Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus

Watson, Caroline J.; Nordi, Wiolene Montanari; Esbaugh, Andrew J.

doi:10.1016/j.cbpa.2014.08.008

Cited by 39 publications

(25 citation statements)

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“…The red drum is one such species; tolerating direct transfer from full‐strength seawater to freshwater (Watson et al. ). This transition resulted in a modest, but persistent, decrease in plasma osmolality with no effect on muscle water content.…”

Section: Introductionmentioning

confidence: 99%

Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Esbaugh¹,

Cutler²

2016

Physiol Rep

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Euryhaline fishes, such as the red drum (Sciaenops ocellatus), must quickly transition between hyperosmotic and hypoosmotic physiological strategies. When freshwater individuals transition to seawater they are exposed to increased diffusive water loss and ion gain. To maintain osmoregulatory balance these animals must drink and absorb seawater through the intestine, followed by ion excretion at the gills. The ability of fishes to transition between strategies can limit the magnitude of osmotic shock that can be tolerated. Here, we demonstrate that red drum can tolerate direct transfer from freshwater to full‐strength seawater with marginal impacts on osmotic balance, as indicated by plasma and muscle ion concentration, as well as muscle water. Seawater transition is concurrent with a significant increase in intestinal fluid volume. Typical patterns of osmoregulatory plasticity were observed in the gill with increased expression of nkcc1 and cftr. Expression changes in the anterior intestine were observed after 24 h for nkcc2 with smaller and later responses observed for slc26a3, slc26a6, and nbc. Immunofluorescence staining demonstrated similar patterns of NKCC localization in freshwater and seawater intestines; however, reduced basolateral staining of V‐type ATPase was observed in seawater. Electrophysiological preparations demonstrated that seawater fish had increased absorptive current in the anterior intestine, which was significantly reduced in the presence of 10 μmol/L bumetanide. Overall, these results suggest that nkcc2 plays a crucial role during hyperosmotic transitions, and may be a more important complement to the well‐known bicarbonate secretion pathway than generally considered.

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Section: Introductionmentioning

confidence: 99%

Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Esbaugh¹,

Cutler²

2016

Physiol Rep

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“…NKCC is an integral membrane protein responsible for the simultaneous transport of one Na + , one K + , and two Cl − ions from the external to the internal side of epithelial cells (Kang et al 2010). Although previous studies suggest that NKCC plays a critical role in the osmoregulatory endurance of fish (Kang et al 2010;Watson et al 2014;LorinNebel et al 2006;Ip et al 2013;Chandrasekar et al 2014), its role in salinity adaptations has been little studied in crustaceans compared to other ion transport genes (i.e., Na + , K + -ATPase, V-type H + -ATPase, carbonic anhydrase (CA)) (Tsai and Lin 2007;Lucu et al 2008;Firmino et al 2011;Han et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Effects of salinity acclimation and eyestalk ablation on Na+, K+, 2Cl− cotransporter gene expression in the gill of Portunus trituberculatus:a molecular correlate for salt-tolerant trait

Zhang

Ping

et al. 2016

Cell Stress and Chaperones

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The Na− cotransporter (NKCC) is an important gene in ion transport. In order to elucidate its function, and regulatory mechanisms, in salinity acclimation, the complete cDNA sequence of NKCC (4218 bp) from Portunus trituberculatus (PtNKCC) was first cloned and characterized. It was found to encode 1055 amino acids containing conserved AA-permease and SLC12 motifs. Results show that PtNKCC is expressed to the greatest extent in gills. High salinity stress exposure led to significant increases (9.6-fold) of PtNKCC mRNA expression in the gills 12 h after treatment, declining to less than the levels seen in the control group between 48 and 72 h. During low salinity stress, expression levels of PtNKCC in gills were found to be upregulated at each sampling time, reaching their peak after 6 h (a 12.4-fold increase). Eyestalk ablation also triggered an 11.3-fold increase in PtNKCC mRNA, while re-injection with eyestalk homogenates significantly reduced the expression of PtNKCC mRNA. Four single nucleotide polymorphisms (SNPs) were detected in the PtNKCC open reading frame, and one SNP was associated with salt tolerance. Our results indicate that PtNKCC plays an important role in the salinity acclimation of P. trituberculatus, while there may be a compound present in the XOSG that inhibits the expression of PtNKCC.

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“…This is likely the result of sufficient baseline activity to account for these acid-base disturbances, which is supported by the whole animal acid flux measurements discussed above. Interestingly, a previous study showed that red drum nhe2 and nhe3 expression was also unchanged in the gill in response to freshwater transfer52. It is well-known that NHE proteins play a major role in Na + uptake in freshwater and many euryhaline species show significant up-regulation in response to freshwater transfer21535455.…”

Section: Discussionmentioning

confidence: 98%

“…Real time PCR primers were developed for nbc and vha (β-subunit), whereas primers for nhe1, nhe2, nhe3, ca-c , and elongation factor 1α ( ef1α ) had previously been developed for red drum52. Full length sequences for both nbc and vha were identified from an in-house gill/intestine transcriptome using Blaststation software.…”

Section: Methodsmentioning

confidence: 99%

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Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

Allmon¹,

Esbaugh²

2017

Sci Rep

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Anthropogenic CO2 is expected to drive ocean pCO2 above 1,000 μatm by 2100 – inducing respiratory acidosis in fish that must be corrected through branchial ion transport. This study examined the time course and plasticity of branchial metabolic compensation in response to varying levels of CO2 in an estuarine fish, the red drum, which regularly encounters elevated CO2 and may therefore have intrinsic resilience. Under control conditions fish exhibited net base excretion; however, CO2 exposure resulted in a dose dependent increase in acid excretion during the initial 2 h. This returned to baseline levels during the second 2 h interval for exposures up to 5,000 μatm, but remained elevated for exposures above 15,000 μatm. Plasticity was assessed via gene expression in three CO2 treatments: environmentally realistic 1,000 and 6,000 μatm exposures, and a proof-of-principle 30,000 μatm exposure. Few differences were observed at 1,000 or 6,000 μatm; however, 30,000 μatm stimulated widespread up-regulation. Translocation of V-type ATPase after 1 h of exposure to 30,000 μatm was also assessed; however, no evidence of translocation was found. These results indicate that red drum can quickly compensate to environmentally relevant acid-base disturbances using baseline cellular machinery, yet are capable of plasticity in response to extreme acid-base challenges.

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Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus

Cited by 39 publications

References 58 publications

Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Effects of salinity acclimation and eyestalk ablation on Na+, K+, 2Cl− cotransporter gene expression in the gill of Portunus trituberculatus:a molecular correlate for salt-tolerant trait

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

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Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus

Cited by 39 publications

References 58 publications

Intestinal Na + , K + , 2Cl − cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Intestinal Na + , K + , 2Cl − cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Effects of salinity acclimation and eyestalk ablation on Na+, K+, 2Cl− cotransporter gene expression in the gill of Portunus trituberculatus:a molecular correlate for salt-tolerant trait

Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost

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Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost

Intestinal Na ⁺ , K ⁺ , 2Cl ⁻ cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost