Literature DB >> 25274361

What is the primary function of the early teleost gill? Evidence for Na+/NH+4 exchange in developing rainbow trout (Oncorhynchus mykiss).

Alex M Zimmer1, Patricia A Wright2, Chris M Wood3.   

Abstract

Post-hatch fishes lack a functional gill and use cutaneous surfaces for exchange with the surrounding environment. The ionoregulatory hypothesis posits that ionoregulation is the first physiological process to be limited by cutaneous exchange, necessitating its shift to the gills. We hypothesized that the ontogeny of branchial ammonia excretion (J amm) is coupled to Na(+) uptake (J Na in) in accordance with the current model for Na+/NH4+ in exchange in freshwater. Using divided chambers, branchial and cutaneous J amm, J Na in and oxygen consumption (MO2) by larval rainbow trout were assessed. Following hatch, the skin accounted for 97% and 86% of total J amm and J Na in, respectively. J amm and J Na in shifted to the gills simultaneously at 15 days post-hatch (dph) and were highly correlated (R(2) = 0.951) at the gills, but not the skin, over development. Contrastingly, MO2 shifted significantly later at 27 dph, in agreement with the ionoregulatory hypothesis. Moreover, the mRNA expression and/or enzymatic activity of Rhesus proteins, Na(+)/H(+)-exchanger, H(+)-ATPase, Na(+)/K(+)-ATPase and carbonic anhydrase, all key components of the Na+/NH4+-exchange system, increased in the gills over larval development. We propose that the ontogeny of branchial J Na in occurs as Na+/NH4+ exchange and provide evidence for a novel element to the ionoregulatory hypothesis, the excretion of potentially lethal metabolic ammonia.
© 2014 The Author(s) Published by the Royal Society. All rights reserved.

Entities:  

Keywords:  ammonia excretion; gill development; ionoregulatory hypothesis; oxygen consumption; rainbow trout (Oncorhynchus mykiss) larvae; sodium uptake

Mesh:

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Year:  2014        PMID: 25274361      PMCID: PMC4213616          DOI: 10.1098/rspb.2014.1422

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  25 in total

1.  Ammonia excretion via Rhcg1 facilitates Na⁺ uptake in larval zebrafish, Danio rerio, in acidic water.

Authors:  Yusuke Kumai; Steve F Perry
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2011-08-10       Impact factor: 3.619

Review 2.  The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste.

Authors:  David H Evans; Peter M Piermarini; Keith P Choe
Journal:  Physiol Rev       Date:  2005-01       Impact factor: 37.312

3.  Expression of carbamoyl-phosphate synthetase III mRNA during the early stages of development and in muscle of adult rainbow trout (Oncorhynchus mykiss).

Authors:  J J Korte; W L Salo; V M Cabrera; P A Wright; A K Felskie; P M Anderson
Journal:  J Biol Chem       Date:  1997-03-07       Impact factor: 5.157

4.  Ammonia transport across the skin of adult rainbow trout (Oncorhynchus mykiss) exposed to high environmental ammonia (HEA).

Authors:  Alex M Zimmer; Colin J Brauner; Chris M Wood
Journal:  J Comp Physiol B       Date:  2013-10-11       Impact factor: 2.200

5.  Ammonia excretion in rainbow trout (Oncorhynchus mykiss): evidence for Rh glycoprotein and H+-ATPase involvement.

Authors:  C Michele Nawata; Carrie C Y Hung; Tommy K N Tsui; Jonathan M Wilson; Patricia A Wright; Chris M Wood
Journal:  Physiol Genomics       Date:  2007-08-21       Impact factor: 3.107

6.  Ammonia excretion by the skin of zebrafish (Danio rerio) larvae.

Authors:  Tin-Han Shih; Jiun-Lin Horng; Pung-Pung Hwang; Li-Yih Lin
Journal:  Am J Physiol Cell Physiol       Date:  2008-09-24       Impact factor: 4.249

Review 7.  Ontogeny and paleophysiology of the gill: new insights from larval and air-breathing fish.

Authors:  Colin J Brauner; Peter J Rombough
Journal:  Respir Physiol Neurobiol       Date:  2012-08-08       Impact factor: 1.931

8.  Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss.

Authors:  Clarice Fu; Jonathan M Wilson; Peter J Rombough; Colin J Brauner
Journal:  Proc Biol Sci       Date:  2010-01-13       Impact factor: 5.349

9.  Gills are needed for ionoregulation before they are needed for O(2) uptake in developing zebrafish, Danio rerio.

Authors:  Peter Rombough
Journal:  J Exp Biol       Date:  2002-06       Impact factor: 3.312

10.  The respiratory development of Atlantic salmon. II. Partitioning of oxygen uptake among gills, yolk sac and body surfaces

Authors: 
Journal:  J Exp Biol       Date:  1996       Impact factor: 3.312

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  2 in total

1.  Ion regulation at gills precedes gas exchange and the origin of vertebrates.

Authors:  Michael A Sackville; Christopher B Cameron; J Andrew Gillis; Colin J Brauner
Journal:  Nature       Date:  2022-10-19       Impact factor: 69.504

2.  Physiological and molecular ontogeny of branchial and extra-branchial urea excretion in posthatch rainbow trout (Oncorhynchus mykiss).

Authors:  Alex M Zimmer; Chris M Wood
Journal:  Am J Physiol Regul Integr Comp Physiol       Date:  2015-11-25       Impact factor: 3.619

  2 in total

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