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Biomarkers and bioindicators of hypoxia and sediment toxicity in Monoporeia affinis
Stockholm University, Faculty of Science, Department of Applied Environmental Science (ITM).ORCID iD: 0000-0001-9522-5824
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. , p. 35
Keywords [en]
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: urn:nbn:se:su:diva-102828ISBN: 978-91-7447-905-8 (print)OAI: oai:DiVA.org:su-102828DiVA, id: diva2:713398
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: 2018-09-15Bibliographically approved
List of papers
1. Single and combined effects of hypoxia and contaminated sediments on the amphipod Monoporeia affinis in laboratory toxicity bioassays based on multiple biomarkers
Open this publication in new window or tab >>Single and combined effects of hypoxia and contaminated sediments on the amphipod Monoporeia affinis in laboratory toxicity bioassays based on multiple biomarkers
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2010 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 99, no 2, p. 263-274Article in journal (Refereed) Published
Abstract [en]

In estuaries, hypoxic conditions and pollution are among the major factors responsible for the declines in habitat quality, yet little is known about their combined effects on estuarine organisms. In this study, to investigate single and combined effects of hypoxia and contaminated sediment, the Baltic amphipod Monoporeia affinis was exposed for 5-9 days to four different combinations of oxygen conditions (moderate hypoxia vs. normoxia) and contamination (polluted vs. unpolluted sediments) at environmentally realistic levels. To detect oxidative stress, a suite of biomarkers was used - antioxidant enzymes [superoxide dismutases (SOD), catalase (CAT), and glutathione S-transferases (GST)], acetylcholinesterase (AChE), lipid peroxidation status (TBARS concentration), protein carbonyl content (PCC), and DNA strand breakage (DNA-SB). To assay effects at the organism level, we used RNA:DNA ratio as a proxy for growth and metabolic rate and mortality. There were significant increases in CAT and SOD activities and TBARS levels in response to both moderate hypoxia and contaminated sediment, while GST increased and AChE decreased in response to the contamination only. Significant positive correlations were observed among the antioxidant enzymes and between the enzyme activities and TBARS concentration, suggesting a complex response to the oxidative stress. No significant changes in PCC were recorded in any of the treatments. Furthermore, the negative effect of hypoxia on DNA integrity was significant; with frequency of DNA-SB increasing in animals exposed to hypoxia in contaminated sediment. Despite clear effect at the cellular and biochemical levels, no responses at the organism level were observed. Multivariate analyses of the dataset have allowed us to link exposure factors to individual biomarker responses. Of the potential biomarkers assessed in this study, CAT activity was found to be associated with hypoxia, while SOD, GST and AChE activities appear to predict best the effects of exposure to sediments containing several contaminants (e.g. heavy metals, PCBs and PAHs), and TBARS concentration is particularly indicative of combined effects of hypoxia and contamination. In addition to providing new knowledge on the combined effects of multiple stressors on estuarine organisms, the findings of the present study are also important to understand data from biomonitoring studies in the Baltic Sea and in other regions where multiple stress factors co-occur.

Keywords
AChE, Antioxidant enzymes, Contaminated sediments, DNA strand breaks, Hypoxia, Multivariate analysis, Oxidative stress biomarkers
National Category
Natural Sciences
Identifiers
urn:nbn:se:su:diva-52239 (URN)10.1016/j.aquatox.2010.05.005 (DOI)000280510700018 ()
Note
authorCount :7Available from: 2011-01-13 Created: 2011-01-13 Last updated: 2018-01-24Bibliographically approved
2. Exposure to contaminants exacerbates oxidative stress in amphipod Monoporeia affinis subjected to fluctuating hypoxia
Open this publication in new window or tab >>Exposure to contaminants exacerbates oxidative stress in amphipod Monoporeia affinis subjected to fluctuating hypoxia
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2013 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 127, p. 46-53Article 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.

Keywords
AChE, Anticipatory response, Antioxidant enzymes, Glutathione redox status, Lipid peroxidation, Recovery from hypoxia, Reoxygenation, RNA:DNA ratio
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-88269 (URN)10.1016/j.aquatox.2012.01.022 (DOI)000314623100006 ()
Note

AuthorCount:5;

Available from: 2013-03-13 Created: 2013-03-12 Last updated: 2018-01-24Bibliographically approved
3. Embryo aberrations in the amphipod Monoporeia affinis as indicators of toxic pollutants in sediments: A field evaluation
Open this publication in new window or tab >>Embryo aberrations in the amphipod Monoporeia affinis as indicators of toxic pollutants in sediments: A field evaluation
2016 (English)In: Ecological Indicators, ISSN 1470-160X, E-ISSN 1872-7034, Vol. 60, p. 18-30Article in journal (Refereed) Published
Abstract [en]

Reproduction in the amphipod Monoporeia affinis is sensitive to contaminant exposure, and embryo aberrations are used in the Swedish National Monitoring Program to indicate biological effects of contaminants. However, empirical support for a causal relationship between contaminant load and frequency of aberrations is largely based on experimental studies. A field evaluation of aberration frequency in relation to contaminant exposure is required, if we are to use reproductive disorders as indicators of contaminant effects in risk assessment. In this study, we evaluated occurrence of females carrying malformed embryos and frequency of specific embryo aberrations in broods of M. affinis in relation to concentrationsof various pollutants in sediments. Gravid M. affinis and surface sediment were sampled at ten sites in the Gulf of Bothnia located at varying proximity to historical and current polluting point sources. At each site, concentrations of polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and trace and heavy metals in surface sediments were determined. Amphipod fecundity and embryo development status were assayed with regard to morphologically recognizable aberrations (malformed embryos, membrane-damaged embryos, embryos with arrested development and females with dead brood). Our key finding is that different types of embryo aberrations were significantly associated with specific contaminant groups in the sediment. In particular, occurrence of females with embryo malformations was strongly related to elevated concentrations of Cd and PCBs, while females with membrane-damaged embryos occurred at high PAH concentrations. Also, frequency of embryos with arrested development was linked to elevated concentrations of PAHs and metals. Finally, frequency of females carrying dead broods, which was earlier considered to be a hypoxia-induced pathology, was significantly positively related to PAH concentrations. Thus, these reproductive aberrations in M. affinis can serve as contaminant-specific indicators of PCB, PAH and heavy metal exposure in biological effect monitoring.

Keywords
Amphipod Monoporeia affinis, Baltic Sea, Biological effect monitoring, Embryo aberrations, PAHs and PCBs, Metals
National Category
Environmental Sciences
Research subject
Applied Environmental Science
Identifiers
urn:nbn:se:su:diva-122439 (URN)10.1016/j.ecolind.2015.05.058 (DOI)000367407000003 ()
Projects
BONUS+ BEAST project
Funder
EU, FP7, Seventh Framework Programme, 217246Swedish Environmental Protection Agency
Available from: 2015-11-02 Created: 2015-11-02 Last updated: 2018-09-15Bibliographically approved
4. Biomarker-enhanced assessment of reproductive disorders in Monoporeia affinis exposed to contaminated sediment in the Baltic Sea
Open this publication in new window or tab >>Biomarker-enhanced assessment of reproductive disorders in Monoporeia affinis exposed to contaminated sediment in the Baltic Sea
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2016 (English)In: Ecological Indicators, ISSN 1470-160X, E-ISSN 1872-7034, Vol. 63, p. 187-195Article in journal (Refereed) Published
Abstract [en]

Introducing biomarkers into monitoring programs requires understanding of their responses in relation to higher-level biological effects as well as modulating effects of confounding environmental factors. We evaluated relationships between the general toxicity biomarkers (acetylcholinesterase [AChE], lysosomal membrane stability [LMS], oxygen radical absorbance capacity [ORAC]) and reproductive performance (fecundity and embryo aberrations) in the amphipod Monoporeia affinis in the Baltic Sea. To further link biomarker response to contaminant (PCBs, PAHs and metals) levels in the surrounding sediments as well as environmental factors (salinity, bottom depth and total organic carbon in sediments [TOC]), correlation and partial least square regression (PLSR) analyses were applied. The observed contaminants levels were frequently elevated for heavy metals and PAHs, but not PCBs. In the amphipod populations, female ORAC values were positively related to the occurrence of females carrying malformed or membrane-damaged embryos and to the percentage of such embryos in their broods, but also to the fecundity. Female AChE activity was negatively related to the frequency of the membrane-damaged embryos, and positively to the frequency of embryos with arrested development in the broods. Moreover, higher AChE activity and ORAC values in the females occurred at elevated concentrations of metals and PAHs, while there was a negative correlation between embryo ORAC and some PCB congeners. The PLSR models explained over 80% of the variation in the female ORAC and AChE values by variation in contaminant concentrations in combination with environmental variables. Specifically, CB180 and PAM4,9 were identified as negative predictors for ORAC, whereas many PAHs and some metals were positive predictors. The AChE activity was positively related to some metals and negatively to PCBs. In the PLSR models, environmental factors had significant modulating effects, with positive effect of salinity on female ORAC and AChE, and negative effect of TOC on the AChE. The LMS data were less informative, with no apparent relation to any of the contaminants. Linking subcellular responses to the reproduction effects facilitates environmental stress assessment and understanding of the response mechanisms, but also calls for more experimental and field data providing a mechanistic understanding to these linkages.

Keywords
Biomarkers of biological effects of contaminants in sediment, Acetylcholinesterase activity, Antioxidant status, Lysosomal membrane stability, Embryo aberrations, Amphipod Monoporeia affinis, Baltic Sea
National Category
Environmental Sciences
Research subject
Applied Environmental Science
Identifiers
urn:nbn:se:su:diva-126021 (URN)10.1016/j.ecolind.2015.11.024 (DOI)000370906000020 ()
Projects
BONUS + BEAST project
Funder
EU, FP7, Seventh Framework Programme, 217246Swedish Environmental Protection Agency
Available from: 2016-01-22 Created: 2016-01-22 Last updated: 2018-09-15Bibliographically approved

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