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Exposure to contaminants exacerbates oxidative stress in amphipod Monoporeia affinis subjected to fluctuating hypoxia
Stockholm University, Faculty of Science, Department of Applied Environmental Science (ITM).
Stockholm University, Faculty of Science, Department of Applied Environmental Science (ITM).
Stockholm University, Faculty of Science, Department of Applied Environmental Science (ITM).
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2013 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 127, 46-53 p.Article in journal (Refereed) Published
Abstract [en]

Fitness and survival of an organism depend on its ability to mount a successful stress response when challenged by exposure to damaging agents. We hypothesized that co-exposure to contaminants may exacerbate oxidative stress in hypoxia-challenged benthic animals compromising their ability to recover upon reoxygenation. This was tested using the amphipod Monoporeia affinis exposed to hypoxia followed by reoxygenation in sediments collected in polluted and pristine areas. In both sediment types, oxygen radical absorbance capacity (ORAC) and antioxidant enzyme activities [superoxide dismutase (SOD) and catalase (CAT)] increased during hypoxia, suggesting that M. affinis has a strategy of preparation for oxidative stress that facilitates recovery after a hypoxic episode. Exposure to contaminants altered this anticipatory response as indicated by higher baselines of ORAC and SOD during hypoxia and no response upon reoxygenation. This coincided with significantly elevated oxidative damage evidenced by a marked reduction in glutathione redox status (ratio of reduced GSH/oxidized GSSG) and an increase in lipid peroxidation (TSARS levels). Moreover, RNA:DNA ratio, a proxy for protein synthetic activity, decreased in concert with increased TBARS, indicating a linkage between oxidative damage and fitness. Finally, inhibited acetylcholinesterase (AChE) activity in animals exposed to contaminated sediments suggested a neurotoxic impact, whereas significant correlations between AChE and oxidative biomarkers may indicate connections with redox state regulation. The oxidative responses in pristine sediments suggested a typical scenario of ROS production and removal, with no apparent oxidative damage. By contrast, co-exposure to contaminants caused greater increase in antioxidants, lipid peroxidation, and slowed recovery from hypoxia as indicated by CAT, GSH/GSSG, TBARS and AChE responses. These results support the hypothesized potential of xenobiotics to hamper ability of animals to cope with fluctuating hypoxia. They also emphasize the importance of understanding interactions between antioxidant responses to different stressors and physiological mechanisms of oxidative damage.

Place, publisher, year, edition, pages
2013. Vol. 127, 46-53 p.
Keyword [en]
AChE, Anticipatory response, Antioxidant enzymes, Glutathione redox status, Lipid peroxidation, Recovery from hypoxia, Reoxygenation, RNA:DNA ratio
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-88269DOI: 10.1016/j.aquatox.2012.01.022ISI: 000314623100006OAI: oai:DiVA.org:su-88269DiVA: diva2:610812
Note

AuthorCount:5;

Available from: 2013-03-13 Created: 2013-03-12 Last updated: 2017-12-06Bibliographically approved
In thesis
1. Biomarkers and bioindicators of hypoxia and sediment toxicity in Monoporeia affinis
Open this publication in new window or tab >>Biomarkers and bioindicators of hypoxia and sediment toxicity in Monoporeia affinis
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Two of the most pressing environmental problems in the Baltic Sea are pollution and oxygen deficiency. The aim of this doctoral thesis was to evaluate a set of biomarkers and reproductive variables in the amphipod Monoporeia affinis to test their suitability as indicators of exposure to contaminants and hypoxia. In Paper I and Paper II, field-sampled M. affinis were exposed to varying oxygen conditions in combination with contaminated or reference sediment. Paper I showed that the combined effect of hypoxia and contaminants induced larger increases in antioxidant enzyme activities and higher levels of damaged lipids, resulting from oxidative stress, than single-stress treatments. The biomarkers AChE and GST responded only to the contaminant exposure. Paper II demonstrated that M. affinis can prepare against oxidative stress that facilitates recovery after a hypoxic episode, but that exposure to contaminants altered this response and resulted in higher baselines of antioxidants during hypoxia and no response upon reoxygenation. Paper III linked the occurrence of different embryo aberrations in M. affinis to concentrations of PAHs, PCBs and metals in sediments in the field. A key finding is that different types of embryo aberrations were associated with specific contaminant groups in the sediment. Paper IV addressed the link between biomarkers and bioindicators in M. affinis and found positive associations between increased antioxidant capacity in females and higher occurrence and frequencies of malformed and membrane-damaged embryos. AChE inhibition was linked to frequency of membrane-damaged embryos. Links between biomarker response and fecundity and embryo developmental stage were also established. Further, a large part of the variation in female antioxidant capacity and AChE activity could be explained by variation in concentrations of different metals, PAHs and PCB congeners, in combination with the environmental variables salinity, depth and sediment TOC.

Place, publisher, year, edition, pages
Stockholm: Department of Applied Environmental Science (ITM), Stockholm University, 2014. 35 p.
Keyword
Biomarkers, Bioindicators, Embryo aberrations, Hypoxia, Contaminated sediment, PAHs, PCBs, Metals, Baltic Sea, Amphipods, Monoporeia affinis
National Category
Environmental Sciences
Research subject
Applied Environmental Science
Identifiers
urn:nbn:se:su:diva-102828 (URN)978-91-7447-905-8 (ISBN)
Public defence
2014-05-28, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14, Stockholm, 10:00 (Swedish)
Opponent
Supervisors
Note

At the time of the doctoral defence the following papers were unpublished and had a status as follows: Paper 3: Manuscript; Paper 4: Manuscript.

Available from: 2014-05-06 Created: 2014-04-22 Last updated: 2014-04-25Bibliographically approved
2. Improved environmental monitoring and assessment: Establishing links between effects of chemical pollution at different levels of biological organization in a Baltic Sea bioindicator species (Monoporeia affinis)
Open this publication in new window or tab >>Improved environmental monitoring and assessment: Establishing links between effects of chemical pollution at different levels of biological organization in a Baltic Sea bioindicator species (Monoporeia affinis)
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

A large number of chemicals enters the marine environment via atmospheric deposition, run-off, rivers and streams, industrial effluents and municipal wastewater. To understand how chemicals affect environmental health, monitoring and assessment approaches need to combine physical, chemical and biological effect parameters from different levels of biological organization. Embryo aberrations and reproductive success in the Baltic Sea key species Monoporeia affinis have been linked to various stressors, including chemicals, and have been applied as a bioindicator of chemical pollution since the 1970s. The current thesis aimed to improve this bioindicator by linking effects at different levels of biological organization. Understanding how effects are linked, from sub-cellular effects, to decreased organism fitness and further on to populations, will improve the ability to give early warnings and understand risks that an ecosystem faces. Paper I links point sources of chemical pollution to embryo aberrations, and shows that effects can be detected 20-30 km from point sources. Paper II demonstrates on a sub-cellular level how M. affinis´ ability to cope with hypoxia is adversely affected by chemical stress, and how it could decrease fitness. Paper III link sub-cellular effects to embryo aberrations and suggests a mechanistic link between oxidative stress and embryo aberrations. Paper III also shows that sub-cellular effects respond more distinctly compared to fecundity, survival and embryo aberrations and can thus improve the ability to detect stress at an early stage. In Paper IV, a population model was developed, which shows that populations could be severely affected if levels of embryo aberrations persist at levels commonly observed in Baltic Sea. This thesis contributes to a more holistic understanding of how chemical pollution affects M. affinis, thereby improving our ability to early detect negative effects and understand potential risks that the Baltic Sea faces.

Place, publisher, year, edition, pages
Stockholm: Department of Environmental Science and Analytical Chemistry, Stockholm University, 2015. 32 p.
Keyword
Environmental health assessment, environmental monitoring, chemical pollution, hypoxia, bioindicators, biomarkers, teratogenicity, embryo toxicity, oxidative stress, acetylcholine esterase. Monoporeia affinis, Baltic Sea
National Category
Biological Sciences
Research subject
Applied Environmental Science
Identifiers
urn:nbn:se:su:diva-111067 (URN)978-91-7649-078-5 (ISBN)
Public defence
2015-01-30, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14, Stockholm, 10:00 (English)
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2015-01-08 Created: 2014-12-21 Last updated: 2014-12-30Bibliographically approved

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