Biomarkers for assessing marine pollution effects

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Biomonitoring of marine pollution

Biomonitoring uses organisms and their biological responses to detect pollutant exposure and harmful biological effects, including effects of substances or mixtures that may escape chemical monitoring.

The Coastal Wiki articles on this subject provide complementary perspectives:


Effects of diverse toxic substances on different marine animals are described in articles in the category ecotoxicology.


Introduction

A biomarker is a measurable biological characteristic or response that indicates exposure to pollutants or their biological effects. Biomarkers can be measured at molecular, biochemical, cellular, physiological or behavioral level. Some biomarkers respond mainly to particular classes of contaminants, whereas others indicate more general physiological stress or damage. Their interpretation therefore requires information on contaminant exposure and on environmental and biological factors that can also influence the response.

Biomarkers are generally measured in selected bioindicator or sentinel species. Suitable bioindicators are readily sampled, sufficiently abundant and show a well-characterized response to the pollutants or effects being monitored. Mussels and other bivalves are widely used in coastal biomonitoring because they are sessile, filter large volumes of water and accumulate many contaminants over time. Their limited mobility allows observed contaminant burdens and biomarker responses to be related relatively closely to local environmental conditions. Besides monitoring indigenous mussel populations, active biomonitoring can be carried out by transplanting or caging mussels at selected sites, which allows greater control over their origin and exposure period.[1]

Fish provide complementary information. They occupy higher trophic levels, accumulate contaminants through both water and food, and permit assessment of a wide range of biochemical, physiological and pathological effects. In wild fish, however, the location and duration of previous exposure are often uncertain, which makes it difficult to relate biomarker responses to a specific pollution source. Active biomonitoring with caged fish can overcome this limitation by exposing animals of known origin at selected sites for a defined period.[2][3]

Different bioindicator species therefore provide complementary information rather than interchangeable measures of pollution. Modern biomonitoring programmes commonly combine biomarkers from several sentinel species with measurements of contaminant concentrations and relevant environmental conditions.[4]

Biomarkers are commonly classified according to whether they indicate exposure, biological effects or susceptibility to adverse effects. The biomarkers considered in this article mainly belong to the first two groups. Biomarkers of biological effect include indicators of cellular and physiological stress, genotoxicity and reproductive impairment.

Biomarkers of exposure

Biomarker Mainly indicates
metallothioneins [5][6] Exposure/adaptation to certain metals
Mixed-function oxygenase [7][8][9][10] / CYP1A / EROD activity [11] Exposure to AhR-active organic contaminants such as certain PAHs and planar halogenated compounds
Acetylcholinesterase inhibition[12][13] Exposure to neurotoxic compounds that inhibit cholinesterase activity
PAH metabolites in fish bile Recent uptake of PAHs

For example, metallothioneins (MTs) are small proteins present inside cells that bind metal ions. They play an important role in regulating essential metals such as zinc and copper and in detoxifying toxic metals such as cadmium and mercury. Exposure to elevated metal concentrations stimulates the production of metallothioneins, which can therefore be used as biomarkers of metal exposure.

Biomarkers of cellular and physiological stress

Biomarkers related to physiological stress indicate the effects of a wide range of pollutants; they are not substance specific. Cellular and physiological stress include: oxidative stress, lysosomal membrane stability, neutral lipid/lipofuscin accumulation and scope for growth.

Reduced tolerance to environmental stress

Some biomarkers assess whether exposure to pollutants has reduced the capacity of an organism to cope with additional environmental stress. Two examples are the stress-on-stress response and scope for growth.

The stress-on-stress biomarker measures the resistance of an organism to a standardized stress after prior exposure to pollution. In molluscs, this is often tested by exposing the animals to air and recording their survival time. Polluted or physiologically stressed animals generally have less physiological reserve and therefore survive for a shorter period than unstressed reference animals. The test thus indicates whether pollution has diminished the organism's capacity to withstand environmental stress.

Scope for growth estimates the energy available for growth and reproduction after subtracting metabolic costs from the energy acquired through feeding. Pollution can reduce this energetic surplus by impairing feeding or increasing metabolic costs.

Histological and cytological stress parameters

Fig. 1 Dilated extracellular spaces between adjacent ciliated cells in the palps of the mussel Mytilus galloprovincialis. Such morphologigal alterations are often related to the effects of pollutants.
Fig. 2 Lipid inclusions in digestive tubule cells of the mussel Mytilus galloprovincialis stained with Oil Red O. The size and the number of these cell compounds are often affected by pollution.
Fig. 3 Cryosection of a digestive gland tubule of the mussel Mytilus galloprovinciali. The lysosomes in the tubule cells are stained purple with the enzyme N-acetyl-β-hexosaminidase for the assessment of lysosomal membrane stability[14][15][16]. Similar cryosections are used for the application of the biomarker LMS, as well as for cytological / morphometrical observations.

Histopathological biomarkers detect structural changes in cells, tissues and organs. Because they represent actual tissue damage, they are generally more directly relevant to organism health than early molecular responses, but are less specific to particular pollutants.

Pollution can alter the structure and functioning of cells before effects become visible at the level of the whole organism. In mussels, the digestive gland is often examined because it is an important site of contaminant uptake, storage and detoxification.[17][18]

Histological and cytological biomarkers include changes in cell and tissue structure, accumulation of neutral lipids and lipofuscin, and changes in lysosomal membrane stability. Figures 1 and 2 illustrate structural and intracellular changes that can occur in mussels exposed to pollutants: Fig. 1 shows altered spacing between epithelial cells, whereas Fig. 2 shows accumulation of lipid inclusions in digestive-gland cells.[19][5]

Lysosomes are cell organelles involved in the breakdown and sequestration of foreign or harmful substances. Their membranes can become destabilized under pollutant stress. Lysosomal membrane stability (LMS) is therefore widely used as a biomarker of cellular stress in mussels. Figure 3 shows a cryosection of a digestive-gland tubule in which lysosomes are stained for LMS assessment.

In the LMS test, the stability of lysosomal membranes is assessed from the time required for acid treatment to release lysosomal enzymes and produce maximum staining. Shorter labilization times indicate lower lysosomal membrane stability and generally greater cellular stress, whereas longer times indicate more stable lysosomes.[20][16]

Biomarkers of genotoxicity

DNA damage

Genotoxicity biomarkers include DNA single- and double-strand breaks, modified bases, DNA-DNA crosslinks and DNA-protein crosslinks. Alkaline elution and the COMET assay are commonly used methods for detecting such damage.[21][22][23] [24][25][26]

Micronucleus formation

The micronucleus(MN) test is a cytogenetic technique commonly used for the evaluation of genotoxic effects caused by chemical stressors. Micronuclei are formed during cell division when whole chromosomes or chromosome fragments fail to be incorporated in the daughter nuclei, forming small additional nuclei. The test consists in the scoring of cells containing one or more cytosolic micronuclei in addition to the main nucleus.[22][27][28] as well as in in different cell types of fishes.[29][30][31]

Biomarkers of reproductive impairment

Pollutants can impair reproduction through several mechanisms, including direct toxicity to reproductive tissues and disruption of hormonal regulation. Substances that alter function(s) of the endocrine system are called Endocrine Disrupting Compounds (EDCs).

Histological parameters for assesment of changes in gonad development are often used in both molluscs and fish studies. Biomarkers assessing gonad (sex gland) development (such as ‘simple gonad index’ or ‘changes in structure of gonad tissue’) are helpful, giving indications of the effects of pollution on the reproductive performance of animals.[32][33][34] [35][36]

Vitellogenin is normally produced in mature female fish under estrogenic stimulation. Its induction in males or juveniles therefore provides a sensitive biomarker of exposure to estrogenic substances. Other biochemical indicators of endocrine disruption which have been regarded as useful tools for an assessment of endocrine disruption caused by chemicals in fish include changes in zona radiata proteins (zona radiata=radiately striated membrane situated next to the yolk of an ovum)[37][38] and steroid hormone balance.[39][40][41]

Endocrine-mediated reproductive effects and their mechanisms are discussed in Endocrine disruption by marine pollutants.

Combining biomarkers

No single biomarker provides a complete assessment of pollution impact. Exposure biomarkers can indicate contact with particular contaminant classes, whereas general stress, genotoxicity, histopathology and reproductive biomarkers provide information on biological effects of increasing ecological relevance but generally decreasing pollutant specificity. Biomonitoring programs therefore commonly combine several complementary biomarkers with measurements of contaminant concentrations.

Interpretation requires standardized methods and suitable reference or assessment values because biomarker responses are also influenced by factors such as temperature, season, age, nutritional condition and reproductive state. Integrated approaches combining chemical and biological-effect measurements are used in marine monitoring programs such as OSPAR's Coordinated Environmental Monitoring Program.[42]

High-throughput molecular approaches such as transcriptomics, proteomics and metabolomics are increasingly used to identify pollutant-response pathways and candidate biomarkers. Their application in routine environmental monitoring remains more limited because standardization, natural variability and interpretation of ecological significance are challenging.


Related articles

Biomonitoring of pollution impacts in the marine environment
Endocrine disruption by marine pollutants
Health biomarkers in marine mammals
Biomarker
Bioindicator
Endocrine disrupting compounds

References

  1. ↑ Beyer, J., Green, N.W., Brooks, S., Allan, I.J., Ruus, A., Gomes, T., Bråte, I.L.N., Schøyen, M., 2017. Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: A review. Marine Environmental Research 130: 338–365
  2. ↑ Oikari A., 2006. Caging techniques for field exposures of fish to chemical contaminants. Aquat Toxicol. 78(4), 370-81
  3. ↑ Kroon, F., Streten, C., Harries, S., 2017. A protocol for identifying suitable biomarkers to assess fish health: A systematic review. PLoS ONE 12(4): e0174762
  4. ↑ Van der Oost, R., Beyer, J. and Vermeulen, N.P.E., 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 13, 57-149
  5. ↑ 5.0 5.1 Viarengo, A., 1989. Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. CRC Critical Reviews in Aquatic Science 1, 295–317
  6. ↑ Viarengo, A., Burlando, B., Dondero, F., Marrò, A., Fabbri, R., 1999b. Metallothionein as a tool in biomonitoring programmes. Biomarkers 4, 455-466
  7. ↑ Payne, J.F., 1976. Field evaluation of benzopyrene hydroxylase induction as a monitor for marine petroleum pollution. Science 191, 945-946
  8. ↑ Stegeman, J.J., Hahn, M.E., 1994. Biochemistry and molecular biology of monooxygenase: current perspective on forms, functions, and regulation of cytochrome P450 in aquatic species. In: Malins, D.C., Ostrander, G.K., (Eds.), Aquatic toxicology: molecular, biochemical and cellular perspectives. Lewis Publishers, Boca Raton, FL, pp. 87-206
  9. ↑ Bucheli, T.D., Fent, K., 1995. Induction of cytocrome P450 as a biomarker for environmental contamination in aquatic ecosystem. Crit. Rev. Environ. Sci. Technol. 25, 201-268
  10. ↑ Goeptar, A.R., Scheerens, H., Vermeulen, N.P.E., 1995. Oxygen reductase and substrate reductase activity of cytochrome P450. Crit. Rev. Toxicol. 25, 25-65
  11. ↑ Viarengo, A., Bettella, E., Fabbri, R., Burlando, B., Lafaurie, M., 1997b. Heavy metal inhibition of EROD activity in liver microsomes from the bass Dicentrarchus labrax exposed to organic xenobiotics: role of GSH in the reduction of heavy metal effects. Mar. Environ. Res. 44, 1-11
  12. ↑ Sturm, A., da Silva de Assis, H.C., Hansen, P.D., 1999. Cholinesterases of marine teleost fish: enzymological characterization and potential use in the monitoring of neurotoxic contamination. Mar. Environ. Res. 47, 389-398
  13. ↑ Rodriguez-Fuentes, G., Gold-Bouchot, G., 2004. Characterization of cholinesterase activity from different tissues of Nile tilapia (Oreochromis niloticus). Mar. Environ. Res. 58, 505-509
  14. ↑ Viarengo, A., Moore, M.N., Mancinelli, G., Mazzucotelli, A., Pipe, R.K., Farrar, S.V., 1987. Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels: the effect of cadmium in the presence and absence of phenanthrene. Marine Biology 94, 251–257
  15. ↑ Lowe, D.M., Pipe, R.K., 1994. Contaminant induced lysosomal membrane damage in marine mussel digestive cells: an in vitro study. Aquat. Toxicol. 30, 357-365
  16. ↑ 16.0 16.1 UNEP/RAMOGE, 1999. Manual on the biomarkers recommended for the MED POL biomonitoring programme. UNEP, Athens, Greece.
  17. ↑ Moore, M.N., 1985. Cellular responses to pollutants. Marine Pollution Bulletin 16, 134–139
  18. ↑ Lowe, D.M., Moore, M.N., Clarke, R.K., 1981. Effects of oil on digestive cells in mussels:quantitative alterations in cellular and lysosomal structure. Aquat. Toxicol. 1, 213-226
  19. ↑ Lowe, D. M., 1988. Alteration in the cellular structure of Mytilus edulis resulting from exposure to environmental contaminants under field and experimental conditions. Mar. Ecol. Prog.Ser. 46, 91-100
  20. ↑ Moore, M.N., 1976. Cytochemical demonstration of latency of lysosomal hydrolases in digestive cells of the common mussel Mytilus edulis, and changes induced by thermal stress. Cell Tissue Research 175 (3), 279–287
  21. ↑ Batel, R., Vukmirovic, M., Jacsic, Z., Bihari, N., 1994. Impact of pollution on DNA fragmentation in marine invertebrates. Use of Aquatic Invertebrates as Tools for Monitoring the Environmental Hazards, 109-117
  22. ↑ 22.0 22.1 Bolognesi, C., Landini, E., Roggieri, P., Fabbri, R., Viarengo, A., 1999. Genotoxicity biomarkers in the assessment of heavy metal effects in mussels: experimental studies. Environ. Mol. Mutagen. 33, 287-292
  23. ↑ Bolognesi, C., Frenzilli, G., Lasagna, C., Perrone, E., Roggieri, P., 2004. Genotoxicity biomarkers in Mytilus galloprovincialis: wild versus caged mussels. Mutat. Res. 552, 187-196
  24. ↑ Bolognesi, C., Perrone, E., Roggieri, P., Pampanin, D., Sciutto, A., 2006. Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat. Toxicol. 78, S93-98
  25. ↑ Lee, R.F., Steinert, S., 2003. Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res. 544, 43-64
  26. ↑ Frenzilli, G., Scarcelli, V., Del Barga, I., Nigro, M., Forlin, L., Bolognesi, C., Sture, J., 2004. DNA damage in Eelpout (Zoarces viviparous) from Goteborg harbour. Mutat. Res. 552, 153-162
  27. ↑ Majone, F., Brunetti, R., Fumagalli, O., Gabriele, M., Levis, A.G., 1990. Induction of micronuclei by mitomycin C and colchicine in the marine mussel Mytilus galloprovincialis. Mutat. Res. 244, 147-151
  28. ↑ Scarpato, R., Migliore, L., Alfinito-Cognetti, G., Barale, R., 1990. Induction of micronuclei in gill tissue of Mytilus galloprovincialis exposed to polluted marine waters. Mar. Pollut. Bull. 21, 74-80.
  29. ↑ Al-Sabti, K., Metcalfe, C.D., 1995. Fish micronuclei for assessing genotoxicity in water. Mutat. Res. 343, 121-135
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  31. ↑ Barsiene, J., Lehtonen, K. K., Koehler, A., Broeg, K., Vuorinen, P.J., Lang, T., Pempkowiak, J., Šyvokien_, J., Dedonyte, V., Rybakovas, A., Repeka, R., Vuontisjärvi, H., Kopecka,J., 2006. Biomarker responses in flounder (Platichthys flesus) and mussel (Mytilus edulis) in the Klaipeda-B_ting_ area (Baltic Sea). Mar. Poll. Bull. 53, 422-436
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  34. ↑ Minier, C., Levy, F., Rabel, D., Bocquené, G., Godefroy, D., Burgeot, T., Leboulenger, F., 2000. Flounder health status in the Seine Bay. A multibiomarker study. Mar. Environ. Res. 50, 373-377
  35. ↑ Van der Oost, R., Beyer, J., Vermeulen, N.P.E., 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ. Toxicol. Pharmacol. 13, 57-149
  36. ↑ Aarab, N., Lemaire-Gony, S., Unruh, E., Hanson, P.D., Larsen, B.K., Andersen, O.K., Narbonne, J.F., 2006. Preliminary study of responses in mussel (Mytilus edilus) exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether. Aquat Toxicol. 1;78 Suppl 1:S86-92
  37. ↑ Haux, C., Björnsson, B.T., Förlin, L., Larsson, Å., Deftos, L.J., 1988. Influence of cadmium exposure on plasma calcium, vitellogenin and calcitonin in vitelogenic rainbow trout. Mar.Environ. Res. 24, 199-210.
  38. ↑ Spies, R.B., Stegeman, J.J., Rice, D.W., Jr., Woodlin, B., Thomas, P., Hose, J.E., Cross, J.N., Prieto, M., 1990. Sublethal responses of Platichtus stellatus to organic contamination in San Francisco Bay with emphasis on reproduction. In: McCarthy, J. F., Shugart, L. R.(Eds.), Biomarkers of Environmental Contamination. CRC Press, Boca Raton, FL, pp. 87-122.
  39. ↑ Karels, A., Soimasuo, M., Lappivaara, J., Leppänen, H., Aaltonen, T., Mellanen, P., Oikari, A.,1998. Effects of bleached kraft mill effluent on reproductive steroids and liver MFO activity in populations of perch and roach. Ecotoxicology 7, 123-132
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  41. ↑ Martin-Skilton, R., Lavado, R., Thibaut, R., Minier, C., Porte, C., 2006. Evidence of endocrine alteration in the red mullet, Mullus barbatus from the NW Mediterranean. Environ. Pollut.141, 60-8.
  42. ↑ Burgeot, T., Mauffret, A., J., Anderson, Brooks, S., Assuncao, M., Bellas Bereijo, J., Bignell, J., Campillo, J.A., Coorman, K., Förlin, L., Giltrap, M., Guls, H.D., Hylland, K., Halldorsson, H.P., Martinez-Gomez, C., McHugh, B., Parmentier, K., Scharsack, H., Sturve, J., Tairova, Z., 2022. Integrated biological effects and chemical contaminants approach: a case study. In: OSPAR, 2023: The 2023 Quality Status Report for the North-East Atlantic. OSPAR Commission, London.


The main author of this article is Vasilis Dimitriadis
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