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Physiological effects of five different marine natural organic matters (NOMs) and three different metals (Cu, Pb, Zn) on early life stages of the blue mussel ( Mytilus galloprovincialis )

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ABSTRACT

Metals are present in aquatic environments as a result of natural and anthropogenic inputs, and may induce toxicity to organisms. One of the main factors that influence this toxicity in fresh water is natural organic matter (NOM) but all NOMs are not the same in this regard. In sea water, possible protection by marine NOMs is not well understood. Thus, our study isolated marine NOMs by solid-phase extraction from five different sites and characterized them by excitation-emission fluorescence analysis—one inshore (terrigenous origin), two offshore (autochthonous origin), and two intermediate in composition (indicative of a mixed origin). The physiological effects of these five NOMS alone (at 8 mg/L), of three metals alone (copper, lead and zinc at 6 µg Cu/L, 20 µg Pb/L, and 25 µg Zn/L respectively), and of each metal in combination with each NOM, were evaluated in 48-h exposures of mussel larvae. Endpoints were whole body Ca2++Mg2+-ATPase activity, carbonic anhydrase activity and lipid peroxidation. By themselves, NOMs increased lipid peroxidation, Ca2++Mg2+-ATPase, and/or carbonic anhydrase activities (significant in seven of 15 NOM-endpoint combinations), whereas metals by themselves did not affect the first two endpoints, but Cu and Pb increased carbonic anhydrase activities. In combination, the effects of NOMs predominated, with the metal exerting no additional effect in 33 out of 45 combinations. While NOM effects varied amongst different isolates, there was no clear pattern with respect to optical or chemical properties. When NOMs were treated as a single source by data averaging, NOM had no effect on Ca2++Mg2+-ATPase activity but markedly stimulated carbonic anhydrase activity and lipid peroxidation, and there were no additional effects of any metal. Our results indicate that marine NOMs may have direct effects on this model marine organism, as well as protective effects against metal toxicity, and the quality of marine NOMs may be an important factor in these actions.

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The results of an analysis in which all NOMs were considered the same and pooled.(A) Ca2++Mg2+-ATPase activity, (B) carbonic anhydrase activity, and (C) lipid peroxidation of M. galloprovincialis larvae exposed to copper (6 µg/L), lead (20 µg/L), or zinc (25 µg/L) for 48 h at the beginning of development. See the ‘Discussion’ section for details. Mean values represent control condition (Bamfield sea water with no added NOM or metal), average of all NOM exposures (no added metal), and NOMs with additional copper, lead or zinc. No NOM, control condition; NOM, natural organic matter only added; NOM + Cu, natural organic matter plus copper; NOM + Pb, natural organic matter plus lead; NOM + Zn, natural organic matter plus zinc. Bars sharing the same letter are not significantly different. Data are means ± standard error (N = 15 replicates of 2,500 larvae each).
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fig-5: The results of an analysis in which all NOMs were considered the same and pooled.(A) Ca2++Mg2+-ATPase activity, (B) carbonic anhydrase activity, and (C) lipid peroxidation of M. galloprovincialis larvae exposed to copper (6 µg/L), lead (20 µg/L), or zinc (25 µg/L) for 48 h at the beginning of development. See the ‘Discussion’ section for details. Mean values represent control condition (Bamfield sea water with no added NOM or metal), average of all NOM exposures (no added metal), and NOMs with additional copper, lead or zinc. No NOM, control condition; NOM, natural organic matter only added; NOM + Cu, natural organic matter plus copper; NOM + Pb, natural organic matter plus lead; NOM + Zn, natural organic matter plus zinc. Bars sharing the same letter are not significantly different. Data are means ± standard error (N = 15 replicates of 2,500 larvae each).

Mentions: With this background in mind , we re-analysed the current data set considering all NOMs as a single source, thereby pooling all NOM data together (Figs. 5A –5C). The pooled data could not be normalized by standard transformations, so a one-way non-parametric ANOVA was used, followed by multiple comparisons test. As comparison to Figs. 2–4 will indicate, rather different conclusions would be reached. For Ca2++Mg2+-ATPase activity, the combined NOM treatment, alone or in combination with various metals, had no significant effect (Fig. 5A). However for carbonic anhydrase activity (Fig. 5B) and lipid peroxidation (Fig. 5C), the combined NOM treatments resulted in substantial (two-fold) increases relative to the control with no added NOM, and none of the three metals exerted any additional effects—i.e., the influence of NOM alone completely dominated, and the presence and/or nature of the metal did not matter. Clearly, many of the subtle physiological differences seen with individual NOMs were lost. Whether this will matter with respect to the toxicological effects of these metals, as assessed by classic mortality tests, remains to be seen. In terms of enviromental significance, these results suggest that more emphasis should be placed on the site-specific nature and typical concentration of NOM in selecting sites for mussel aquaculture, as well as in interpreting whether metal levels in inshore waters are a threat to these model organisms, which play important roles in setting marine water quality standards.


Physiological effects of five different marine natural organic matters (NOMs) and three different metals (Cu, Pb, Zn) on early life stages of the blue mussel ( Mytilus galloprovincialis )
The results of an analysis in which all NOMs were considered the same and pooled.(A) Ca2++Mg2+-ATPase activity, (B) carbonic anhydrase activity, and (C) lipid peroxidation of M. galloprovincialis larvae exposed to copper (6 µg/L), lead (20 µg/L), or zinc (25 µg/L) for 48 h at the beginning of development. See the ‘Discussion’ section for details. Mean values represent control condition (Bamfield sea water with no added NOM or metal), average of all NOM exposures (no added metal), and NOMs with additional copper, lead or zinc. No NOM, control condition; NOM, natural organic matter only added; NOM + Cu, natural organic matter plus copper; NOM + Pb, natural organic matter plus lead; NOM + Zn, natural organic matter plus zinc. Bars sharing the same letter are not significantly different. Data are means ± standard error (N = 15 replicates of 2,500 larvae each).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5391792&req=5

fig-5: The results of an analysis in which all NOMs were considered the same and pooled.(A) Ca2++Mg2+-ATPase activity, (B) carbonic anhydrase activity, and (C) lipid peroxidation of M. galloprovincialis larvae exposed to copper (6 µg/L), lead (20 µg/L), or zinc (25 µg/L) for 48 h at the beginning of development. See the ‘Discussion’ section for details. Mean values represent control condition (Bamfield sea water with no added NOM or metal), average of all NOM exposures (no added metal), and NOMs with additional copper, lead or zinc. No NOM, control condition; NOM, natural organic matter only added; NOM + Cu, natural organic matter plus copper; NOM + Pb, natural organic matter plus lead; NOM + Zn, natural organic matter plus zinc. Bars sharing the same letter are not significantly different. Data are means ± standard error (N = 15 replicates of 2,500 larvae each).
Mentions: With this background in mind , we re-analysed the current data set considering all NOMs as a single source, thereby pooling all NOM data together (Figs. 5A –5C). The pooled data could not be normalized by standard transformations, so a one-way non-parametric ANOVA was used, followed by multiple comparisons test. As comparison to Figs. 2–4 will indicate, rather different conclusions would be reached. For Ca2++Mg2+-ATPase activity, the combined NOM treatment, alone or in combination with various metals, had no significant effect (Fig. 5A). However for carbonic anhydrase activity (Fig. 5B) and lipid peroxidation (Fig. 5C), the combined NOM treatments resulted in substantial (two-fold) increases relative to the control with no added NOM, and none of the three metals exerted any additional effects—i.e., the influence of NOM alone completely dominated, and the presence and/or nature of the metal did not matter. Clearly, many of the subtle physiological differences seen with individual NOMs were lost. Whether this will matter with respect to the toxicological effects of these metals, as assessed by classic mortality tests, remains to be seen. In terms of enviromental significance, these results suggest that more emphasis should be placed on the site-specific nature and typical concentration of NOM in selecting sites for mussel aquaculture, as well as in interpreting whether metal levels in inshore waters are a threat to these model organisms, which play important roles in setting marine water quality standards.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Metals are present in aquatic environments as a result of natural and anthropogenic inputs, and may induce toxicity to organisms. One of the main factors that influence this toxicity in fresh water is natural organic matter (NOM) but all NOMs are not the same in this regard. In sea water, possible protection by marine NOMs is not well understood. Thus, our study isolated marine NOMs by solid-phase extraction from five different sites and characterized them by excitation-emission fluorescence analysis—one inshore (terrigenous origin), two offshore (autochthonous origin), and two intermediate in composition (indicative of a mixed origin). The physiological effects of these five NOMS alone (at 8 mg/L), of three metals alone (copper, lead and zinc at 6 µg Cu/L, 20 µg Pb/L, and 25 µg Zn/L respectively), and of each metal in combination with each NOM, were evaluated in 48-h exposures of mussel larvae. Endpoints were whole body Ca2++Mg2+-ATPase activity, carbonic anhydrase activity and lipid peroxidation. By themselves, NOMs increased lipid peroxidation, Ca2++Mg2+-ATPase, and/or carbonic anhydrase activities (significant in seven of 15 NOM-endpoint combinations), whereas metals by themselves did not affect the first two endpoints, but Cu and Pb increased carbonic anhydrase activities. In combination, the effects of NOMs predominated, with the metal exerting no additional effect in 33 out of 45 combinations. While NOM effects varied amongst different isolates, there was no clear pattern with respect to optical or chemical properties. When NOMs were treated as a single source by data averaging, NOM had no effect on Ca2++Mg2+-ATPase activity but markedly stimulated carbonic anhydrase activity and lipid peroxidation, and there were no additional effects of any metal. Our results indicate that marine NOMs may have direct effects on this model marine organism, as well as protective effects against metal toxicity, and the quality of marine NOMs may be an important factor in these actions.

No MeSH data available.


Related in: MedlinePlus