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First published online August 8, 2003

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Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host

L. F. Whitehead^* and A. E. Douglas

Department of Biology (Area 2), University of York, Heslington, York, YO10 5YW, UK

View larger version (12K): [in a new window]   Fig. 1. Identification of candidate mobile photosynthetic compounds by metabolite comparison. The algal cells are shown as the shaded oval within the animal (square). Control symbiosis: NaH14CO3 is supplied to the symbiosis under photosynthesizing conditions; the mobile compound(s), M, labelled with 14C, is translocated from the algal cells to the animal, where it is metabolized to compounds A, B and C. Experimental symbiosis: 14C-labelled organic carbon source (S) supplied to the symbiosis under non-photosynthesizing conditions is metabolized to compounds X, Y and Z in the animal. When compounds X, Y and Z are similar to compounds A, B and C, the carbon source S is interpreted to be the same as, or allied to, the mobile compound M.

View larger version (15K): [in a new window]   Fig. 2. Incorporation of NaH14CO3 into the principal chemical fractions of the algal cells (black bars) and anemone tissue (white bars) of A. viridis under photosynthesizing (A) and non-photosynthesizing (B) conditions. Bars represent means ± S.E.M. of 14 and 11 replicates, respectively. TCA, trichloroacetic acid. Multivariate analysis of variance (MANOVA) for data expressed as d.p.m. mg–1 protein after logarithmic transformation: Wilk's for algal cells/animal tissue, F3,40=72.34, P<0.001; for photosynthesizing/non-photosynthesizing conditions, F3,40=103.60, P<0.001; interaction, F3,40=20.43, P<0.001. The full data set did not conform to the assumption of normal distribution and homogeneity, but exclusion of the non-conforming data resulted in no change in significance levels.

View larger version (12K): [in a new window]   Fig. 3. Incorporation of NaH14CO3 into the trichloroacetic acid (TCA)-soluble fractions of the algal cells (A) and animal tissue (B) of A. viridis under non-photosynthesizing (black bars) and photosynthesizing (white bars) conditions, expressed as a percentage of the total radioactivity in the TCA-soluble fraction. Bars represent means ± S.E.M. of 12 and 9 replicates, respectively. Multivariate analysis of variance (MANOVA) for data expressed as d.p.m. mg–1 protein after logarithmic transformation: Wilk's for algal cells/animal tissue, F3,34=53.35, P<0.001; for photosynthesizing/non-photosynthesizing conditions, F3,34=169.25, P<0.001; interaction, F3,34=19.26, P<0.001. The full data set showed homogeneity and closely approached normality.

View larger version (15K): [in a new window]   Fig. 4. Incorporation of 14C into the trichloroacetic acid (TCA)-soluble fractions of A. viridis after incubation in (A) NaH14CO3, as in Fig. 3B, (B) [14C]glucose, (C) [14C]glycerol, (D) [14C]citrate, (E) [14C]fumarate, (F) [14C]malate and (G) [14C]succinate. Experiments were performed over 5 min and, except in A, in the presence of 5 µmol l–1 dichlorophenyl dimethyl urea (DCMU). Data are expressed as a percentage of the total label in the TCA-soluble fraction. Bars (except in A) represent the means ± S.E.M. of 5–9 replicates.

View larger version (10K): [in a new window]   Fig. 5. Incorporation of 14C into the trichloroacetic acid (TCA)-soluble fractions of A. viridis after incubation in (A) NaH14CO3, as in Fig. 3B, (B) [14C]glucose + [14C]succinate, (C) [14C]glucose + [14C]fumarate, (D) [14C]glycerol + [14C]succinate and (E) [14C]glycerol + [14C]fumarate. Experiments were performed over 5 min and, except in A, in the presence of 5 µmol l–1 dichlorophenyl dimethyl urea (DCMU). Data are expressed as a percentage of the total label in the TCA-soluble fraction. Bars (except in A) represent the means ± S.E.M. of 5–6 replicates.