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Sci Rep
2016 May 19;6:26086. doi: 10.1038/srep26086.
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Subtle reproductive impairment through nitric oxide-mediated mechanisms in sea urchins from an area affected by harmful algal blooms.
Migliaccio O
,
Castellano I
,
Di Cioccio D
,
Tedeschi G
,
Negri A
,
Cirino P
,
Romano G
,
Zingone A
,
Palumbo A
.
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The health of the sea urchin Paracentrotus lividus, a key species in the Mediterranean Sea, is menaced by several pressures in coastal environments. Here, we aimed at assessing the reproductive ability of apparently healthy P. lividus population in a marine protected area affected by toxic blooms of Ostreospsis cf. ovata. Wide-ranging analyses were performed in animals collected prior to and during the bloom, as well as at several times thereafter, during the reproductive season. Adults showed a low fertilization rate, along with high nitric oxide (NO) levels in the gonads and the nitration of the major yolk protein toposome, which is an important player in sea urchin development. Serious developmental anomalies were observed in the progeny, which persist several months after the bloom. NO levels were high in the different developmental stages, which also showed variations in the transcription of several genes that were found to be directly or indirectly modulated by NO. These results highlight subtle but important reproductive flaws transmitted from the female gonads to the offspring with the NO involvement. Despite a recovery along time after the bloom, insidious damages can be envisaged in the local sea urchin population, with possible reverberation on the whole benthic system.
Figure 2. Gene expression of the progenies of P. lividus from the Gaiola MPA.Eggs from sea urchin females collected at Gaiola site some months after O. cf. ovata bloom, i.e. in October, February and April, were fertilized with mixed sperm from 3 males from the control site of Castel dell’Ovo. Different developmental stages (early blastula EB, swimming blastula SB, prism Pr and pluteus Pl) were examined for the expression of selected genes by Real Time qPCR. Data are reported as fold difference in the expression levels of the analyzed genes, compared to control (mean ± SEM) represented by offspring of females collected from Castel dell’Ovo. Fold differences greater than ±2 (horizontal guidelines) were considered significant.
Figure 4. NO-modulated development of the progenies of P. lividus from the Gaiola MPA.Offspring of sea urchins collected at Gaiola site after O. cf. ovata bloom (October, February and April) were examined for NO concentration (A) and gene expression (B). (A) NO levels determined as nitrite by the Griess assay from animals collected at Gaiola site and at the control site Castel dell’Ovo. Data are reported as mean ± SEM. *Significant difference compared to the control: **P < 0.01, ***P < 0.001. Kruskal-Wallis test (K/S) with Mann-Whitney pairwise post hoc test (P < 0.05). N = 6. (B) The expression of the genes found to be altered at Gaiola site, as shown in Fig. 2, was followed at the different developmental stages (early blastula EB, swimming blastula SB, prism Pr and pluteus Pl) by Real Time qPCR under low NO levels in the presence of 10−4 M TRIM. Data are reported as fold difference compared to control (mean ± SEM), offspring of females collected from Gaiola and reared in the absence of TRIM. Fold differences greater than ±2 (see horizontal guidelines at values of 2 and −2) were considered significant.
Figure 5. Gene expression of the progenies of P. lividus from the control site Castel dell’Ovo under induced high levels of NO.The expression of the genes found to be altered by TRIM treatment in Gaiola offspring, as shown in Fig. 4, was followed by Real Time qPCR in the different developmental stages (early blastula EB, swimming blastula SB, prism Pr and pluteus Pl) of the offspring from the control site reared under high NO levels in the presence of 4 × 10−5 M sperNO. Data are reported as a fold difference (mean ± SEM) in the expression levels of the analyzed genes compared to controls (mean ± SEM), the offspring of females collected from Castel dell’Ovo and reared in the presence of spermine, the product derived from sperNO after NO release, respectively. Fold differences greater than ±2 (see horizontal guidelines at values of 2 and −2) were considered significant.
Figure 6. Schematic summary of the NO involvement in the modulation of gene expression in the offspring development of P. lividus from the MPA Gaiola.The expression of selected genes was examined in natural conditions at Gaiola site, where sea urchin progeny was characterized by high endogenous NO levels, in comparison to the progeny of animals from the control site to which NO was added experimentally. (A) Genes showing consistent regulation patterns in the two conditions, suggesting a direct regulation of NO (B) Genes showing opposite regulation patterns, suggesting an indirect regulation of NO.
Figure 7. Proposed model of the processes involving P. lividus at the Gaiola MPA.Sea urchins subjected to intense summer blooms of Ostreopsis cf. ovata show alterations in their gonads and in several aspects of the reproductive process, as well as in the development of their progeny following the bloom. In July, the toxic agent, presumably acting through the ingestion of the epiphytic microalgae living on macroalgae as epiphytes, causes toxin accumulation and toposome nitration in the gonads of the immature sea urchin population. In the following seasons, toposome nitration persists in the mature gonads, while fertilization and developmental processes show impairments that decrease over time, yet not attaining a complete recovery. The expression of several marker genes is also altered in the sea urchin progeny, as a consequence of the increased NO levels. The reproductive impairment likely affects the recruitment potential of this key-species, with foreseeable consequences on adult populations and on the whole benthic ecosystem.
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