First published online February 15, 2006
Journal of Experimental Biology 209, 860-870 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02055
The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species
Jason R. Treberg1,*,
Ben Speers-Roesch2,
Peter M. Piermarini3,
Yuen K. Ip4,
James S. Ballantyne2 and
William R. Driedzic1
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
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Fig. 1. The separation of common organic osmolytes using a Waters SugarPak column,
as described in the Materials and methods. (B) Separation of most major
osmolytes common in elasmobranch muscle, as well as several other common
organic osmolytes, using a mobile phase of 500 mg l–1
Ca-EDTA. (A) Enlargement of the region of response from the approximate
retention times of 12.5 to 21 min, using different concentrations of Ca-EDTA
as the mobile phase. Note the retention times of glycine and alanine are
reduced as the concentration of Ca-EDTA decreases.
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Fig. 2. Muscle organic osmolyte contents (µmol g–1) in marine,
euryhaline and freshwater elasmobranchs. Values are mean ± s.e.m. and
N=6 (C. punctatum), 4 (L. ocellata), 4 (L.
erinacea), 6 (T. lymma), 5 (D. Sabina), 7 (all
compounds except TMAO, where N=5) in H. signifer acclimated
to 50% seawater, 10 (all compounds except TMAO, where N=9) in H.
signifer acclimated to freshwater (FW), 7 (all compounds except TMAO,
where N=5) in P. motoro.
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Fig. 3. Muscle urea content (µmol g–1) with the total
methylamine and ß-amino acid (non-urea osmolytes) contents (µmol
g–1) in marine, euryhaline species in freshwater (FW) and
freshwater elasmobranchs. Values are mean ± s.e.m. and N=6
(C. punctatum), 4 (L. ocellata), 4 (L. erincea), 6
(T. lymma), 5 (D. sabina), 5 (methylamines) and 7
(ß-amino acids) in H. signifer acclimated to 50% seawater, 9
(methylamines) and 10 (ß-amino acids) in H. signifer acclimated
to freshwater, 5 (methylamines) and 7 (ß-amino acids) in P.
motoro.
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Fig. 4. Relationship of muscle urea content with total methylamine (closed symbols,
solid line) or combined total of methylamine and ß-amino acid (open
symbols, broken line) content in marine (circles), euryhaline species in
freshwater (FW) (triangles) and freshwater elasmobranchs (squares). Values are
mean ± s.e.m. and N values are the same those for total
methylamine contents in Fig. 4. The regressions are statistically significant
(total methylamines, P<0.01; total methylamines plus ß-amino
acids, P<0.001).
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Fig. 5. Relationship between liver enzyme activities of betaine synthesis (nmol
min–1 mg protein–1) and the accumulation of
betaine in the muscle (µmol g–1) of marine, euryhaline and
freshwater elasmobranchs. Figures are for muscle betaine and (A) liver choline
dehydrogenase activity (ChoDH), (B) liver betaine aldehyde dehydrogenase
(BADH), (C) ratio of BADH/ChoDH. The regression equations for A and B are only
for species able to survive in full-strength seawater (marine and euryhaline)
while the equation in C is for all species; for C, the equation (not shown)
for those species able to survive under marine conditions is not significantly
different from the regression equation including all species. Data are taken
from Table 1 and
Fig. 3.
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Fig. 6. Summary of the capacity for the oxidation of trimethylamine to
trimethylamine oxide (TMAO), indicative of TMAO synthetic capacity, in
chondrichthyian fishes (elasmobranchs and chimaeras) arranged
phylogenetically. The tree is simplified from Winchell et al.
(Winchell et al., 2004 ) and,
for simplicity, orders where no data on the oxidation of trimethylamine are
available have not been included. *TMAO synthesis was assessed in
vitro;  TMAO synthesis was assessed by in vivo
conversion of labeled precursor; –, below limits of detection or
questionable synthetic capacity; +, significant TMAO synthesis present. Values
in parentheses indicate the source of data:
1Baker et al., 1963;
2Goldstein et al.,
1967; 3Goldstein and
Funkenhouser, 1972;
4Goldstein and Dewitt-Harley,
1973; 5Treberg and
Driedzic, 2002; 6present study.
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© The Company of Biologists Ltd 2006
