Abstract
Two 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.
Highlights
Lampreys are one of two surviving lineages of jawless fishes of the group Agnatha
It has been hypothesized that a first-round of whole-genome duplication (1R) in vertebrates led to an initial divergence of NKCC from NCC and that a second round of whole-genome duplication (2R) in the vertebrate lineage resulted in multiple NKCC and NCC isoforms, NKCC1/NKCC2 and NCC1/NCC248
Our molecular phylogenetic analysis showed that the NCC1 and NCC2 of bony fishes were grouped into distinct NCC1 and NCC2 clades
Summary
Lampreys are one of two surviving lineages of jawless fishes of the group Agnatha. Agnathans appear to have diverged during the late Ordovician period ~ 450 million years ago (mya)[1,2] and persisted through several confirmed mass extinctions on Earth[3,4]. Modern lampreys are iono- and osmoregulators, in that they maintain their plasma osmolality at approximately one-third that of seawater (SW) regardless of external salinity This osmoregulatory strategy is found in most other extant vertebrate lineages, with the notable exception of elasmobranchs, coelacanths, and lungfishes[11,12]. The osmotic force for water absorption from the lumen is driven by salt transport and facilitated along the gastrointestinal tract by luminal C aCO3 precipitation[21] This process begins with ingested SW filling lateral intercellular spaces between ion-transporting e nterocytes[23]. Expression of an orthologous NCC (termed NCC1) in teleost fishes acclimated to freshwater (FW) environments has been shown to be highly expressed in the kidney, presumably fulfilling a similar role in NaCl a bsorption[33,34]. Information regarding the importance of NCC in intestinal ion and water uptake in other fish species is still scarce[20]
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
