Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics.

Metabolic responses to environmental pollution, mainly related to Hg and PAHs, were investigated in mussels. Specimens of Mytilus galloprovincialis, sedentary filter-feeders, were caged in anthropogenic-impacted and reference sites along the Augusta coastline (Sicily, Italy). The gills, mainly involved in nutrient uptake, digestion and gas exchange, were selected as target organ being the first organ to be affected by pollutants. Severe alterations in gill tissue were observed in mussels from the industrial area compared with control, while gill metabolic profiles, obtained by (1)H NMR spectroscopy and analyzed by multivariate statistics, exhibited significant changes in amino acids, energy metabolites, osmolytes and neurotransmitters. Overall, the morphological changes and metabolic disturbance detected in gill tissues may suggest that the mussels transplanted to the contaminated field site were suffering from adverse environmental condition. The concurrent morphological and metabolomic investigations as applied here result effective in assessing the environmental influences on health status of aquatic organisms.

[1]  M. E. Clark,et al.  Living with water stress: evolution of osmolyte systems. , 1982, Science.

[2]  Salvatore Fasulo,et al.  Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). , 2013, Marine environmental research.

[3]  J. Hellou,et al.  Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. , 2003, Environmental pollution.

[4]  S. Ferrando,et al.  Stress factors in the gills of Liza aurata (Perciformes, Mugilidae) living in polluted environments , 2005 .

[5]  M. Auffret Histopathological changes related to chemical contamination in Mytilus edulis from field and experimental conditions , 1988 .

[6]  Salvatore Fasulo,et al.  Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. , 2012, Ecotoxicology and environmental safety.

[7]  G. Cammarata,et al.  Ecotoxicological and human health risk in a petrochemical district of southern Italy. , 2008, Marine environmental research.

[8]  F. Galgani,et al.  Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. , 2010, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[9]  D. Giordano,et al.  Effects of "in vivo" exposure to toxic sediments on juveniles of sea bass (Dicentrarchus labrax). , 2011, Aquatic toxicology.

[10]  D. Fattorini,et al.  Contaminant accumulation and biomarker responses in caged mussels, Mytilus galloprovincialis, to evaluate bioavailability and toxicological effects of remobilized chemicals during dredging and disposal operations in harbour areas. , 2008, Aquatic toxicology.

[11]  Tracey B. Schock,et al.  NMR-based microbial metabolomics and the temperature-dependent coral pathogen Vibrio coralliilyticus. , 2009, Environmental science & technology.

[12]  M. Bebianno,et al.  Glutathione S-tranferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. , 2007, Environment international.

[13]  S. D. Probert,et al.  Water and sediment movements in harbours , 2000 .

[14]  O. Fiehn Metabolomics – the link between genotypes and phenotypes , 2004, Plant Molecular Biology.

[15]  A. Bellanca,et al.  Impact of human activities on the central Mediterranean offshore: Evidence from Hg distribution in box-core sediments from the Ionian Sea , 2008 .

[16]  S. Fasulo,et al.  Effect of natural confinement on the gill cell types and bony elements of Lebias fasciata (Teleostei, Cyprinodontidae): A morphological and immunohistochemical analysis , 2002 .

[17]  Jianmin Zhao,et al.  Metabolic responses in gills of Manila clam Ruditapes philippinarum exposed to copper using NMR-based metabolomics. , 2011, Marine environmental research.

[18]  Ronald S. Tjeerdema,et al.  Metabolomics: Methodologies and applications in the environmental sciences , 2006 .

[19]  I. Sunila Acute histological responses of the gill of the mussel, Mytilus edulis, to exposure by environmental pollutants , 1988 .

[20]  G. Somero Osmolyte and metabolic end products of mollusks : the design of compatible solute systems , 1983 .

[21]  T. Esch,et al.  Tyrosine and tyramine increase endogenous ganglionic morphine and dopamine levels in vitro and in vivo: cyp2d6 and tyrosine hydroxylase modulation demonstrates a dopamine coupling. , 2005, Medical science monitor : international medical journal of experimental and clinical research.

[22]  Regoli Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. , 2000, Aquatic toxicology.

[23]  S. Fasulo,et al.  Expression of metallothionein mRNAs by in situ hybridization in the gills of Mytilus galloprovincialis, from natural polluted environments. , 2008, Aquatic toxicology.

[24]  F. Iacono,et al.  Environmental metabolomics and multibiomarker approaches on biomonitoring of aquatic habitats , 2010 .

[25]  D. Livingstone,et al.  Mussels and environmental contaminants : molecular and cellular aspects , 1992 .

[26]  S. Mazzola,et al.  Mercury in fishes from Augusta Bay (southern Italy): risk assessment and health implication. , 2013, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[27]  Oliver A.H. Jones,et al.  Systems toxicology approaches for understanding the joint effects of environmental chemical mixtures. , 2010, The Science of the total environment.

[28]  Salvatore Fasulo,et al.  Effects of sublethal, environmentally relevant concentrations of hexavalent chromium in the gills of Mytilus galloprovincialis. , 2012, Aquatic toxicology.

[29]  G. Hwang,et al.  Characterizing the effect of heavy metal contamination on marine mussels using metabolomics. , 2012, Marine pollution bulletin.

[30]  R. Preston Transport of amino acids by marine invertebrates , 1993 .

[31]  J. Girard,et al.  Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. , 2003, Environmental pollution.

[32]  E. Brunelli,et al.  Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L., exposed to cadmium. , 2011, Acta histochemica.

[33]  I. Wilson,et al.  APPLICATION OF HIGH RESOLUTION H-NMR SPECTROSCOPY TO THE DETECTION OF PENICILLAMINE AND ITS METABOLITES IN HUMAN URINE , 1988 .

[34]  A. Sureda,et al.  Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Eivissa Island, Spain). , 2011, Aquatic toxicology.

[35]  P. Cary,et al.  An environmental 1H NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation , 2009, Metabolomics.

[36]  Elena De Domenico,et al.  A multibiomarker approach in Coris julis living in a natural environment. , 2010, Ecotoxicology and environmental safety.

[37]  M. Viant,et al.  Identifying health impacts of exposure to copper using transcriptomics and metabolomics in a fish model. , 2010, Environmental science & technology.

[38]  A. Viarengo,et al.  The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. , 2007, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[39]  F. Galgani,et al.  Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. , 2004, Marine pollution bulletin.

[40]  Mark R Viant,et al.  Direct sampling of organisms from the field and knowledge of their phenotype: key recommendations for environmental metabolomics. , 2007, Environmental science & technology.

[41]  D. Fattorini,et al.  An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoring the impact of an offshore platform in the Adriatic Sea. , 2008, Marine environmental research.

[42]  B. Mayer,et al.  Neuronal nitric oxide synthase (nNOS) expression in the epithelial neuroendocrine cell system and nerve fibers in the gill of the catfish, Heteropneustes fossilis. , 1999, Acta histochemica.

[43]  Haakil Lee,et al.  Metabolomic Investigations of American Oysters Using 1H-NMR Spectroscopy , 2010, Marine drugs.

[44]  C. Mangum,et al.  Salt and water balance in the oligohaline clam, Rangia cuneata II. Accumulation of intracellular free amino acids during high salinity adaptation , 1980 .

[45]  Mark R. Viant,et al.  Applications of metabolomics to the environmental sciences , 2009, Metabolomics.

[46]  A. Anandraj,et al.  Correlations between metal uptake in the soft tissue of Perna perna and gill filament pathology after exposure to mercury. , 2002, Marine pollution bulletin.

[47]  S. Ferrando,et al.  Gut morphology and metallothionein immunoreactivity in Liza aurata from different heavy metal polluted environments , 2006 .

[48]  Huifeng Wu,et al.  NMR-based metabolomic studies on the toxicological effects of cadmium and copper on green mussels Perna viridis. , 2010, Aquatic toxicology.

[49]  David S. Wishart,et al.  HMDB: a knowledgebase for the human metabolome , 2008, Nucleic Acids Res..

[50]  Salvatore Fasulo,et al.  Toxicity of Foroozan crude oil to ornate wrasse (Thalassoma pavo, Osteichthyes, Labridae): ultrastructure and cellular biomarkers , 2012 .

[51]  E. Fukusaki,et al.  Quality evaluation and prediction of Citrullus lanatus by 1H NMR-based metabolomics and multivariate analysis. , 2008, Journal of agricultural and food chemistry.

[52]  S. Fasulo,et al.  Immunohistochemical and molecular biomarkers in Coris julis exposed to environmental contaminants. , 2010, Ecotoxicology and environmental safety.

[53]  S. Ferrando,et al.  Apoptosis, cell proliferation and serotonin immunoreactivity in gut of Liza aurata from natural heavy metal polluted environments: preliminary observations. , 2009, European journal of histochemistry : EJH.

[54]  Mark R Viant,et al.  NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism health. , 2003, Environmental science & technology.

[55]  Jianmin Zhao,et al.  Benzo(a)pyrene-induced metabolic responses in Manila clam Ruditapes philippinarum by proton nuclear magnetic resonance ((1)H NMR) based metabolomics. , 2011, Environmental toxicology and pharmacology.

[56]  M. Viant Improved methods for the acquisition and interpretation of NMR metabolomic data. , 2003, Biochemical and biophysical research communications.

[57]  A. Cundy,et al.  Possible impacts of Hg and PAH contamination on benthic foraminiferal assemblages: an example from the Sicilian coast, central Mediterranean. , 2007, The Science of the total environment.

[58]  C. S. Fontanetti,et al.  Fine structure of Mytella falcata (Bivalvia) gill filaments. , 2008, Micron.

[59]  M. Viant,et al.  High-throughput tissue extraction protocol for NMR- and MS-based metabolomics. , 2008, Analytical biochemistry.

[60]  Y. Choi,et al.  NMR-based metabolomic analysis of plants , 2010, Nature Protocols.