Ammonium excretion by a symbiotic sponge supplies the nitrogen requirements of its rhodophyte partner
Simon K. Davy1,*,
Donelle A. Trautman1,2,
Michael A. Borowitzka2 and
Rosalind Hinde1
1 School of Biological Sciences, A08, University of Sydney, New South Wales
2006, Australia
2 School of Biological Sciences and Biotechnology, Murdoch University,
Murdoch, Western Australia 6150, Australia
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Fig. 1. Uptake of dissolved inorganic nitrogen from sea water by the
Haliclona—Ceratodictyon symbiosis. (A) Uptake of ammonium from
sea water spiked with 20 µmol l-1 NH4Cl, when
branches were incubated in the light (N=3). (B) Uptake of nitrate
from `normal', unspiked sea water, when branches were incubated in the light
(N=5). Values are means ± S.D. Ammonium and nitrate
concentrations in sea water without the association did not change
significantly over time (one-way analysis of variance, P>0.2,
N=3 for both nutrients), with ammonium concentrations being
20.84±0.83 µmol l-1 and 18.84±2.89 µmol
l-1 and nitrate concentrations being 2.10±0.27 µmol
l-1 and 1.36±0.43 µmol l-1 at the start and
end of the experiments, respectively.
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Fig. 2. The influence of nutrient enrichment in the field on the physiology of the
Haliclona—Ceratodictyon symbiosis. (A) The maximum rate of
gross photosynthesis (Pmax). (B) The dark respiration rate
(R). Treated branches (N=10) were placed in either sea water
plus 10 µmol l-1 NaNO3 (`Nitrate') or sea water only
(`Control') for 24 h. Treated branches were compared with branches harvested
directly from the field (`Freshly collected'). Values are means ± S.D.
Measurements obtained in laboratory-based experiments were similar to those
obtained in the field experiments and are therefore not shown.
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Fig. 3. Ammonium flux from the Haliclona—Ceratodictyon symbiosis in
darkness. Branches had been pre-incubated in darkness for 4 h (filled
circles), 8 h (open circles) or 24 h (filled triangles) (N=5 for each
time point). Values are means ± S.D.
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Fig. 4. Nitrogen budget for the Haliclona—Ceratodictyon symbiosis.
The budget incorporates the maximum ammonium release rate in darkness (0.110
mg Ng-1 dry mass day-1), the growth rate of the
association (0.83% day-1, as reported by
Trautman et al., 2000 ), the
alga:sponge biomass ratio (70%:30% alga:sponge) and the nitrogen content of
the two partners (alga, 1.9%; sponge, 6.7%; both on a dry mass basis).
Nitrogen that is surplus to the growth requirements of the alga is assumed to
be translocated back to the sponge, and the budget is balanced by the presumed
acquisition of nitrogen from the ambient environment. Abbreviations: dissolved
inorganic nitrogen (DIN); dissolved organic nitrogen (DON); particulate
organic nitrogen (PON). Biomass units are mg nitrogen g-1 dry mass
of the whole association. Flux units are mg nitrogen g-1 dry mass
of the whole association per day. Solid arrows are used for proven fluxes
(quantified directly except where stated as `derived'), while broken arrows
are used for possible fluxes.
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Fig. 5. Nitrogen status of Ceratodictyon spongiosum in the field and in
culture, as measured by the enhancement of dark carbon fixation in the
presence of ammonium (20µmol l-1 NH4Cl). C.
spongiosum was first cultured in 100µmol l-1
NH4Cl for 3 weeks and then either deprived of nitrogen for up to 6
weeks or provided with 100µmol l-1 NH4Cl for a
further 6weeks (+NH4+). Freshly collected C.
spongiosum (`Field') was analysed within 24h. N=3 for each time
point/condition. Values are means ± S.D. FSW, filtered sea water
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© The Company of Biologists Ltd 2002
