Abstract
This manuscript describes the results of a metalloproteomic study of mercury in samples of muscle and liver tissue of the species Serrasalmus rhombeus, popularly known as black piranha and characterised as the most voracious and aggressive predator in the Brazilian Amazon. The metalloproteomic study involved using two-dimensional electrophoresis (2D PAGE) to fractionate the proteome of the muscle and liver tissue samples, along with atomic absorption spectrometry in a graphite furnace (GFAAS) to identify mercury associated with protein SPOTs and mass spectrometry with electrospray ionisation (ESI-MS/MS) to characterise the mercury-binding proteins. The protein SPOTs characterised showed concentrations in the order of 156 mg kg−1, which ranks as the highest concentrations of mercury determined so far in metalloproteomic studies involving fish species in the Amazon region. Based on FASTA sequences of proteins characterised by ESI-MS/MS, bioinformatics studies were performed that allowed identifying nine proteins with characteristics of biomarkers of mercury exposure. Of those proteins, glutathione peroxidase stands out as an enzyme of great importance in the antioxidant defence of organisms subjected to oxidative stress caused by xenobiotics.
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References
De Lacerda LD , Malm O (2008) Contaminação por mercúrio em ecossistemas aquáticos: uma análise das áreas críticas. Estud. av., São Paulo. 22(63) :173-190, https://doi.org/10.1590/S0103-40142008000200011.
WHO (World Health Organization) (2016) Mercury and health. January 2016. Archived fromthe original on 20 November. Retrieved 19 November 2016.
Pfeiffer WC, Lacerda LD, Salomons W, Malm O (1993) Environment fate of mercury from gold mining in the Brazilian Amazon. Environ Rev 1:26–37
Bastos, W. R.; Almeida, R.; Zara, L. F.; Rocha, J. C.; Santos A. Programa de Monitoramento Hidrobiogeoquímico do AHE JIRAU – Bacia do Rio Madeira. Tectebel Energia, 2009.
Lima PM, Neves RDCF, Dos Santos FA, Pérez CA, Da Silva MOA, Arruda MAZ, De Castro GR, Padilha PM (2010) Analytical approach to the metallomic of Nile tilapia (Oreochromis niloticus) liver tissue by SRXRF and FAAS after 2D-PAGE separation: preliminary results. Talanta 82(3):1052–1056. https://doi.org/10.1016/j.talanta.2010.06.023
Braga CP et al (2015) Mercury fractionation in dourada (Brachyplatystoma rousseauxii) of the Madeira River in Brazil using metalloproteomic strategies. Talanta 132:239–244
Garcia JS, Magalhães CS, Arruda MAZ (2006) Trends in metal-binding and metalloprotein analysis. Talanta 69:1–15
Bittarello AC, Vieira JCS, Braga CP, Bataglioli IC, Oliveira G, Rocha LC, Zara LF, Buzalaf MAR, Oliveira LCS, Adamec J, Padilha PM (2020) Metalloproteomic approach of mercury-binding proteins in liver and kidney tissues of Plagioscion squamosissimus (corvina) and Colossoma macropomum (tambaqui) from Amazon region: possible identification of mercury contamination biomarkers. Sci Total Environ 711:134547. https://doi.org/10.1016/j.scitotenv.2019.134547
Cavecci-Mendonça B, Vieira JCS, Lima PM, Leite AL, Buzalaf MAR, Zara LF, Padilha PM (2020) Study of proteins with mercury in fish from the Amazon region. Food Chem 309:125460. https://doi.org/10.1016/j.foodchem.2019.125460
http://www.correionoticias.com.br/site/piranha-preta-considerado-o-animal-com-a-dentada-mais-poderosa/ Acess: 02/13/2020
Vieira JCS, Cavecci B, Queiroz JV et al (2015) Determination of the mercury fraction linked to protein of muscle and liver tissue of tucunaré (Cichla spp.) from the Amazon Region of Brazil. Arch Environ Contam Toxicol 69:422–430. https://doi.org/10.1007/s00244-015-0160-9
Bittarello AC, Vieira JCS, Braga CP, Araújo WLP, Bataglioli IC, Silva JM, Buzalaf MAR, Fleuri LF, Padilha PM (2019) Characterization of molecular biomarkers of mercury exposure to muscle tissue of Plagioscion squamosissimus and Colossoma macropomum from the Amazon region. Food Chem 276:247–254
Bataglioli IC, Vieira JCS, Queiroz JV, Fernandes MS, Bittarello AC, Braga CP, Buzalaf MAR, Adamec J, Zara LF, Padilha PM (2019) Physiological and functional aspects of metal-binding protein associated with mercury in the liver tissue of pirarucu (Arapaima gigas) from the Brazilian Amazon, Chemosphere. Volume 236:124320
Vieira JCS, DE Oliveira G, Braga CP et al (2020) Parvalbumin and Ubiquitin as Potential Biomarkers of Mercury Contamination of Amazonian Brazilian Fish. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02026-w
Doumas BT, Bayse DD, Carter RJ, Peters JR, Schaffer RT (1981) A candidate reference method for determination of total protein in serum I. Development and validation. Clin Chem 27:1642–1650
Santos FA, Lima PM, Neves RCF et al (2011) Metallomic study on plasma samples from Nile tilapia using SR-XRF and GFAAS after separation by 2D PAGE: initial results. Microchim Acta 173:43–49. https://doi.org/10.1007/s00604-010-0522-y
Silva AF, Cavecci B, Baldassini W, Lima PM, Moraes PM, Roldan P, Padilha CF, Padilha PM (2013) Selenium fractionation from plasma, muscle and liver of Nile tilapia (Oreochromis niloticus). J Food Meas Charact 7:158–165. https://doi.org/10.1007/S11694-013-9151-6
Moraes PM et al (2013) GFAAS determination of mercury in muscle samples of fish from Amazon, Brazil. Food Chem 141(3):2614–2617
Silva F, Padilha C, Pezzato L, Barros M, Padilha P (2006) Determination of chromium by GFAAS in slurries of fish feces to estimate the apparent digestibility of nutrients in feed used in pisciculture. Talanta 69:1025–1030
Shevchenko AH, Tomas J, Havlis JV, Olsen M (2006) MANN, In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860
UniProt (2020) Universal Protein Resource (UniProt). 2020. Available at: http://www.uniprot.org/
Moraes PM, Santos FA, Padilha CCF et al (2012) A Preliminary and Qualitative Metallomics Study of Mercury in the Muscle of Fish from Amazonas, Brazil. Biol Trace Elem Res 150:195–199. https://doi.org/10.1007/s12011-012-9502-x
Vieira JCS, Braga CP, DE Oliveira G et al (2017) Identification of protein biomarkers of mercury toxicity in fish. Environ Chem Lett 15:717–724. https://doi.org/10.1007/s10311-017-0644-0
Vieira JCS et al (2018) Mercury exposure: protein biomarkers of mercury exposure in jaraqui fish from the Amazon Region. Biol Trace Elem Res 183:164–171. https://doi.org/10.1007/s12011-017-1129-5
DE Queiroz JV, Vieira JCS, DE Oliveira G et al (2019) Identification of Biomarkers of Mercury Contamination in Brachyplatystoma filamentosum of the Madeira River, Brazil, Using Metalloproteomic Strategies. Biol Trace Elem Res 187:291–300. https://doi.org/10.1007/s12011-018-1363-5
Olivero J, Solano B (1998) Mercury in environmental samples from a waterbody contaminated by gold mining in Colombia, South America. Sci Total Environ, Amsterdam 217(1-2):83–89
Campbell LM, Osano O, Hecky RE, Dixon DG (2003) Mercury in fish from three rift valley lakes (Turkana, Naivasha and Baringo), Kenya, East Africa. Environ Pollut, London 125(2):281–286
Ikigura JD, Akagi H (1999) Methyl mercury production and distribution in aquatic systems. Sci Total Environ, Amsterdam 234:109–118
Kim AY, Lim B, Choi J, Kim J (2015) A TFG-TEC oncoproteína induz a activação transcricional do gene da enolase β-humano através de modificação da cromatina da região promotora. Mol Carcinog. https://doi.org/10.1002/mc.22384
Huai-Dong SONG, Xiao-Jian SUN, Deng M, Zhang G-W, Zhou Y, Wu X-A, Sheng Y, Chen Y, Ruan Z, Jiang C-L, Fan H-Y, Zon LI, Kanki JP, Liu TX, Look AT, Chen Z (2004) Hematopoietic gene expression profile in zebrafish kidney marrow. Proc Natl Acad Sci 101(46):16240–16245. https://doi.org/10.1073/pnas.0407241101
Pu L, Igbavboa U, Madeira WG, Roths JB, Kier AB, Spener F, Schroeder F (1999) A expressão de proteínas de ligação de ácidos graxos é alterado de cérebro envelhecido do rato. Mol Cell Biochem 198(1-2):69–78. https://doi.org/10.1023/A:1006946027619
Basu P, Morris PE, Haar JL, Wani MA, Lingrel JB, Gaensler KM, Lloyd JA (2005) KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo. Blood 106(7):2566–2571. https://doi.org/10.1182/blood-2005-02-0674 PMC 1895257free to read
Quinkertz A, Campos-Ortega J (1999) A new β-globin gene from the zebrafish, β E1 , and its pattern of transcription during embryogenesis. Dev Genes Evol 209:126–131. https://doi.org/10.1007/s004270050235
Brownlie A, Hersey C, Oates AC, Paw BH, Falick AM, Witkowska HE, Flint J, Higgs D, Jessen J, Bahary N, Zhu N, Lin S, Zon L (2003) Characterization of embryonic globin genes of the zebrafish. Dev Biol 255(1):48–61. https://doi.org/10.1016/S0012-1606(02)00041-6
Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the “phosphocreatine circuit” for cellular energy homeostasis. Biochem J 281(1):21–40. https://doi.org/10.1042/bj2810021.PMC1130636freetoread
Berbel P, Marco P, Cerezo JR, Felipe J (1996) Distribution of parvalbumin immunoreactivity in the neocortex of hypothyroid adult rats. Neurosci Lett 204:65–68
Mccall KA, Huang C, Fierke CA (2000) Function and mechanism of zinc metalloenzymes. J Nutr 130:5147S–1446S
Faibane AM, Williams DR (1981) The principle of bio-inorganic chemistry. In: Chemical Society Monographs for Teachers, vol 31. The Chemical Society, London
Xu Y, He J, Wang X, Lim TM, Gong Z (2000) Asynchronous activation of 10 muscle-specific protein (MSP) genes during zebra fish somitogenesis. Dev Dyn 219:201–215
Wasko MM, Faraj S (2005) Why should I share? Examining social capital and knowledge contribution in electronic networks of practice. MIS Q 29(1):35–57
Gunning P, Ponte P, Okayama H, Engel J, Blau H, Kedes L (1983) Isolation and characterization of full-length cDNA clones for human α-, β-, and γ-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed Mol. Cell Biol 3:787–795
Decker RH, Kang HH, Leach FR, Henderson LM (1961) A purificação e propriedades da oxidase de 3-hidroxiantranico. J Biol Chem 236:3076–3082
Pearson RG (1963) Hard and soft acids and bases. J Am Chem Soc 85:3533–3539
Ladenstein O, Wendel RA (1983) A estrutura refinada da glutationa peroxidase selenoenzyme com resolução de 0,2 nm. Eur J Biochem/FEBS 133(1):51–69. https://doi.org/10.1111/j.1432-1033.1983.tb07429.x
De Queiroz JV, Vieira JCS, Da Cunha Bataglioli I et al (2018) Total Mercury Determination in Muscle and Liver Tissue Samples from Brazilian Amazon Fish Using Slurry Sampling. Biol Trace Elem Res 184:517–522. https://doi.org/10.1007/s12011-017-1212-y
Funding
The authors received FAPESP process nos. 2013/21297-1, 2016/19404-2; CNPq process nos. 304768/2018-9, 404485/2016-2; and the NATURAE Environmental Consultancy and to the Sustainable Energy P&D Project of Brazil S.A. (6631-0001/2012 Contract Jirau 004/13). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
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The protocol and ethics of this study were approved by the Animal Use Ethics Committee—AUEC, Faculty of Veterinary Medicine and Zootechny—UNESP, protocol 110/2015.
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de Queiroz, J.V., Cavecci-Mendonça, B., Vieira, J.C.S. et al. Metalloproteomic Strategies for Identifying Proteins as Biomarkers of Mercury Exposure in Serrasalmus rhombeus from the Amazon Region. Biol Trace Elem Res 199, 712–720 (2021). https://doi.org/10.1007/s12011-020-02178-9
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DOI: https://doi.org/10.1007/s12011-020-02178-9