strategy include the ability to perceive changes in environmental salinity that perturb body water and salt homeostasis (osmosensing), signaling networks that encode information about the direction and magnitude of salinity change, and epithelial transport and permeability effectors. These mechanisms of euryhalinity likely arose by mosaic evolution involving ancestral and derived protein functions. Most proteins necessary for euryhalinity are also critical for other biological functions and are preserved even in stenohaline fish. Only a few proteins have evolved functions specific to euryhaline fish and they may vary in different fish taxa because of multiple independent phylogenetic origins of euryhalinity in fish. Moreover, proteins involved in combinatorial osmosensing are likely interchangeable. Most euryhaline fishes have an upper salinity tolerance limit of approximately 2× seawater (60 g kg −1). However, some species tolerate up to 130 g kg −1 salinity and they may be able to do so by switching their adaptive strategy when the salinity exceeds 60 g kg −1. The superior salinity stress tolerance of euryhaline fishes represents an evolutionary advantage favoring their expansion and adaptive radiation in a climate of rapidly changing and pulsatory fluctuating salinity. Because such a climate scenario has been predicted, it is intriguing to mechanistically understand euryhalinity and how this complex physiological phenotype evolves under high selection pressure.

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Section: −1mentioning

confidence: 97%

Section: Evolution Of High Salinity Tolerance In Euryhaline Fishesmentioning

confidence: 99%

Physiological mechanisms used by fish to cope with salinity stress

Kültz

2015

Journal of Experimental Biology

298

161

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“…Tilapia (Oreochromis mossambicus) in hypersaline conditions significantly shift their gill proteome, featuring increased expression of mitochondrial proteins and the stress protein NDRG1 (Kültz et al, 2013). The Salton Sea, an endorheic lake in California (current salinity 44‰) has endemic fish populations of strongly euryhaline fish (Riedel et al, 2002) and responses to hypersalinity involve ionoregulatory responses primarily to gill and posterior intestine epithelia (reviewed by Laverty and Skadhauge, 2012). Whereas strongly euryhaline fish can survive indefinitely in salinities well above full-strength seawater (32‰), hypersaline conditions above 65‰ cause significant increases in plasma ions (Na + and Cl − ), loss of tissue water content and increased apoptosis in gill ionocytes of the strongly euryhaline tilapia hybrid (Oreochromis mossambicus× O. urolepsis honorum) (Sardella et al, 2004).…”

Section: Nacl Secretion In Seawater and Hypersaline Conditionsmentioning

confidence: 99%

Paracellular pathway remodeling enhances sodium secretion by teleost fish in hypersaline environments

Cozzi

Robertson

Spieker

et al. 2015

Journal of Experimental Biology

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In vertebrate salt-secreting epithelia, Na + moves passively down an electrochemical gradient via a paracellular pathway. We assessed how this pathway is modified to allow Na + secretion in hypersaline environments. Mummichogs (Fundulus heteroclitus) acclimated to hypersaline [2× seawater (2SW), 64‰] for 30 days developed invasive projections of accessory cells with an increased area of tight junctions, detected by punctate distribution of CFTR (cystic fibrosis transmembrane conductance regulator) immunofluorescence and transmission electron miscroscopy of the opercular epithelia, which form a gill-like tissue rich in ionocytes. Distribution of CFTR was not explained by membrane raft organization, because chlorpromazine (50 μmol l ) did not affect opercular epithelia electrophysiology. Isolated opercular epithelia bathed in SW on the mucosal side had a transepithelial potential (V t ) of +40.1±0.9 mV (N=24), sufficient for passive Na + secretion (Nernst equilibrium voltage≡E Na =+24.11 mV). Opercular epithelia from fish acclimated to 2SW and bathed in 2SW had higher V t of +45.1±1.2 mV (N=24), sufficient for passive Na + secretion (E Na =+40.74 mV), but with diminished net driving force. Bumetanide block of Cl − secretion reduced V t by 45% and 29% in SW and 2SW, respectively, a decrease in the driving force for Na + extrusion. Estimates of shunt conductance from epithelial conductance (G t ) versus short-circuit current (I sc ) plots (extrapolation to zero I sc ) suggested a reduction in total epithelial shunt conductance in 2SW-acclimated fish. In contrast, the morphological elaboration of tight junctions, leading to an increase in accessory-cell-ionocyte contact points, suggests an increase in local paracellular conductance, compensating for the diminished net driving force for Na + and allowing salt secretion, even in extreme salinities.

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“…These included genes related to hyper-and hypo-osmotic stress (Kalujnaia et al 2007;Evans and Somero 2008;Laverty and Skadhauge 2012), heat stress (Fangue et al 2006;Purohit et al 2014), hypoxia and oxidative stress (Almeida et al 2002;Woo et al 2013) (see Table S1 for the complete list of genes). Additionally, we investigated the expression levels of the entire set of genes of the ornithine-urea cycle (OUC) pathway: N-acetylglutamate synthase (NAGS), ornithine carbamoyl transferase (OTC), carbamoyl-phosphate synthase III (CPSIII), argininosuccinate synthase (ASS), argininosuccinate lysase (ASL), and arginase (ARG), and one accessory urea pathway gene (ornithine glutamine synthetase (GS)) ( Table 2).…”

Section: Survey Of Published Stress-response Genes Among Degs and Urementioning

confidence: 99%

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

et al. 2015

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The Magadi tilapia (Alcolapia grahami) is a cichlid fish that inhabits one of the Earth's most extreme aquatic environments, with high pH ( -10), salinity (-60 % of seawater), high temperatures ( -40 °C), and fluctuating oxygen regimes. The Magadi tilapia evolved several unique behavioral, physiological, and anatomical adaptations, some of which are constituent and thus retained in freshwater conditions. We conducted a transcriptomic analysis on A. grahami to study the evolutionary basis of tolerance to multiple stressors. To identify the adaptive regulatory changes associated with stress responses, we massively sequenced gill transcriptomes (RNAseq) from wild and freshwater-acclimated specimens of A. grahami. As a control, corresponding transcriptome data from Oreochromis leucostictus, a closely related freshwater species, were generated. We found expression differences in a large number of genes with known functions related to osmoregulation, energy metabolism, ion transport, and chemical detoxification. Over-representation of metabolism-related gene ontology terms in wild individuals compared to laboratory-acclimated specimens suggested that freshwater conditions greatly decrease the metabolic requirements of this species. Twenty-five genes with diverse physiological functions related to responses to water stress showed signs of divergent natural selection between the Magadi tilapia and its freshwater relative, which shared a most recent common ancestor only about four million years ago. The complete set of genes responsible for urea excretion was identified in the gill transcriptome of A. grahami, making it the only fish species to have a functional ornithine-urea cycle pathway in the gills a major innovation for increasing nitrogenous waste efficiency.

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Adaptation of teleosts to very high salinity

Cited by 67 publications

References 66 publications

Physiological mechanisms used by fish to cope with salinity stress

Physiological mechanisms used by fish to cope with salinity stress

Paracellular pathway remodeling enhances sodium secretion by teleost fish in hypersaline environments

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

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