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Journal ArticleDOI

Dogmas and controversies in the handling of nitrogenous wastes: osmoregulation during early embryonic development in the marine little skate Raja erinacea; response to changes in external salinity.

15 May 2004-The Journal of Experimental Biology (The Company of Biologists Ltd)-Vol. 207, Iss: 12, pp 2021-2031

TL;DR: The data indicate that little skate embryos synthesize and retain urea, as well as a suite of other osmolytes, in order to regulate osmotic balance with the external environment.

AbstractSUMMARY Marine elasmobranchs retain relatively high levels of urea to counterbalance the osmotic strength of seawater. Oviparous species, such as the little skate Raja erinacea , release encapsulated embryos that hatch after about 9 months on the seafloor. To study the ureosmotic capability of skate embryos, we measured a variety of possible osmolytes and ornithine–urea cycle (OUC) enzyme activities in little skate embryos, and determined their physiological response to dilute seawater (75% SW) exposure relative to controls (100% SW). The urea:trimethylamine oxide (TMAO) + other osmolytes ratio was 2.3–2.7:1. At the earliest stage of development investigated (4 months), there were significant levels of the key OUC enzyme, carbamoyl phosphate synthetase III, as well as ornithine transcarbamoylase, arginase and glutamine synthetase, providing evidence for a functional OUC. Embryos (4 and 8 months) survived and recovered from exposure to 5 days of 75% SW. There was a significant increase in the rate of urea excretion (five- to tenfold), no change in OUC enzyme activities, and significant decreases in the tissue content of urea, TMAO and other osmolytes in embryos exposed to 75% SW compared to 100% SW. Taken together, the data indicate that little skate embryos synthesize and retain urea, as well as a suite of other osmolytes, in order to regulate osmotic balance with the external environment. Interestingly, these ureosmotic mechanisms are in place as early as 4 months, around the time at which the egg capsule opens and the embryo is in more direct contact with the external environment.

Topics: Osmolyte (57%), Skate (56%), Arginase (50%)

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Citations
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Journal ArticleDOI
24 Jan 2007-PLOS ONE
TL;DR: Bayesian analysis is used to examine the evolution of vertebrate Vtg genes in relation to the “3R hypothesis” of whole genome duplication (WGD) and the functional end points of LvH degradation during oocyte maturation to find that teleost Vtgs have experienced a post-R3 lineage-specific gene duplication to form paralogous clusters that correlate to the pelagic and benthic character of the eggs.
Abstract: The spiny ray-finned teleost fishes (Acanthomorpha) are the most successful group of vertebrates in terms of species diversity. Their meteoric radiation and speciation in the oceans during the late Cretaceous and Eocene epoch is unprecedented in vertebrate history, occurring in one third of the time for similar diversity to appear in the birds and mammals. The success of marine teleosts is even more remarkable considering their long freshwater ancestry, since it implies solving major physiological challenges when freely broadcasting their eggs in the hyper-osmotic conditions of seawater. Most extant marine teleosts spawn highly hydrated pelagic eggs, due to differential proteolysis of vitellogenin (Vtg)-derived yolk proteins. The maturational degradation of Vtg involves depolymerization of mainly the lipovitellin heavy chain (LvH) of one form of Vtg to generate a large pool of free amino acids (FAA 150–200 mM). This organic osmolyte pool drives hydration of the ooctye while still protected within the maternal ovary. In the present contribution, we have used Bayesian analysis to examine the evolution of vertebrate Vtg genes in relation to the “3R hypothesis” of whole genome duplication (WGD) and the functional end points of LvH degradation during oocyte maturation. We find that teleost Vtgs have experienced a post-R3 lineage-specific gene duplication to form paralogous clusters that correlate to the pelagic and benthic character of the eggs. Neo-functionalization allowed one paralogue to be proteolyzed to FAA driving hydration of the maturing oocytes, which pre-adapts them to the marine environment and causes them to float. The timing of these events matches the appearance of the Acanthomorpha in the fossil record. We discuss the significance of these adaptations in relation to ancestral physiological features, and propose that the neo-functionalization of duplicated Vtg genes was a key event in the evolution and success of the teleosts in the oceanic environment.

180 citations


Cites background from "Dogmas and controversies in the han..."

  • ...Interestingly, this adaptation is analogous to the oviparous Chondrichthyes that store the organic endproducts of protein metabolism (urea and trimethylamine oxides) in their eggs [143–145]....

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Journal ArticleDOI
TL;DR: This study summarizes available data for chondrichthyes and describes resources for one of the largest projects to characterize one of these fish, Leucoraja erinacea, the little skate, serving as the skate genome project portal linking data, research tools, and teaching resources.
Abstract: Chondrichthyan fishes are a diverse class of gnathostomes that provide a valuable perspective on fundamental characteristics shared by all jawed and limbed vertebrates. Studies of phylogeny, species diversity, population structure, conservation, and physiology are accelerated by genomic, transcriptomic and protein sequence data. These data are widely available for many sarcopterygii (coelacanth, lungfish and tetrapods) and actinoptergii (ray-finned fish including teleosts) taxa, but limited for chondrichthyan fishes. In this study, we summarize available data for chondrichthyes and describe resources for one of the largest projects to characterize one of these fish, Leucoraja erinacea, the little skate. SkateBase ( http://skatebase.org) serves as the skate genome project portal linking data, research tools, and teaching resources.

59 citations


Journal ArticleDOI
TL;DR: A broad review of osmoregulation in elasmobranchs for non-specialists, focusing on recent advances, is provided, highlighting the contribution of drinking and eating processes in maintaining osmotic consistency.
Abstract: This article provides a broad review of osmoregulation in elasmobranchs for non-specialists, focusing on recent advances. Marine and euryhaline elasmobranchs in seawater regulate urea and other body fluid solutes (trimethylamine oxide (TMAO), Na+, Cl−) such that they remain hyper-osmotic to their environment. Salt secretions of the rectal gland and excretions in the urine compensate for continuous inward diffusion of environmental salts. Freshwater and euryhaline elasmobranchs in fresh water synthesise less urea and retain less urea and other body fluid solutes compared to marine elasmobranchs and thus have relatively lower osmolarity. Electrolyte uptake at the gills and kidney reabsorption of salts maintain acid–base balance and ionic consistency. The role of the gills, kidney, liver and rectal gland in elasmobranch osmoregulation is reviewed. The ontogeny of osmoregulatory systems in elasmobranchs and the contribution of drinking and eating processes in maintaining osmotic consistency are discussed. Rec...

59 citations


Cites background from "Dogmas and controversies in the han..."

  • ...Raja erinacea embryos contain significant levels of OUC enzymes as well as synthesise and retain urea, as well as other osmolytes, in order to osmoregulate with changes in external salinity (Steele et al. 2004)....

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  • ...erinacea are in place as early as 4 months, around the time at which the egg capsule opens and the embryo becomes bathed by the external environment (Steele et al. 2004)....

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  • ...These osmoregulatory mechanisms in R. erinacea are in place as early as 4 months, around the time at which the egg capsule opens and the embryo becomes bathed by the external environment (Steele et al. 2004)....

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Journal ArticleDOI
TL;DR: Data suggest that a functional OUC may be present in the skeletal muscle tissues of R. erinacea and that enhanced urea excretion rates and the downregulation of the anchor OUC enzyme, arginase, in the liver may be critical in regulating tissue urea content under dilute‐seawater stress.
Abstract: Urea synthesis via the hepatic ornithine urea cycle (OUC) has been well described in elasmobranchs, but it is unknown whether OUC enzymes are also present in extrahepatic tissues. Muscle and liver urea, trimethylamine oxide (TMAO), and other organic osmolytes, as well as selected OUC enzymes (carbamoyl phosphate synthetase III, ornithine transcarbamoylase, arginase, and the accessory enzyme glutamine synthetase), were measured in adult little skates (Raja erinacea) exposed to 100% or 75% seawater for 5 d. Activities of all four OUC enzymes were detected in the muscle. There were no changes in muscle OUC activities in skates exposed to 75% seawater; however, arginase activity was significantly lower in the liver, compared to controls. Urea, TMAO, and several other osmolytes were significantly lower in the muscle of little skates exposed to 75% seawater, whereas only glycerophosphorylcholine was significantly lower in the liver. Urea excretion rates were twofold higher in skates exposed to 75% seaw...

47 citations


Cites background from "Dogmas and controversies in the han..."

  • ...Alternatively, the OUC in the muscle may simply be a vestige of an important pathway during early development (Steele et al. 2004)....

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  • ...Similarly, urea excretion rates were elevated within the first 3 h after embryonic R. erinacea were exposed to 75% SW (Steele et al. 2004)....

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  • ...Raja erinacea embryos downregulate tissue urea, TMAO, and/or other organic solutes after 5 d of exposure to 75% seawater (SW; Steele et al. 2004)....

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  • ...Moreover, CPSase III and other OUC-related enzymes have been detected in the muscle of Raja erinacea embryos (Steele et al. 2004)....

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Journal ArticleDOI
TL;DR: Despite the similarities of early events related to development of the branchial region and initial outgrowth of the fins, later stages are increasingly characterized by taxon‐specific morphologies making a universal staging table for chondrichthyans less applicable.
Abstract: The ontogeny of the northwestern Atlantic batoid, Leucoraja ocellata, is described with special focus on the development of skate specific morphologies and the development of the fins. The results show that the sequence of events involving the early outgrowth of the paired fins and the initial development of the pharyngeal region is remarkably constant in skates, holocephalians, and sharks. However, differences exist in timing of the reshaping of the mandibular arch region, development of branchial filaments, median fins, denticles, and the order of branchial cleft formation. Despite the similarities of early events related to development of the branchial region and initial outgrowth of the fins, later stages are increasingly characterized by taxon-specific morphologies making a universal staging table for chondrichthyans less applicable. The staging table presented in this study represents an important resource for future studies on batoid embryology.

44 citations


Cites background from "Dogmas and controversies in the han..."

  • ...This need would be caused by factors such as an earlier opening of the egg case to seawater, an event that necessitates having functional osmoregulatory mechanisms in elasmobranchs (Mellinger et al., 1986; Steele et al., 2004)....

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References
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691 citations


Journal ArticleDOI
TL;DR: The sensitivity of the colorimetric reaction and stability of the colour are enhanced over existing related procedures and the serum blank diminished, enabling urea to be precisely measured in micro amounts (1--5 microliters) of serum.
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Journal ArticleDOI
TL;DR: Phylogenetic position, geographical distribution, benthic vs. pelagic habitat, adult size, egg-embryo size, feeding ecology, and embryonic osmoregulation are factors in the retention of oviparity or the evolution of viviparity.
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410 citations


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Journal ArticleDOI
TL;DR: Experiments indicate that evolutionary changes in intracellular solute compositions as well as in protein amino acid sequences can have important roles in intrACEllular protein function.
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364 citations


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Journal ArticleDOI
Abstract: Several procedures for ammonia determination in natural waters by the colorimetric indophenol blue method were tested. Solorzano's procedure, with phenol-alcohol, nitroprusside, alkaline citrate and hypochlorite as reagents, was shown to be appropriate for routine work. An improvement of this procedure was obtained by replacing hypochlorite with sodium dichloro-iso-cyanurate, by adding the catalyst after all other reagents, and by increasing the working pH. Concentration factors are statistically the same as in the original procedure, but the reagent blanks are lower and the color develops faster, both in fresh and in sea water.

323 citations