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Toxigenic effects of two benthic diatoms upon grazing activity of the sea urchin: morphological, metabolomic and de novo transcriptomic analysis.
Ruocco N
,
Costantini S
,
Zupo V
,
Lauritano C
,
Caramiello D
,
Ianora A
,
Budillon A
,
Romano G
,
Nuzzo G
,
D'Ippolito G
,
Fontana A
,
Costantini M
.
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Diatoms are unicellular algae playing a key role as photosynthetic organisms in the world''s ocean food webs. The chemical ecology of planktonic diatoms is well documented, but few studies have reported on the effects of benthic diatoms on their consumers, also due to difficulties in the collection, quantification and massive culturing of benthic species. Here for the first time we investigate the effects of feeding on two abundantly occurring benthic diatoms, Nanofrustulum shiloi and Cylindrotheca closterium, isolated from the leaves of the seagrass Posidonia oceanica, on the sea urchin Paracentrotus lividus. Adult P. lividus were fed for one month on diets of either one of the two diatoms and on the green alga Ulva rigida, used as a feeding control. By combining morphological, metabolomic and de novo transcriptomic approaches, we demonstrate toxigenic effect on embryos generated by females fed with these benthic diatoms. Furthermore, chemical analysis reveal the presence of polyunsaturated aldehydes only for N. shiloi, and a high production of other oxylipins (cytotoxic compounds on their grazers and on cancer cell lines) for both diatoms, including some additional peaks not correlated to the canonic oxylipins commonly observed in planktonic diatoms. These findings open new perspectives in the study of diatom secondary metabolites influencing their grazers.
Figure 1. Scanning electron micrographs (SEM) of (A) C. closterium and (B) N. shiloi isolates. Scale bar = 1 μm.
Figure 3. OPLS-DA (A) and Loading (B) plots (where the metabolites increased or decreased) of aqueous extracts from gonad tissues from adults sea urchin P. lividus after one month of feeding with U. rigida (used ad feeding control, reported as CTRL), N. shiloi (reported as TREAT1) and C. closterium (reported as TREAT2).
Figure 4. OPLS-DA (A) and Loading plots of (B) lipids and (C) fatty acids from lipophilic extracts of gonad tissues from adults sea urchin P. lividus after one month of feeding with U. rigida (used as feeding control, reported as CTRL), N. shiloi (reported as TREAT1) and C. closterium (reported as TREAT2).
Figure 5. Blastx top hit species distribution of matches with known sequences.
Figure 6. Overrepresented GO terms of sea urchin plutei after feeding experiments with the two benthic diatoms, N. shiloi and C. closterium, in comparison with U. rigida (feeding control), in the three major functional categories: biological process (BP), molecular function (MF) and cellular component (CC). The tree bars represent: black bar “control versus N. shiloi”, white bar “control versus C. closterium” and grey bar “N. shiloi versus C. closterium”.
Figure 7. Synopsis of the patterns of up- and downregulation of different classes of genes in sea urchin embryos spawned from adults fed for one month with the two benthic diatoms N. shiloi and C. closterium (see also Supplementary Table S4 for the values and Supplementary Figs S7–S8).
Figure 8. Venn diagrams considering upregulated genes and downregulated genes comparing the groups “control (U. rigida, feeding control) versus N. shiloi”, “control versus C. closterium” and “N. shiloi versus C. closterium”. N. shiloi and C. closterium induced an increase in the expression of 85 (11.6%) and 453 (61.7%) genes, respectively, compared to the control diet (U. rigida); they also induced the downregulation of 94 (27.9%) and 112 (33.2%) genes, respectively. The two diatoms had a few common targets (see also Supplementary Table S5 for the names of the common genes). In fact, in the case of up-regulated genes we found 19 common genes (2.6%) comparing the groups “control versus N. shiloi” and “control versus C. closterium”; 4 common genes (0.5%) comparing the groups “control versus N. shiloi”, “control versus C. closterium” and “N. shiloi versus C. closterium”; 5 common genes (0.7%) “control versus N. shiloi” and “N. shiloi versus C. closterium”; 65 common genes (8.9%) comparing “control versus C. closterium” and “N. shiloi versus C. closterium”. Considering the down-regulated genes, we found 5 common genes (1.5%) comparing the groups “control versus N. shiloi” and “control versus C. closterium”; 2 common genes (0.6%) comparing the groups “control versus N. shiloi”, “control versus C. closterium” and “N. shiloi versus C. closterium”; 3 common genes (0.9%) “control versus N. shiloi” and “N. shiloi versus C. closterium”; 10 common genes (3.0%) comparing “control versus C. closterium” and “N. shiloi versus C. closterium”.
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