scholarly journals Osmoregulatory role of the intestine in the sea lamprey (Petromyzon marinus)

2020 ◽  
Vol 318 (2) ◽  
pp. R410-R417 ◽  
Author(s):  
A. Barany ◽  
C. A. Shaughnessy ◽  
J. Fuentes ◽  
J. M. Mancera ◽  
S. D. McCormick
Keyword(s):  
Water Absorption ◽  
Salinity Tolerance ◽  
Ex Vivo ◽  
Petromyzon Marinus ◽  
Sea Lamprey ◽  
Posterior Intestine ◽  
Direct Exposure ◽  
Plasma Chloride ◽  
Anterior Intestine

Lampreys are the most basal vertebrates with an osmoregulatory strategy. Previous research has established that the salinity tolerance of sea lamprey increases dramatically during metamorphosis, but underlying changes in the gut have not been examined. In the present work, we examined changes in intestinal function during metamorphosis and seawater exposure of sea lamprey ( Petromyzon marinus). Fully metamorphosed juvenile sea lamprey had 100% survival after direct exposure to 35 parts per thousand seawater (SW) and only slight elevations in plasma chloride (Cl−) levels. Drinking rates of sea lamprey juveniles in seawater were 26-fold higher than juveniles in freshwater (FW). Na+-K+-ATPase (NKA) activity in the anterior and posterior intestine increased 12- and 3-fold, respectively, during metamorphosis, whereas esophageal NKA activity was lower than in the intestine and did not change with development. Acclimation to SW significantly enhanced NKA activity in the posterior intestine but did not significantly change NKA activity in the anterior intestine, which remained higher than that in the posterior intestine. Intestinal Cl− and water uptake, which were observed in ex vivo preparations of anterior and posterior intestine under both symmetric and asymmetric conditions, were higher in juveniles than in larvae and were similar in magnitude of those of teleost fish. Inhibition of NKA by ouabain in ex vivo preparations inhibited intestinal water absorption by 64%. Our results indicate drinking and intestinal ion and water absorption are important to osmoregulation in SW and that preparatory increases in intestinal NKA activity are important to the development of salinity tolerance that occurs during sea lamprey metamorphosis.

scholarly journals Tissue and salinity specific Na+/Cl− cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
A. Barany ◽  
C. A. Shaughnessy ◽  
R. M. Pelis ◽  
J. Fuentes ◽  
J. M. Mancera ◽  
...  
Keyword(s):  
Water Absorption ◽  
Salinity Tolerance ◽  
Ex Vivo ◽  
Short Circuit ◽  
Short Circuit Current ◽  
Sea Lamprey ◽  
Mrna Levels ◽  
Gene Encoding ◽  
Distal Intestine ◽  
Proximal Intestine

AbstractTwo orthologues of the gene encoding the Na+-Cl− cotransporter (NCC), termed ncca and nccb, were found in the sea lamprey genome. No gene encoding the Na+-K+-2Cl− cotransporter 2 (nkcc2) was identified. In a phylogenetic comparison among other vertebrate NCC and NKCC sequences, the sea lamprey NCCs occupied basal positions within the NCC clades. In freshwater, ncca mRNA was found only in the gill and nccb only in the intestine, whereas both were found in the kidney. Intestinal nccb mRNA levels increased during late metamorphosis coincident with salinity tolerance. Acclimation to seawater increased nccb mRNA levels in the intestine and kidney. Electrophysiological analysis of intestinal tissue ex vivo showed this tissue was anion absorptive. After seawater acclimation, the proximal intestine became less anion absorptive, whereas the distal intestine remained unchanged. Luminal application of indapamide (an NCC inhibitor) resulted in 73% and 30% inhibition of short-circuit current (Isc) in the proximal and distal intestine, respectively. Luminal application of bumetanide (an NKCC inhibitor) did not affect intestinal Isc. Indapamide also inhibited intestinal water absorption. Our results indicate that NCCb is likely the key ion cotransport protein for ion uptake by the lamprey intestine that facilitates water absorption in seawater. As such, the preparatory increases in intestinal nccb mRNA levels during metamorphosis of sea lamprey are likely critical to development of whole animal salinity tolerance.

Development of longitudinal mucosal folds in the intestine of the anadromous sea lamprey, Petromyzon marinus L., during metamorphosis

1978 ◽  
Vol 56 (11) ◽  
pp. 2364-2371 ◽  
Author(s):  
John H. Youson ◽  
Kerry L. Connelly
Keyword(s):  
Connective Tissue ◽  
Late Stage ◽  
Petromyzon Marinus ◽  
Sea Lamprey ◽  
Intestinal Development ◽  
Proliferating Cells ◽  
Posterior Intestine ◽  
Anterior Intestine ◽  
Mode Of Development ◽  
Mucosal Folds

During metamorphosis of the anadromous sea lamprey, Petromyzon marinus L., the larval intestine develops numerous longitudinal folds. The initiation of this event is marked by a decrease in diameter of the intestine and in the height of the typhlosole and is followed by an increase in numbers of cells undergoing DNA synthesis, first in the anterior intestine and later in the posterior intestine. Foci of proliferating cells along the epithelial walls of both regions result in the development of longitudinal folds which seem to elongate by further proliferation of the epithelial cells at their bases and by evagination of the underlying connective tissue and muscle. Slight variations in the mode of development of folds in the anterior and posterior intestines likely reflect the different functions of these regions in the adult. Metamorphosis of the lamprey provides an opportunity to study intestinal development in a vertebrate during a late stage of ontogeny.

Tissue- and Salinity-specific Na–Cl Cotransporter (NCC) Orthologues Involved in the Sea lamprey (Petromyzon Marinus) Adaptive Osmoregulation

2021 ◽  
Author(s):  
A. Barany ◽  
C. A. Shaughnessy ◽  
R. M. Pelis ◽  
J. Fuentes ◽  
J. M. Mancera ◽  
...  
Keyword(s):  
Water Absorption ◽  
Ex Vivo ◽  
Short Circuit ◽  
Ussing Chamber ◽  
Petromyzon Marinus ◽  
Short Circuit Current ◽  
Sea Lamprey ◽  
Intestinal Tissue ◽  
Distal Intestine ◽  
Phylogenetic Comparison

Abstract Two ncc orthologues (termed ncca and nccb) were found in the sea lamprey genome, whereas nkcc2 was not. In a phylogenetic comparison among other vertebrate amino acids, NCC and NKCC deduced sequences, the sea lamprey NCC’s occupied basal positions within the NCC clade. In freshwater, ncca mRNA was found only in the gill and nccb only in the intestine, whereas both were found in the kidney. Acclimation to seawater increased nccb mRNA in the intestine and kidney. Intestinal nccb mRNA also increased during late metamorphosis. The electrophysiological approach in the Ussing chamber of intestinal tissue ex vivo showed significant differences between freshwater and seawater-acclimated juveniles. Luminal application of indapamide (NCC inhibitor) resulted in 73 and 30% inhibition of short-circuit current (Isc) in the proximal and distal intestine, respectively. The luminal application of bumetanide (NKCC inhibitor) did not affect intestinal Isc. Indapamide also inhibited ex vivo intestinal water absorption. Our results indicate that NCCb is likely the key passive ion cotransporter protein for ion uptake by the lamprey intestine to facilitate water absorption in seawater. As such, the preparatory increases in intestinal nccb mRNA expression during metamorphosis are likely critical to the development of whole animal salinity tolerance.

Guanylin peptides regulate electrolyte and fluid transport in the Gulf toadfish (Opsanus beta) posterior intestine

2014 ◽  
Vol 307 (9) ◽  
pp. R1167-R1179 ◽  
Author(s):  
Ilan M. Ruhr ◽  
Charlotte Bodinier ◽  
Edward M. Mager ◽  
Andrew J. Esbaugh ◽  
Cameron Williams ◽  
...  
Keyword(s):  
Fluid Transport ◽  
Short Circuit ◽  
Secretory Response ◽  
Seawater Adaptation ◽  
Posterior Intestine ◽  
Ussing Chambers ◽  
Opsanus Beta ◽  
Anterior Intestine ◽  
Gulf Toadfish

The physiological effects of guanylin (GN) and uroguanylin (UGN) on fluid and electrolyte transport in the teleost fish intestine have yet to be thoroughly investigated. In the present study, the effects of GN, UGN, and renoguanylin (RGN; a GN and UGN homolog) on short-circuit current ( Isc) and the transport of Cl−, Na+, bicarbonate (HCO3−), and fluid in the Gulf toadfish ( Opsanus beta) intestine were determined using Ussing chambers, pH-stat titration, and intestinal sac experiments. GN, UGN, and RGN reversed the Isc of the posterior intestine (absorptive-to-secretory), but not of the anterior intestine. RGN decreased baseline HCO3− secretion, but increased Cl− and fluid secretion in the posterior intestine. The secretory response of the posterior intestine coincides with the presence of basolateral NKCC1 and apical cystic fibrosis transmembrane conductance regulator (CFTR), the latter of which is lacking in the anterior intestine and is not permeable to HCO3− in the posterior intestine. However, the response to RGN by the posterior intestine is counterintuitive given the known role of the marine teleost intestine as a salt- and water-absorbing organ. These data demonstrate that marine teleosts possess a tissue-specific secretory response, apparently associated with seawater adaptation, the exact role of which remains to be determined.

scholarly journals 11-Deoxycortisol is a stress responsive and gluconeogenic hormone in a jawless vertebrate, the sea lamprey (Petromyzon marinus)

2021 ◽  
Author(s):  
Ciaran A. Shaughnessy ◽  
Stephen D. McCormick
Keyword(s):  
Plasma Glucose ◽  
Phosphoenolpyruvate Carboxykinase ◽  
Ex Vivo ◽  
Petromyzon Marinus ◽  
Regulatory Protein ◽  
Intraperitoneal Administration ◽  
Sea Lamprey ◽  
Mrna Levels ◽  
Binding Studies ◽  
Handling Stress

Although corticosteroid-mediated hepatic gluconeogenic activity in response to stress has been extensively studied in fishes and other vertebrates, there is little information on the stress response in basal vertebrates. In sea lamprey (Petromyzon marinus), a representative member of the most basal extant vertebrate group Agnatha, 11-deoxycortisol and deoxycorticosterone are the major circulating corticosteroids. The present study examined changes in circulating glucose and 11-deoxycortisol concentrations in response to a physical stressor. Furthermore, the gluconeogenic actions of 11-deoxycortisol and deoxycorticosterone were examined. Within 6 h after exposure of larval and juvenile sea lamprey to an acute handling stress, plasma 11-deoxycortisol levels increased 15- and 6-fold, respectively, and plasma glucose increased 3- and 4-fold, respectively. Radiometric receptor binding studies revealed that a corticosteroid receptor (CR) is present in the liver at lower abundance than other tissues (gill and anterior intestine) and that the binding affinity of the liver CR was similar for 11-deoxycortisol and deoxycorticosterone. Transcriptional tissue profiles indicate a wide distribution of cr transcription, kidney-specific transcription of steroidogenic acute regulatory protein (star), and liver-specific transcription of phosphoenolpyruvate carboxykinase (pepck). Ex vivo incubation of liver tissue with 11-deoxycortisol resulted in dose-dependent increases in pepck mRNA levels. Finally, intraperitoneal administration of 11-deoxycortisol and deoxycorticosterone demonstrated that only 11-deoxycortisol resulted in an increase in plasma glucose. Together, these results provide the first direct evidence for the gluconeogenic activity of 11-deoxycortisol in an Agnathan, indicating that corticosteroid regulation of plasma glucose is a basal trait among vertebrates.

The role of local ecological knowledge for the conservation and sustainable fisheries of the sea lamprey (Petromyzon marinus Linnaeus, 1758) in the Iberian Peninsula

2020 ◽  
Vol 198 ◽  
pp. 105345
Author(s):  
Heitor Oliveira Braga ◽  
Mário Jorge Pereira ◽  
Joelson Musiello-Fernandes ◽  
Fernando Morgado ◽  
Amadeu M.V.M. Soares ◽  
...  
Keyword(s):  
Iberian Peninsula ◽  
Local Ecological Knowledge ◽  
Petromyzon Marinus ◽  
Sea Lamprey ◽  
Ecological Knowledge ◽  
Sustainable Fisheries

Decline and Recovery of the Lake Superior Gull Island Reef Lake Trout (Salvelinus namaycush) Population and the Role of Sea Lamprey (Petromyzon marinus) Predation

1980 ◽  
Vol 37 (11) ◽  
pp. 2074-2080 ◽  
Author(s):  
Bruce L. Swanson ◽  
Donald V. Swedberg
Keyword(s):  
Lake Trout ◽  
Lake Superior ◽  
Petromyzon Marinus ◽  
Total Mortality ◽  
Mortality Rates ◽  
Sea Lamprey ◽  
Salvelinus Namaycush ◽  
Steady Increase ◽  
Egg Deposition

The Gull Island Reef lake trout (Salvelinus namaycush) population was one of the few in Lake Superior that was not annihilated by the combined effects of excessive fishing and sea lamprey (Petromyzon marinus) predation. Following control of the lamprey in the early 1960s, this population of lake trout began a slow but steady increase in the average age and numbers of lake trout. Total annual mortality rates for spawning lake trout were 32% for age VI fish, 48% for ages VII–VIII, and 75% for ages IX and older. These total mortality rates included a 7.3% exploitation rate u, a 20% natural mortality n, and annual lamprey-induced mortalities of 6% for ages V–VI, 24%, for ages VII–VIII, and 56% for ages IX and older fish. The estimated number of lake trout eggs deposited annually on Gull Island Reef from 1964 to 1979 ranged from 3.3 million eggs in 1965 to 28 million eggs in 1979, with a mean of 9 million eggs per year. At present levels of lamprey predation, the estimated egg to spawning fish return rate on Gull Island Reef is 0.18%.Key words: lake trout, sea lamprey, survival, population structure, egg deposition

scholarly journals The role of the rectum in osmoregulation and the potential effect of renoguanylin on SLC26a6 transport activity in the Gulf toadfish (Opsanus beta)

2016 ◽  
Vol 311 (1) ◽  
pp. R179-R191 ◽  
Author(s):  
Ilan M. Ruhr ◽  
Yoshio Takei ◽  
Martin Grosell
Keyword(s):  
Water Absorption ◽  
Short Circuit ◽  
Short Circuit Current ◽  
Potential Effect ◽  
Posterior Intestine ◽  
Distal Intestine ◽  
Opsanus Beta ◽  
Ion Absorption ◽  
Gulf Toadfish

Teleosts living in seawater continually absorb water across the intestine to compensate for branchial water loss to the environment. The present study reveals that the Gulf toadfish ( Opsanus beta) rectum plays a comparable role to the posterior intestine in ion and water absorption. However, the posterior intestine appears to rely more on SLC26a6 (a HCO3−/Cl− antiporter) and the rectum appears to rely on NKCC2 (SLC12a1) for the purposes of solute-coupled water absorption. The present study also demonstrates that the rectum responds to renoguanylin (RGN), a member of the guanylin family of peptides that alters the normal osmoregulatory processes of the distal intestine, by inhibited water absorption. RGN decreases rectal water absorption more greatly than in the posterior intestine and leads to net Na+ and Cl− secretion, and a reversal of the absorptive short-circuit current ( ISC). It is hypothesized that maintaining a larger fluid volume within the distal segments of intestinal tract facilitates the removal of CaCO3 precipitates and other solids from the intestine. Indeed, the expression of the components of the Cl−-secretory response, apical CFTR, and basolateral NKCC1 (SLC12a2), are upregulated in the rectum of the Gulf toadfish after 96 h in 60 ppt, an exposure that increases CaCO3 precipitate formation relative to 35 ppt. Moreover, the downstream intracellular effects of RGN appear to directly inhibit ion absorption by NKCC2 and anion exchange by SLC26a6. Overall, the present findings elucidate key electrophysiological differences between the posterior intestine and rectum of Gulf toadfish and the potent regulatory role renoguanylin plays in osmoregulation.

scholarly journals Functional characterization and osmoregulatory role of the Na+-K+-2Cl− cotransporter in the gill of sea lamprey (Petromyzon marinus), a basal vertebrate

2020 ◽  
Vol 318 (1) ◽  
pp. R17-R29 ◽  
Author(s):  
Ciaran A. Shaughnessy ◽  
Stephen D. McCormick
Keyword(s):  
Petromyzon Marinus ◽  
Functional Characterization ◽  
Sea Lamprey ◽  
Peptide Sequence ◽  
Muscle Water Content ◽  
Muscle Water ◽  
Basal Position ◽  
Salt Secretion

The present study provides molecular and functional characterization of Na+-K+-2Cl− cotransporter (NKCC1/Slc12a2) in the gills of sea lamprey ( Petromyzon marinus), the most basal extant vertebrate with an osmoregulatory strategy. We report the full-length peptide sequence for the lamprey Na-K-Cl cotransporter 1 (NKCC1), which we show groups strongly with and occupies a basal position among other vertebrate NKCC1 sequences. In postmetamorphic juvenile lamprey, nkcc1 mRNA was present in many tissues but was fivefold higher in the gill than any other examined tissue, and NKCC1 protein was only detected in the gill. Gill mRNA and protein abundances of NKCC1 and Na+-K+-ATPase (NKA/Atp1a1) were significantly upregulated (20- to 200-fold) during late metamorphosis in fresh water, coinciding with the development of salinity tolerance, and were upregulated an additional twofold after acclimation to seawater (SW). Immunohistochemistry revealed that NKCC1 in the gill is found in filamental ionocytes coexpressing NKA, which develop during metamorphosis in preparation for SW entry. Lamprey treated with bumetanide, a widely used pharmacological inhibitor of NKCC1, exhibited higher plasma Cl− and osmolality as well as reduced muscle water content after 24 h in SW; there were no effects of bumetanide in freshwater-acclimated lamprey. This work provides the first functional characterization of NKCC1 as a mechanism for branchial salt secretion in lampreys, providing evidence that this mode of Cl− secretion has been present among vertebrates for ~550 million years.

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