A new paradigm for ammonia excretion in aquatic animals: Role of rhesus (RH) glycoproteins

Patricia A. Wright, Chris M. Wood

Research output: Contribution to journalArticle

222 Citations (Scopus)

Abstract

Ammonia excretion at the gills of fish has been studied for 80 years, but the mechanism(s) involved remain controversial. The relatively recent discovery of the ammonia-transporting function of the Rhesus (Rh) proteins, a family related to the Mep/Amt family of methyl ammonia and ammonia transporters in bacteria, yeast and plants, and the occurrence of these genes and glycosylated proteins in fish gills has opened a new paradigm. We provide background on the evolution and function of the Rh proteins, and review recent studies employing molecular physiology which demonstrate their important contribution to branchial ammonia efflux. Rhag occurs in red blood cells, whereas several isoforms of both Rhbg and Rhcg occur in many tissues. In the branchial epithelium, Rhcg appears to be localized in apical membranes and Rhbg in basolateral membranes. Their gene expression is upregulated during exposure to high environmental ammonia or internal ammonia infusion, and may be sensitive to synergistic stimulation by ammonia and cortisol. Rhcg in particular appears to be coupled to H+ excretion and Na+ uptake mechanisms. We propose a new model for ammonia excretion in freshwater fish and its variable linkage to Na+ uptake and acid excretion. In this model, Rhag facilitates NH3 flux out of the erythrocyte, Rhbg moves it across the basolateral membrane of the branchial ionocyte, and an apical "Na+/NH 3+ exchange complex" consisting of several membrane transporters (Rhcg, V-type H+- ATPase, Na+/H++ exchanger NHE-2 and/or NHE-3, Na+ channel) working together as a metabolon provides an acid trapping mechanism for apical excretion. Intracellular carbonic anhydrase (CA-2) and basolateral Na+/HCO 3- cotransporter (NBC-1) and Na+/K +-ATPase play indirect roles. These mechanisms are normally superimposed on a substantial outward movement of NH3 by simple diffusion, which is probably dependent on acid trapping in boundary layer water by H+ ions created by the catalysed or non-catalysed hydration of expired metabolic CO2. Profitable areas for future investigation of Rh proteins in fish are highlighted: their involvement in the mechanism of ammonia excretion across the gills in seawater fish, their possible importance in ammonia excretion across the skin, their potential dual role as CO 2 transporters, their responses to feeding, and their roles in early life stages prior to the full development of gills.

Original languageEnglish
Pages (from-to)2303-2312
Number of pages10
JournalJournal of Experimental Biology
Volume212
Issue number15
DOIs
StatePublished - Aug 1 2009

Fingerprint

Ammonia
excretion
glycoproteins
Glycoproteins
ammonia
animals
Fishes
membrane
fish
fungal anatomy
protein
transporters
Acids
Membranes
trapping
acid
aquatic animal
Erythrocytes
acids
Fish Proteins

Keywords

  • Ammonia transport
  • Early life stages
  • Gill
  • H-ATPase
  • Rhbg
  • Rhcg
  • Rhg
  • Skin

ASJC Scopus subject areas

  • Animal Science and Zoology
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Physiology
  • Insect Science
  • Aquatic Science

Cite this

A new paradigm for ammonia excretion in aquatic animals : Role of rhesus (RH) glycoproteins. / Wright, Patricia A.; Wood, Chris M.

In: Journal of Experimental Biology, Vol. 212, No. 15, 01.08.2009, p. 2303-2312.

Research output: Contribution to journalArticle

Wright, Patricia A. ; Wood, Chris M. / A new paradigm for ammonia excretion in aquatic animals : Role of rhesus (RH) glycoproteins. In: Journal of Experimental Biology. 2009 ; Vol. 212, No. 15. pp. 2303-2312.
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