The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species

Author:

Treberg Jason R.1,Speers-Roesch Ben2,Piermarini Peter M.3,Ip Yuen K.4,Ballantyne James S.2,Driedzic William R.1

Affiliation:

1. Ocean Sciences Centre, Memorial University of Newfoundland, St John's,Newfoundland and Labrador, Canada A1C 5S7

2. Department of Integrative Biology, University of Guelph, Guelph, Ontario,Canada N1G 2W1

3. Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut, USA 06520

4. Department of Biological Science, National University of Singapore, Kent Ridge, Singapore 117543, Republic of Singapore

Abstract

SUMMARYWe compared levels of the major organic osmolytes in the muscle of elasmobranchs, including the methylamines trimethylamine oxide (TMAO), betaine and sarcosine as well as the β-amino acids taurine and β-alanine,and the activities of enzymes of methylamine synthesis (betaine and TMAO) in species with a wide range of urea contents. Four marine, a euryhaline in freshwater (Dasyatis sabina), and two freshwater species, one that accumulates urea (Himantura signifer) and one that does not(Potamotrygon motoro), were analyzed. Urea contents in muscle ranged from 229–352 μmol g–1 in marine species to 2.0μmol g–1 in P. motoro. Marine elasmobranchs preferentially accumulate methylamines, possibly to counteract urea effects on macromolecules, whereas the freshwater species with lower urea levels accumulate the β-amino acid taurine as the major non-urea osmolyte. A strong correlation (r2=0.84, P<0.001) with a slope of 0.40 was found between muscle urea content and the combined total methylamines plus total β-amino acids, supporting the hypothesis that`non-urea' osmolytes are specifically maintained at an approximately 2:1 ratio with urea in the muscle of elasmobranchs. All species examined had measurable synthetic capacity for betaine in the liver but only one species had detectable TMAO synthetic capacity. We propose a phylogenetic explanation for the distribution of TMAO synthesis in elasmobranchs and suggest that activation of liver betaine aldehyde dehydrogenase, relative to choline dehydrogenase, coincides with betaine accumulation in elasmobranchs. The latter relationship may be important in maintaining methylamine levels during periods of low dietary TMAO intake for species lacking TMAO synthesis.

Publisher

The Company of Biologists

Subject

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

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