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Maternal Exposure to Cadmium and Manganese Impairs Reproduction and Progeny Fitness in the Sea Urchin Paracentrotus lividus.

Migliaccio O, Castellano I, Cirino P, Romano G, Palumbo A - PLoS ONE (2015)

Bottom Line: The effects of these agents were examined on both P. lividus adults and their offspring following reproductive state, morphology of embryos, nitric oxide (NO) production and differential gene expression.Moreover, we found significant differences in the progeny from females exposed to metals and reared in metal-containing sea water compared to embryos reared in non-contaminated sea water.Overall, these results greatly expanded previous studies on the toxic effects of metals on P. lividus and provided new insights into the molecular events induced in the progeny of sea urchins exposed to metals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

ABSTRACT
Metal contamination represents one of the major sources of pollution in marine environments. In this study we investigated the short-term effects of ecologically relevant cadmium and manganese concentrations (10(-6) and 3.6 x 10(-5) M, respectively) on females of the sea urchin Paracentrotus lividus and their progeny, reared in the absence or presence of the metal. Cadmium is a well-known heavy metal, whereas manganese represents a potential emerging contaminant, resulting from an increased production of manganese-containing compounds. The effects of these agents were examined on both P. lividus adults and their offspring following reproductive state, morphology of embryos, nitric oxide (NO) production and differential gene expression. Here, we demonstrated that both metals differentially impaired the fertilization processes of the treated female sea urchins, causing modifications in the reproductive state and also affecting NO production in the ovaries. A detailed analysis of the progeny showed a high percentage of abnormal embryos, associated to an increase in the endogenous NO levels and variations in the transcriptional expression of several genes involved in stress response, skeletogenesis, detoxification, multi drug efflux processes and NO production. Moreover, we found significant differences in the progeny from females exposed to metals and reared in metal-containing sea water compared to embryos reared in non-contaminated sea water. Overall, these results greatly expanded previous studies on the toxic effects of metals on P. lividus and provided new insights into the molecular events induced in the progeny of sea urchins exposed to metals.

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Related in: MedlinePlus

Morphological analysis of the progeny of P. lividus females exposed to cadmium and manganese.Females were treated for 2 and 9 days with cadmium (Cd) 10−6 M and manganese (Mn) 3.6 x 10−5 M, as described in Materials and Methods. Offspring was reared in sea water (sw) or in the presence of the metal. The development was monitored after 48 hpf. A. Percentage of normal and abnormal plutei; B. Representative pictures of the main abnormalities (bar = 100 μm). Significant differences compared to the control **P<0.01, ***P<0.001; Two-way ANOVA (P<0.05), with Bonferroni’s Post Test. Light grey: normal plutei; dark grey: abnormal plutei. N = 8.
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pone.0131815.g002: Morphological analysis of the progeny of P. lividus females exposed to cadmium and manganese.Females were treated for 2 and 9 days with cadmium (Cd) 10−6 M and manganese (Mn) 3.6 x 10−5 M, as described in Materials and Methods. Offspring was reared in sea water (sw) or in the presence of the metal. The development was monitored after 48 hpf. A. Percentage of normal and abnormal plutei; B. Representative pictures of the main abnormalities (bar = 100 μm). Significant differences compared to the control **P<0.01, ***P<0.001; Two-way ANOVA (P<0.05), with Bonferroni’s Post Test. Light grey: normal plutei; dark grey: abnormal plutei. N = 8.

Mentions: For morphological analysis, we considered as normal plutei cone-shaped larvae with four fully developed arms and complete skeletal rods, whereas larvae with defects in arm and skeleton elongation and developmentally delayed were named abnormal, as previously described [10]. The exposure of females to both cadmium and manganese resulted in an increase in the percentage of abnormal plutei in the progeny (Fig 2A). In particular, the offspring of females exposed to cadmium 10−6 M reared in sea water showed 78±4.2% and 92±3.7% of abnormal plutei after 2 and 9 days respectively (Fig 2A), compared to the respective controls (7±1.2 and 9±0.73%). Defects were found in both arms and apex. The arms appeared often malformed or absent, whereas skeletal rods of the apex were folded, crossed or separated (Fig 2B). An increase in the number and type of abnormalities was found in the offspring of exposed females reared in the presence of cadmium with a percentage of abnormal plutei of 93±7.23 and 99±0.54% after 2 and 9 days, respectively, compared to controls in the absence of cadmium (Fig 2A). Larvae appeared severely affected by metal treatment with high percentage of gastrula and prism-like stages and arrested embryos (Fig 2B). The exposure of females to manganese 3.6 x 10−5 M also caused abnormality in the offspring. In details, the embryos generated from those females and reared in sea water reached values of abnormalities of 29±3.23 and 39±4.65 after 2 and 9 days, respectively (Fig 2A), compared to the respective controls, offspring of females kept during the whole experimental period in sea water without metal. The abnormalities regarded especially the arms which appeared shorter than normal or malformed and the skeletal rods of the apex which were crossed or separated (Fig 2B). As in the case of cadmium treatment, an increase in the percentage and type of abnormalities was found in embryos reared in the presence of manganese which reached the values of 42±2.12 and 75±1.9% after 2 and 9 days, respectively, compared to controls. Larvae appeared much smaller in size and defects were found in both arms and apex (Fig 2B).


Maternal Exposure to Cadmium and Manganese Impairs Reproduction and Progeny Fitness in the Sea Urchin Paracentrotus lividus.

Migliaccio O, Castellano I, Cirino P, Romano G, Palumbo A - PLoS ONE (2015)

Morphological analysis of the progeny of P. lividus females exposed to cadmium and manganese.Females were treated for 2 and 9 days with cadmium (Cd) 10−6 M and manganese (Mn) 3.6 x 10−5 M, as described in Materials and Methods. Offspring was reared in sea water (sw) or in the presence of the metal. The development was monitored after 48 hpf. A. Percentage of normal and abnormal plutei; B. Representative pictures of the main abnormalities (bar = 100 μm). Significant differences compared to the control **P<0.01, ***P<0.001; Two-way ANOVA (P<0.05), with Bonferroni’s Post Test. Light grey: normal plutei; dark grey: abnormal plutei. N = 8.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4488381&req=5

pone.0131815.g002: Morphological analysis of the progeny of P. lividus females exposed to cadmium and manganese.Females were treated for 2 and 9 days with cadmium (Cd) 10−6 M and manganese (Mn) 3.6 x 10−5 M, as described in Materials and Methods. Offspring was reared in sea water (sw) or in the presence of the metal. The development was monitored after 48 hpf. A. Percentage of normal and abnormal plutei; B. Representative pictures of the main abnormalities (bar = 100 μm). Significant differences compared to the control **P<0.01, ***P<0.001; Two-way ANOVA (P<0.05), with Bonferroni’s Post Test. Light grey: normal plutei; dark grey: abnormal plutei. N = 8.
Mentions: For morphological analysis, we considered as normal plutei cone-shaped larvae with four fully developed arms and complete skeletal rods, whereas larvae with defects in arm and skeleton elongation and developmentally delayed were named abnormal, as previously described [10]. The exposure of females to both cadmium and manganese resulted in an increase in the percentage of abnormal plutei in the progeny (Fig 2A). In particular, the offspring of females exposed to cadmium 10−6 M reared in sea water showed 78±4.2% and 92±3.7% of abnormal plutei after 2 and 9 days respectively (Fig 2A), compared to the respective controls (7±1.2 and 9±0.73%). Defects were found in both arms and apex. The arms appeared often malformed or absent, whereas skeletal rods of the apex were folded, crossed or separated (Fig 2B). An increase in the number and type of abnormalities was found in the offspring of exposed females reared in the presence of cadmium with a percentage of abnormal plutei of 93±7.23 and 99±0.54% after 2 and 9 days, respectively, compared to controls in the absence of cadmium (Fig 2A). Larvae appeared severely affected by metal treatment with high percentage of gastrula and prism-like stages and arrested embryos (Fig 2B). The exposure of females to manganese 3.6 x 10−5 M also caused abnormality in the offspring. In details, the embryos generated from those females and reared in sea water reached values of abnormalities of 29±3.23 and 39±4.65 after 2 and 9 days, respectively (Fig 2A), compared to the respective controls, offspring of females kept during the whole experimental period in sea water without metal. The abnormalities regarded especially the arms which appeared shorter than normal or malformed and the skeletal rods of the apex which were crossed or separated (Fig 2B). As in the case of cadmium treatment, an increase in the percentage and type of abnormalities was found in embryos reared in the presence of manganese which reached the values of 42±2.12 and 75±1.9% after 2 and 9 days, respectively, compared to controls. Larvae appeared much smaller in size and defects were found in both arms and apex (Fig 2B).

Bottom Line: The effects of these agents were examined on both P. lividus adults and their offspring following reproductive state, morphology of embryos, nitric oxide (NO) production and differential gene expression.Moreover, we found significant differences in the progeny from females exposed to metals and reared in metal-containing sea water compared to embryos reared in non-contaminated sea water.Overall, these results greatly expanded previous studies on the toxic effects of metals on P. lividus and provided new insights into the molecular events induced in the progeny of sea urchins exposed to metals.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

ABSTRACT
Metal contamination represents one of the major sources of pollution in marine environments. In this study we investigated the short-term effects of ecologically relevant cadmium and manganese concentrations (10(-6) and 3.6 x 10(-5) M, respectively) on females of the sea urchin Paracentrotus lividus and their progeny, reared in the absence or presence of the metal. Cadmium is a well-known heavy metal, whereas manganese represents a potential emerging contaminant, resulting from an increased production of manganese-containing compounds. The effects of these agents were examined on both P. lividus adults and their offspring following reproductive state, morphology of embryos, nitric oxide (NO) production and differential gene expression. Here, we demonstrated that both metals differentially impaired the fertilization processes of the treated female sea urchins, causing modifications in the reproductive state and also affecting NO production in the ovaries. A detailed analysis of the progeny showed a high percentage of abnormal embryos, associated to an increase in the endogenous NO levels and variations in the transcriptional expression of several genes involved in stress response, skeletogenesis, detoxification, multi drug efflux processes and NO production. Moreover, we found significant differences in the progeny from females exposed to metals and reared in metal-containing sea water compared to embryos reared in non-contaminated sea water. Overall, these results greatly expanded previous studies on the toxic effects of metals on P. lividus and provided new insights into the molecular events induced in the progeny of sea urchins exposed to metals.

No MeSH data available.


Related in: MedlinePlus