Abstract
The growing interest of our society for the environment, climate change, and the assurance of the quality of life and health has been the motor of new methodological proposals that allow a more comprehensive knowledge of the problems to be solved. In this sense, the potential of omic methodologies to study these problems from a global perspective represents a milestone in environmental studies. Therefore, the study of essential and toxic metals has a special interest, particularly in relation to toxicity issues and their association to biological interactions, transport, binding to biomolecules, and behavior in biological interfaces. These studies have promoted new instrumental platforms and methodological approaches that allow addressing these problems. Furthermore, to encompass the reality of molecule-atoms interactions in their completeness, combinations of omics have been tried, focusing on environment, food, and health issues. In this sense, the present work is situated, with the objective of reviewing the most recent methodological proposals in the field of the environment and their applications, considering not only the analytical approaches but also how they have to be applied, the use of bioindicators’ exposure experiments in the laboratory, and the potential transfer of the findings from the laboratory to the field. This latter point is a true touchstone, which makes these new analytical methodologies in the necessary tools for understanding the environment and the consequences of its imbalance.
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Bellido-Martín A, Gómez-Ariza JL, Smichowsky P, Sánchez-Rodas D (2009) Speciation of antimony in airborne particulate matter using ultrasound probe fast extraction and analysis by HPLC-HG-AFS. Anal Chim Acta 649:191–195. https://doi.org/10.1016/j.aca.2009.07.036
Bonilla-Valverd D, Ruiz-Laguna J, Muñoz A, Ballesteros J, Lorenzo F, Gómez-Ariza JL, López-Barea J (2004) Evolution of biological effects of Aznalcóllar mining spill in the Algerian mouse (Mus spretus) using biochemical biomarkers. Toxicology 197:123–138. https://doi.org/10.1016/j.tox.2003.12.010
Brown SC, Kruppa G, Dasseux JL (2005) Metabolomics applications of FT-ICR mass spectrometry. Mass Spectrom Rev 24:223–231. https://doi.org/10.1002/mas.20011
Compeau GC, Bartha R (1985) Sulfate-reducing bacteria principal methylators of mercury in anoxic estuarine sediment. Appl Envirom Microbiol 50:498–502. https://doi.org/10.1128/aem.50.2.498-502.1985
Contreras-Acuña M, García-Barrera T, García-Sevillano MA, Gómez-Ariza JL (2013) Speciation of arsenic in marine food (Anemonia sulcata) by liquid chromatography coupled to inductively coupled plasma mass spectrometry and organic mass spectrometry. J Chromatogr A 1282:133–141. https://doi.org/10.1016/j.chroma.2013.01.068
Contreras-Acuña M, García-Barrera T, García-Sevillano MA, Gómez-Ariza JL (2014) Arsenic metabolites in human serum and urine after seafood (Anemonia sulcata) consumption and bioaccessibility assessment using liquid chromatography coupled to inorganic and organic mass spectrometry. Microchem J 112:56–64. https://doi.org/10.1016/j.microc.2013.09.007
Damek-Poprawa M, Sawicka-Kapusta K (2004) Histopathological changes in the liver, kidneys, and testes of bank voles environmentally exposed to heavy metal emissions from the steelworks and zinc smelter in Poland. Environ Res 96:72–78. https://doi.org/10.1016/j.envres.2004.02.003
Edmonds JS, Francesconi KA (1988) The origin of arsenobetaine in marine animals. Appl Organomet Chem 2:297–302. https://doi.org/10.1002/aoc.590020404
Fernández-Cisnal R, García-Sevillano MA, García-Barrera T, Gómez-Ariza JL, Abril N (2018) Metabolomic alterations and oxidative stress are associated with environmental pollution in Procambarus clarkii. Aquat Toxicol 205:76–88. https://doi.org/10.1016/j.aquatox.2018.10.005
Gago-Tinoco A, González-Domínguez R, García-Barrera T, Blasco-Moreno J, Bebianno MJ, Gómez-Ariza JL (2014) Metabolic signatures associated with environmental pollution by metals in Doñana National Park using P. clarkii as bioindicator. Environ Sci Pollut Res 21(23):13315–13323. https://doi.org/10.1007/s11356-014-2741-y
Gailer J, George GN, Pickering IJ, Madden S, Prince RC, Yu EY, Denton MB, Younis HS, Aposhian HV (2000) Structural basis of the antagonism between inorganic mercury and selenium in mammals. Chem Res Toxicol 13:1135–1142. https://doi.org/10.1021/tx000050h
García-Sevillano MA, González-Fernández M, Jara-Biedma R, García-Barrera T, López-Barea J, Pueyo C, Gómez-Ariza JL (2012a) Biological response of free-living mouse Mus spretus from Doñana National Park under environmental stress based on assessment of metal-binding biomolecules by SEC-ICP-MS. Anal Bioanal Chem 404:1967–1981. https://doi.org/10.1007/s00216-012-6274-2
García-Sevillano MA, González-Fernández M, Jara-Biedma R, García-Barrera T, Vioque-Fernández A, López-Barea J, Pueyo C, Gómez-Ariza JL (2012b) Speciation of arsenic metabolites in the free-living mouse Mus spretus from Doñana National Park used as a bio-indicator for environmental pollution monitoring. Chem Pap 66:914–924. https://doi.org/10.2478/s11696-012-0207-6
García-Sevillano MA, García-Barrera T, Navarro F, Gómez-Ariza JL (2013a) Analysis of the biological response of mouse liver (Mus musculus) exposed to As2O3 based on integrated-omics approaches. Metallomics 5:1644–1655. https://doi.org/10.1039/c3mt00186e
García-Sevillano MA, García-Barrera T, Gómez-Ariza JL (2013b) Development of a new column switching method for simultaneous speciation of selenometabolites and selenoproteins in human serum. J Chromatogr A 1318:171–179. https://doi.org/10.1016/j.chroma.2013.10.012
García-Sevillano MA, Jara-Biedma R, Gonzalez-Fernandez M, Garcia-Barrera T, Gomez-Ariza JL (2013c) Metal interactions in mice under environmental stress. Biometals 26:651–666. https://doi.org/10.1007/s10534-013-9642-2
García-Sevillano MA, García-Barrera T, Navarro F, Gómez-Ariza JL (2014a) Absolute quantification of superoxide dismutase in cytosol and mitochondria of mice hepatic cells exposed to mercury by a novel metallomic approach. Anal Chim Acta 842:42–50. https://doi.org/10.1016/j.aca.2014.07.014
García-Sevillano MA, García-Barrera T, Gómez-Ariza JL (2014b) Application of metallomic and metabolomic approaches in exposure experiments on laboratory mice for environmental metal toxicity assessment. Metallomics 6:237–248. https://doi.org/10.1039/c3mt00302g
García-Sevillano MA, García-Barrera T, Navarro-Roldán F, Montero-Lobato Z, Gómez-Ariza JL (2014c) A combination of metallomics and metabolomics studies to evaluate the effects of metal interactions in mammals. Application to Mus musculus mice under arsenic/cadmium exposure. J Proteome 104:66–79. https://doi.org/10.1016/j.jprot.2014.02.011
García-Sevillano MA, Contreras-Acuña M, García-Barrera T, Navarro F, Gómez-Ariza JL (2014d) Metabolomic study in plasma, liver and kidney of mice exposed to inorganic arsenic based on mass spectrometry. Anal Bioanal Chem 406:1455–1469. https://doi.org/10.1007/s00216-013-7564-z
García-Sevillano MA, García-Barrera T, Abril N, Pueyo C, López-Barea J, Gómez-Ariza JL (2014e) Omics technologies and their applications to evaluate metal toxicity in mice M. spretus as a bioindicator. J Proteome 104:4–26. https://doi.org/10.1016/j.jprot.2014.02.032
García-Sevillano MA, Garcia-Barrera T, Navarro F, Abril N, Pueyo C, López-Barea J, Gómez-Ariza JL (2014f) Use of metallomics and metabolomics to assess metal pollution in Doñana National Park (SW Spain). Environ Sci Technol 48:7747–7755. https://doi.org/10.1021/es4057938
García-Sevillano MA, García-Barrera T, Navarro F, Gailer J, Gómez-Ariza JL (2014g) Use of elemental and molecular-mass spectrometry to assess the toxicological effects of inorganic mercury in the mouse Mus musculus. Anal Bioanal Chem 406:5853–5865. https://doi.org/10.1007/s00216-014-8010-6
García-Sevillano MA, García-Barrera T, Navarro F, Gómez-Ariza JL (2014h) Cadmium toxicity in Mus musculus mice based on a metallomic study. Antagonistic interaction between Se and Cd in the bloodstream. Metallomics 6:672–681. https://doi.org/10.1039/c3mt00350g
García-Sevillano MA, García-Barrera T, Gómez-Ariza JL (2015a) Environmental metabolomics: biological markers for metal toxicity. Electrophoresis 36:2348–2365. https://doi.org/10.1002/elps.201500052
García-Sevillano MA, García-Barrera T, Navarro F, Montero-Lobato Z, Gómez-Ariza JL (2015b) Shotgun metabolomic approach based on mass spectrometry for hepatic mitochondria of mice under arsenic exposure. Biometals 28:341–351. https://doi.org/10.1007/s10534-015-9837-9
García-Sevillano MA, García-Barrera T, Navarro F, Abril N, Pueyo C, López-Barea J, Gómez-Ariza JL (2015c) Combination of direct infusion mass spectrometry and gas chromatography mass spectrometry for toxicometabolomic study of red blood cells and serum of mice Mus musculus after mercury exposure. J Chromatogr B 985:75–84. https://doi.org/10.1016/j.jchromb.2015.01.029
Gilmour CC, Henry EA, Mitchel R (1992) Sulfate stimulation of mercury methylation in fresh-water sediments. Environ Sci Technol 26:2281–2287. https://doi.org/10.1128/AEM.01556-13
Gomez-Ariza JL, Sánchez-Rodas D, Beltran R, Corns W, Stockwel P (1998) Evaluation of atomic fluorescence spectrometry as a sensitive detection technique for arsenic speciation. Appl Organomet Chem 12:439–447. https://doi.org/10.1002/(SICI)1099-0739(199806)12:6<439::AID-AOC718>3.0.CO;2-8
Gómez-Ariza JL, Sánchez-Rodas D, Beltran R, Giraldez I (1999) Arsenic speciation in biological samples using the couplings HPLC-UV-HG-AAS AND HPLC-UV-HG-AFS. Int J Environ Anal Chem 74:203–213. https://doi.org/10.1080/03067319908031426
Gomez-Ariza JL, Lorenzo-Garcia F, García-Barrera T (2005) Guidelines for routine mercury speciation analysis in seafood by gas chromatography coupled to a home-modified AFS detector. Application to the Andalusian coast (south Spain). Chemosphere 61:1401–1409. https://doi.org/10.1016/j.chemosphere.2005.04.083
Gómez-Ariza JL, Lorenzo F, García-Barrera T (2005) Comparative study of atomic fluorescence spectroscopy and inductively coupled plasma mass spectrometry for mercury and arsenic multispeciation. Anal Bioanal Chem 382:485–492. https://doi.org/10.1007/s00216-005-3094-7
Gómez-Ariza JL, Jahromi EZ, González-Fernández M, García-Barrera T, Gailer J (2011) Liquid chromatography-inductively coupled plasma-based metallomic approaches to probe health-relevant interactions between xenobiotics and mammalian organisms. Metallomics 3:566–577. https://doi.org/10.1039/c1mt00037c
Gonzalez-Fernández M, García-Sevillano MA, Jara-Biedma R, García-Barrera T, Vioque A, López-Barea J, Pueyo C, Gómez-Ariza JL (2011) Size characterization of metal species in liver and brain from free-living (Mus spretus) and laboratory (Mus musculus) mice by SEC-ICP-MS: application to environmental contamination assessment. J Anal At Spectrom 26:141–149. https://doi.org/10.1039/c0ja00127a
Griffin JL, Mann CJ, Scott J, Shoulders CC, Nicholson JK (2001) Choline containing metabolites during cell transfection: an insight into magnetic resonance spectroscopy detectable changes. FEBS Lett 509:263–266. https://doi.org/10.1016/s0014-5793(01)03175-1
Grimalt JO, Ferrer M, MacPherson E (1999) The mine tailing accident in Aznalcollar. Sci Total Environ 242:3–11. https://doi.org/10.1016/s0048-9697(99)00372-1
Hinojosa Reyes L, Marchante-Gayón JM, García Alonso JI, Sanz-Medel A (2003) Quantitative speciation of selenium in human serum by affinity chromatography coupled to post-column isotope dilution analysis ICP-MS. J Anal At Spectrom 18:1210–1216. https://doi.org/10.1039/b305455a
Hu QZ, Noll RJ, Li HY, Makarov A, Hardman M, Cooks RG (2005) The orbitrap: a new mass spectrometer. J Mass Spectrom 40:430–443. https://doi.org/10.1002/jms.856
Jitaru P, Prete M, Cozzi G, Turetta C, Cairns W, Seraglia R, Traldi P, Cescon P, Barbante C (2008) Speciation analysis of selenoproteins in human serum by solid-phase extraction and affinity HPLC hyphenated to ICP-quadrupole MS. J Anal At Spectrom 23:402–406. https://doi.org/10.1039/b712693j
Kitchin KT, Wallace K (2008) The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J Inorg Biochem 102:532–539. https://doi.org/10.1016/j.jinorgbio.2007.10.021
Maret W (2004) Exploring the zinc proteome. J Anal At Spectrom 19:15–19. https://doi.org/10.1039/b307540k
Montes-Nieto R, Fuentes-Almagro CA, Bonilla-Valverde D, Prieto-Alamo MJ, Jurado J, Carrascal M, Gómez-Ariza JL, López-Barea J, Pueyo C (2007) Proteomics in free-living Mus spretus to monitor terrestrial ecosystems. Proteomics 7:4376–4387. https://doi.org/10.1002/pmic.200700409
Moreno F, García-Barrera T, Gómez-Ariza JL (2010) Simultaneous analysis of mercury and selenium species including chiral forms of selenomethionine in human urine and serum by HPLC column-switching coupled to ICP-MS. Analyst 135:2700–2705. https://doi.org/10.1039/c0an00090f
Mounicou S, Szpunar J, Lobinski R (2009) Metallomics: the concept and methodology. Chem Soc Rev 38:1119–1138. https://doi.org/10.1039/b713633c
Naranmandura H, Suzuki KT (2008) Formation of dimethylthioarsenicals in red blood cells. Toxicol Appl Pharmacol 227:390–399. https://doi.org/10.1016/j.taap.2007.11.008
Oliveira V, Gómez-Ariza JL, Sánchez-Rodas D (2005) Extraction procedures for chemical speciation of arsenic in atmospheric total suspended particles. Anal Bioanal Chem 382:335–340. https://doi.org/10.1007/s00216-005-3189-1
Oliveira V, Sarmiento AM, Gómez-Ariza JL, Nieto JM, Sánchez-Rodas D (2006) New preservation method for inorganic arsenic speciation in acid mine drainage samples. Talanta 69:1182–1189. https://doi.org/10.1016/j.talanta.2005.12.034
Outten CE, O’Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492. https://doi.org/10.1126/science.1060331
Rodríguez-Moro G, García-Barrera T, Trombini C, Blasco J, Gómez-Ariza JL (2018) Combination of HPLC with organic and inorganic mass spectrometry to study the metabolic response of the clam Scrobicularia plana to arsenic exposure. Electrophoresis 39:635–644. https://doi.org/10.1002/elps.201700318
Ruiz-Laguna J, Abril N, García-Barrera T, Gómez-Ariza JL, López-Barea J, Pueyo C (2006) Absolute transcript expression signatures of Cyp and Gst genes in Mus spretus to detect environmental contamination. Environ Sci Technol 40:3646–3652. https://doi.org/10.1021/es060056e
Saïd L, Banni M, Kerkeni A, Saïd K, Messaoudi I (2010) Influence of combined treatment with zinc and selenium on cadmium induced testicular pathophysiology in rat. Food Chem Toxicol 48:2759–2765. https://doi.org/10.1016/j.fct.2010.07.003
Sánchez de la Campa AM, de la Rosa J, Sánchez-Rodas D, Oliveira V, Alastuey A, Querol X, Gómez-Ariza JL (2008) Arsenic speciation study of PM2.5 in an urban area near a copper smelter. Atmos Environ 42:6487–6495. https://doi.org/10.1016/j.atmosenv.2008.04.016
Sanchez-Chardi A, Penarroja-Matutano C, Ribeiro CA, Nadal J (2007) Bioaccumulation of metals and effects of a landfill in small mammals. Part II. The wood mouse, Apodemus sylvaticus. Chemosphere 70:101–109. https://doi.org/10.1016/j.chemosphere.2007.06.047
Sanchez-Chardi A, Ribeiro CA, Nadal J (2009) Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. Chemosphere 76:387–394. https://doi.org/10.1016/j.chemosphere.2009.03.036
Sánchez-Rodas D, Geiszinger A, Gómez-Ariza JL, Francesconi KA (2002) Determination of an arsenosugar in oyster extracts by liquid chromatography-electrospray mass spectrometry and liquid chromatography-ultraviolet photo-oxidation-hydride generation atomic fluorescence spectrometry. Analyst 27:60–65. https://doi.org/10.1039/B107527F
Sánchez-Rodas D, Oliveira V, Sarmiento AM, Gómez-Ariza JL, Nieto JL (2006) Preservation procedures for arsenic speciation in a stream affected by acid mine drainage in southwestern Spain. Anal Bioanal Chem 384:1594–1599. https://doi.org/10.1007/s00216-006-0336-2
Sánchez-Rodas D, Sánchez de la Campa A, de la Rosa J, Oliveira V, Gómez-Ariza JL, Querol X, Alastuey A (2007) Arsenic speciation of atmospheric particulate matter (PM10) in an industrialized urban site in southwestern Spain. Chemosphere 66:1485–1493
Sarmiento AM, Oliveira V, Gómez-Ariza JL, Nieto JM, Sánchez-Rodas D (2007) Diel cycles of arsenic speciation due to photooxidation in acid mine drainage from the Iberian Pyrite Belt (Sw Spain). Chemosphere 66:677–683. https://doi.org/10.1016/j.chemosphere.2006.07.084
Sawicka-Kapusta K, Swiergosz R, Zakrzewska M (1990) Bank voles as monitors of environmental contamination by heavy metals. A remote wilderness area in Poland imperilled. Environ Pollut 67:315–324. https://doi.org/10.1016/0269-7491(90)90069-O
Shigeta K, Sato K, Furuta N (2007) Determination of selenoprotein P in submicrolitre samples of human plasma using micro-affinity chromatography coupled with low flow ICP-MS. J Anal At Spectrom 22:911–916. https://doi.org/10.1039/b701206c
Stojsavljević A, Borković-Mitić S, Vujotić L, Grujičić D, Gavrović-Jankulović M, Manojlović D (2019) The human biomonitoring study in Serbia: background levels for arsenic, cadmium, lead, thorium and uranium in the whole blood of adult Serbian population. Ecotoxicol Environ Saf 169:402–409. https://doi.org/10.1016/j.ecoenv.2018.11.043
Stojsavljević A, Jagodić J, Vujotić L, Borković-Mitić S, Rašić-Milutinović Z, Jovanović D, Gavrović-Jankulović M, Manojlović D (2020) Reference values for trace essential elements in the whole blood and serum samples of the adult Serbian population: significance of selenium deficiency. Environ Sci Pollut Res 27:1397–1405. https://doi.org/10.1007/s11356-019-06936-8
Su L, Wang M, Yin ST, Wang HL, Chen L, Sun LG, Ruan DY (2008) The interaction of selenium and mercury in the accumulations and oxidative stress of rat tissues. Ecotoxicol Environ Saf 70:483–489. https://doi.org/10.1016/j.ecoenv.2007.05.018
Suzuki KT (2005) Metabolomics of arsenic based on speciation studies. Anal Chim Acta 540:71–76. https://doi.org/10.1016/j.aca.2004.09.092
Suzuki KT, Mandal BK, Ogra Y (2002) Speciation of arsenic in body fluids. Talanta 58:111–119. https://doi.org/10.1016/S0039-9140(02)00260-6
Tainer JA, Roberts VA, Getzoff (eds) (1991) Metal-binding sites in proteins. Curr Opin Biotechnol 2:582–591. https://doi.org/10.1016/0958-1669(91)90084-I
Vahter M (1981) Biotransformation of trivalent and pentavalent inorganic arsenic in mice and rats. Environ Res 25:286–293. https://doi.org/10.1016/0013-9351(81)90030-x
Vahter M, Norin H (1980) Metabolism of 74As-labeled trivalent and pentavalent inorganic arsenic in mice. Environ Res 21:446–457. https://doi.org/10.1016/0013-9351(80)90049-3
Viant MR, Sommer U (2013) Mass spectrometry based environmental metabolomics: a primer and review. Metabolomics 9:S144–S158. https://doi.org/10.1007/s11306-012-0412-x
Vioque-Fernandez A, de Almeida EA, Ballesteros J, Garcia-Barrera T, Gomez-Ariza JL, Lopez-Barea J (2007) Doñana National Park survey using crayfish (Procambarus clarkii) as bioindicator: esterase inhibition and pollutant levels. Toxicol Lett 168:260–268. https://doi.org/10.1016/j.toxlet.2006.10.023
Vioque-Fernández A, Alves de Almeida E, López-Barea J (2009) Assessment of Doñana National Park contamination in Procambarus clarkii: integration of conventional biomarkers and proteomic approaches. Sci Total Environ 407:1784–1797. https://doi.org/10.1016/j.scitotenv.2008.11.051
Watras CJ, Bloom NS, Claas SA, Morrison KA, Gilmour CC, Craig SR (1995) Methylmercury production in the anoxic hypolimnion of a dimictic seepage lake. Water Air Soil Pollut 80:735–745. https://doi.org/10.1007/BF01189725
Wrobel K, Wrobel K, Caruso JA (2009) Epigenetics: an important challenge for ICP-MS in metallomics studies. Anal Bioanal Chem 393:481–486. https://doi.org/10.1007/s00216-008-2472-3
Yoneda S, Suzuki KT (1997) Equimolar Hg-Se complex binds to selenoprotein P. Biophys Res Commun 231:7–11. https://doi.org/10.1006/bbrc.1996.6036
Zalups RK (2000) Molecular interactions with mercury in the kidney. Pharmacol Rev 52:113–143. https://doi.org/10.1186/1741-7015-11-100
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This work has been supported by the projects CTM2015-67902-C2-1-P and PG2018-096608-B-C21 from the Spanish Ministry of Economy and Competitiveness. Belen Callejón Leblic thanks the Spanish Ministry of Education, Culture and Sports for a PhD scholarship (FPU13/03615). Gema Rodríguez-Moro and Sara Ramírez-Acosta thank the Spanish Ministry of Economy and Competitiveness for PhD scholarships (BES-2013-064501 and BES-2016-076364, respectively). Finally, the authors are grateful to FEDER (European Community) for financial support, grant numbers UNHU13-1E-1611 and UNHU15-CE-3140.
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Rodríguez-Moro, G., Ramírez-Acosta, S., Callejón-Leblic, B. et al. Environmental metal toxicity assessment by the combined application of metallomics and metabolomics. Environ Sci Pollut Res 28, 25014–25034 (2021). https://doi.org/10.1007/s11356-021-13507-3
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DOI: https://doi.org/10.1007/s11356-021-13507-3