In vivo oocyte hydration in Atlantic halibut (Hippoglossus hippoglossus); proteolytic liberation of free amino acids, and ion transport, are driving forces for osmotic water influx

Abstract

SUMMARY The in vivo swelling and hydration of maturing oocytes of Atlantic halibut Hippoglossus hippoglossus were studied in order to characterise the osmotic mechanism underlying oocyte hydration in oviparous marine teleosts that spawn pelagic eggs. Sequential biopsies from two females, spanning four hydration cycles, were examined by osmometry, solute analysis and electrophoresis of dissected hydrating oocytes and ovulated eggs. The hydration cycle of the biopsied halibuts lasted 33–54 h. The majority of ovarian oocytes existed in a pre-hydrated condition (individual wet mass approx. 3.7 mg, diameter approx. 1.87 mm, 63 % H2O) with easily visible, non-coalesced, yolk platelets. Group-synchronous batches of the pre-hydrated oocytes increased in individual wet mass, diameter and water content to reach the ovulated egg stage of approximately 15 mg, 3.0 mm and 90 % H2O, respectively. The yolk osmolality of the hydrating oocytes was transiently hyperosmotic to the ovarian fluid (range 305–350 mOsmol l–1) with a peak osmolality of about 450 mOsmol l–1 in oocytes of 6–8 mg individual wet mass. The transient hyperosmolality was well accounted for by the increase in oocyte content of free amino acids (FAAs; approx. 2300 nmol oocyte–1), K+ (approx. 750 nmol oocyte–1), Cl– (approx. 900 nmol oocyte–1), total ammonium (approx. 300 nmol oocyte–1) and inorganic phosphate (Pi; approx. 200 nmol oocyte–1) when relating to the increase in cellular water. The oocyte content of Na+ did not increase during the hydration phase. Extensive proteolysis of yolk proteins, in particular a 110 kDa protein, correlated with the increase in the FAA pool, although the latter increased by approx. 20 % more than could be accounted for by the decrease in the oocyte protein content. Both indispensable and dispensable amino acids increased in the FAA pool, and particularly serine, alanine, leucine, lysine, glutamine and glutamate. Taurine content remained stable at approx. 70 nmol oocyte–1 during oocyte hydration. The results show that final hydration of Atlantic halibut oocytes is caused by an osmotic water uptake in which FAAs, derived mainly from the hydrolysis of a 110 kDa yolk protein, contribute approximately 50 % of the yolk osmolality and ions (Cl–, K+, Pi, NH4+) make up the balance.

Spatial Ecology of Atlantic Halibut across the Northwest Atlantic: A Recovering Species in an Era of Climate Change

“…A detailed characterization of Gulf of St. Lawrence Atlantic halibut spawning behavior from the same recovered PSATs revealed that Atlantic halibut engage in distinct rapid, 3-202 minute (median of 21 min) rises off the seafloor of an amplitude ranging between 25 and 284 m (Marshall 2020). Supporting earlier evidence for batch spawning (Methven et al 1992), female Atlantic halibut performed between 5 and 13 spawning rises (median of 7) with a median between-rise interval of 3.15 days (Marshall 2020), which corresponds to the time necessary for female Atlantic halibut to hydrate sequential egg batches (Finn et al 2002).…”

Cause of increased size of acipenseriform eggs infected with Polypodium hydriforme

“…Fulton (1897) noted that pelagic eggs of teleosts increase in size during the maturation phase and surmised that this increase in water content affected egg buoyancy. Additional studies have confirmed that pelagic eggs take on more water than benthic eggs of marine teleosts (Finn et al ., 2002a; Matsubara & Koya, 1997) and thus show a greater increase in size. The influx of water is primarily driven by high concentrations of free amino acids (Craik & Harvey, 1987; Finn et al ., 2002b, 2002a; Fyhn et al ., 1999; Thorsen & Fyhn, 1996), and phosphate and other ions (Craik & Harvey, 1986, 1987).…”

“…Additional studies have confirmed that pelagic eggs take on more water than benthic eggs of marine teleosts (Finn et al ., 2002a; Matsubara & Koya, 1997) and thus show a greater increase in size. The influx of water is primarily driven by high concentrations of free amino acids (Craik & Harvey, 1987; Finn et al ., 2002b, 2002a; Fyhn et al ., 1999; Thorsen & Fyhn, 1996), and phosphate and other ions (Craik & Harvey, 1986, 1987). The increase in size in the paddlefish eggs infected with P. hydriforme is comparable to those of pelagic eggs in marine teleosts.…”

Molecular Mechanisms of Spawning Habits for the Adaptive Radiation of Endemic East Asian Cyprinid Fishes

“…Although marine pelagic eggs achieve hydration in the ovary in the same way [37,40,41], the effect of the T-FAA content on the osmolality of marine pelagic eggs is considerably greater than that of freshwater semibuoyant eggs. This result indicates that fishes have likely evolved divergent metabolic pathways under different salinity regimes.…”