Skip to main content

Advertisement

Log in

Toxicity evaluation of vinasse and biosolid samples in diplopod midgut: heat shock protein in situ localization

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Large amounts of residues generated by agricultural, urban and industrial activities are dumped daily on the soil. This practice deserves special attention because it causes serious environmental problems. This study evaluated the toxic potential of the sugarcane vinasse, a by-product of the sugar-alcohol industry, and the biosolid, a residue produced by wastewater treatment plants, both widely used as fertilizers. The evaluation was performed through bioassays using a typical soil bioindicator, the diplopod Rhinocricus padbergi. The specimens were exposed to soils containing these residues in concentrations that are compatible with the Brazilian regulation for agricultural use. Semi-quantitative immunolabelling analyses of the stress protein HSP70 were performed on the midgut of the studied diplopods. There was a significant increase in the immunolabelling of HSP70 proteins as a response to xenobiotics from both residues, particularly in regions where the function of the cells is the detoxification of the organ (e.g. the hepatic cell layer and specific regions of the epithelium). Higher immunolabelling was observed in the specimens exposed to vinasse in comparison with the biosolid exposure. This demonstrates that the substances in the tested residues had proteotoxic action in the exposed animals and induced a cytoprotective response, which led to higher stress protein immunolabelling. Therefore, caution is needed for the use of such residues in agriculture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2010) Biologia Molecular da Célula, quinta ed. Artmed, Porto Alegre (in Portuguese)

    Google Scholar 

  • Alvarenga P, Mourinha C, Farto M, Santos T, Palma P, Sengo J, Morais MC, Cunha-Queda C (2015) Sewage sludge, compost and other representative organic wastes as agricultural soil amendments: benefits versus limiting factors. Waste Manag 40:44–52

    Article  CAS  Google Scholar 

  • Alves PRL, Natal-da-Luz T, Sousa JP, Cardoso EJBN (2015) Ecotoxicological characterisation of sugarcane vinasses when applied to tropical soils. Sci Total Environ 526:222–232

    Article  CAS  Google Scholar 

  • Barros RP, Viégas PRA, Silva TL, Souza RM, Barbosa L, Viégas RA, Barreto MCV, Melo AS (2010) Alterações em atributos químicos de solo cultivado com cana-de-açúcar e adição de vinhaça. Pesq Agropec Trop 40:341–346 (in Portuguese)

    Article  Google Scholar 

  • Boorstein WR, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evol 38(1):1–17

    Article  CAS  Google Scholar 

  • Bovi MLA, Godoy-Júnior G, Costa EAD, Berton RS, Spiering SH, Vega FVA, Cembranelli MAR, Maldonado CAB (2007) Lodo de esgoto e produção de palmito em pupunheira. R Bras Ci Solo 3:153–166 (in Portuguese)

    Article  Google Scholar 

  • Bozzatto V, Fontanetti CS (2012) Sewage sludge toxicity in edaphic organism: analysis of midgut responses in the diplopod Rhinocricus padbergi. Microsc Res Tech 75(7):869–875

    Article  CAS  Google Scholar 

  • Camargo-Mathias MI, Fantazzini ER, Fontanetti CS (2004) Ultrastructural features of the midgut of Rhinocricus padbergi (diplopoda: spirobolida). Braz J Morphol Sci 21(2):65–71

    Google Scholar 

  • Canellas LP, Velloso ACX, Marciano CR, Ramalho JFGP, Rumjanek VM, Rezende CE, Santos GA (2003) Propriedades químicas de um Cambissolo cultivado com cana-de-açúcar, com preservação do palhiço e adição de vinhaça por longo tempo. R Bras Ci Solo 27:935–944 (in Portuguese)

    Article  CAS  Google Scholar 

  • CETESB-Companhia de Tecnologia de Saneamento Ambiental (2005). Norma 195/2005-E: Dispõe sobre a aprovação dos Valores Orientadores para Solos e Águas Subterrâneas no Estado de São Paulo-2005, em substituição aos Valores Orientadores de 2001. 215 (in Portuguese) http://solo.cetesb.sp.gov.br/wpcontent/uploads/sites/34/2014/12/tabela_valores_2005.pdf) Accessed 3 August 2015

  • CETESB-Companhia de Tecnologia de Saneamento Ambiental (2015) Norma P4.231: Vinhaça: Critérios e Procedimentos para Aplicação no Solo Agrícola (in Portuguese) http://www.cetesb.sp.gov.br/Tecnologia/camaras/P4_231.pdf Accessed 3 August 2015

  • Chenon P, Gauthier L, Loubières P, Séverac A, Delpoux M (2003) Evaluation of the genotoxic and teratogenic potential of a municipal sludge and sludge-amended soil using the amphibian Xenopus laevis and the tobacco:Nicotiana tabacum L var xanthi. DulieuSci Total Environ 301:139–150

    Article  CAS  Google Scholar 

  • Christofoletti CA, Francisco A, Fontanetti CS (2012) Biosolid soil application: toxicity tests under laboratory conditions. Appl Environ Soil Sci 2012:1–9

    Article  Google Scholar 

  • Christofoletti CA, Pedro-Escher J, Correia JA, Marinho JFU, Fontanetti CS (2013) Sugarcane vinasse: environmental implications of its use. Waste Manag 33:2752–2761

    Article  CAS  Google Scholar 

  • Christofoletti CA, Francisco A, Pedro-Escher J, Gastaldi VD, Fontanetti CS (2016) Diplopods as soil bioindicators of toxicity after application of residues from sewage treatment plants and ethanol industry. Microsc Microanal 22:1098–1110

    Article  CAS  Google Scholar 

  • CONAMA-Conselho Nacional do Meio Ambiente (2006) Resolução 375/2006. Define critérios e procedimentos, para o uso agrícola de lodos de esgoto gerados em estações de tratamento de esgoto sanitário e seus produtos derivados, e dá outras providências (in Portuguese) http://www.mma.gov.br/port/conama/res/res06/res37506.pdf). Accessed 3 August 2015

  • Correia JE, Christofoletti CA, Marcato ACC, Marinho JFU, Fontanetti CS (2017) Histopathological analysis of tilapia gills (Oreochromis niloticus Linnaeus, 1758) exposed to sugarcane vinasse. Ecotox Environ Saf 135:319–326

    Article  CAS  Google Scholar 

  • Costa CR, Olivi P, Botta CM, Espindola EL (2008) A toxicidade em ambientes aquáticos: discussão e métodos de avaliação. Quim Nova 31(7):1820–1830 (in Portuguese)

    Article  CAS  Google Scholar 

  • Da Silva APM, Bono JAM, Pereira FAR (2014) Aplicação de vinhaça na cultura da cana-de-açúcar: Efeito no solo e na produtividade de colmos. Rev Bras Eng Agríc Ambient 18(1):38–43 (in Portuguese)

    Article  Google Scholar 

  • Danish M, Fatima A, Khanam S, Jyoti S, Ali F, Naz F, Siddique YH (2015) Evaluation of the toxic potential of calcium carbide in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ) Bg9. Chemosphere 139:469–478

    Article  CAS  Google Scholar 

  • Eckwert H, Zanger M, Reiss S, Musolff H, Alberti G, Köhler HR (1994) The effect of heavy metals on the expression of hsp 70 in soil invertebrates. Verh Dtsch Zool Ges 87(1):325

    Google Scholar 

  • Erata GO, Kanbagli O, Durlanik O, Bulut T, Toker G, Uysal M (2005) Induced oxidative stress and decreased expression of inducible heat schock protein (hsp70) in patient with colorectal adenocarcinomas. Jpn J Clin Oncol 35(2):74–78

    Article  Google Scholar 

  • Fantazzini ER, Fontanetti CS, Camargo-Mathias MI (2002) Midgut of the millipede “Rhinocricus padbergi” Verhoeff, 1938 (Diplopoda: Spirobolida): histology and histochemistry. Arthropoda Sel 11:135–142

    Google Scholar 

  • Fontanetti CS, Nogarol LR, Souza RB, Perez DG, Maziviero GT (2011) Bioindicators and biomarkers in the assessment of soil toxicity. In: Pascucci S (ed) Soil Contamination, 1st edn. InTech, Rijeka, pp 143–168

    Google Scholar 

  • Fontanetti CS, Moreira-De-Sousa CM, Pinheiro TG, Souza RB, Francisco A (2015) Diplopoda-digestive system. In: Minelli A (ed) Treatise on zoology-anatomy, taxonomy, biology, 2nd edn. Leiden-Boston, Brill, pp 109–128

    Google Scholar 

  • Fytili D, Zabaniotou A (2008) Utilization of sewage sludge in EU application of old and new methods – a review. Renew Sust Energ Rev 12:116–140

    Article  CAS  Google Scholar 

  • Garcia CFH, Souza RB, de Souza CP, Christofoletti CA, Fontanetti CS (2017) Toxicity of two effluents from agricultural activity: comparing the genotoxicity of sugar cane and orange vinasse. Ecotox Environ Saf 142:216–221

    Article  CAS  Google Scholar 

  • Godoy JAP, Fontanetti CS (2010) Diplopods as bioindicators of soils: analysis of midgut of individuals maintained in substract containing sewage sludge. Water Air Soil Pollut 210:389–398

    Article  CAS  Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci J 86(11–12):377–384

    Article  CAS  Google Scholar 

  • Haynes RJ, Murtaza G, Naidu R (2009) Inorganic and organic constituents and contaminants of biosolids. Adv Agron 104:165–267

    Article  CAS  Google Scholar 

  • Hightower LE (1991) Heat shock, stress proteins, chaperons, and proteotoxicity (meeting review). Cell 66:191–197

    Article  CAS  Google Scholar 

  • Hopkin SP, Read HJ (1992) The biology of millipedes. Oxf Univ, Press, Oxford

    Google Scholar 

  • Kammenga JE, Dallinger R, Donker MH, Köhler HR, Simonsen V, Triebskorn R, Weeks JM (2000) Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Rev Environ Contam Toxicol 164:93–147

    CAS  Google Scholar 

  • Kiang JG, Tsokos GC (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacol Ther 80:183–201

    Article  CAS  Google Scholar 

  • Kiikkila O, Pennanen T, Perkiomaki J, Derome J, Fritze H (2002) Organic material as a copper immobilising agent: a microcosm study on remediation. Basic Appl Ecol 3:245–253

    Article  CAS  Google Scholar 

  • Köhler HR (2002) Localization of metals in cells of saprophagous soil arthropods (Isopoda, Diplopoda, Collembola) Microsc Res Techniq 56:393–401

  • Köhler HR, Triebskorn R, Stöcker W, Kloetzel PM, Alberti G (1992) The 70 kD heat shock protein (hsp70) in soil invertebrates: a possible tool for monitoring environmental toxicants. Arch Environ Con Tox 22(3):334–338

    Article  Google Scholar 

  • Köhler HR, Körtje KH, Alberti G (1995) Content absorption quantities and intracellular storage sites of heavy metals in Diplopoda (Arthropoda). Biometals 8:37–46

    Article  Google Scholar 

  • Köhler HR, Rahman B, Gräff S, Berkus M, Triebskorn R (1996) Expression of the stress-70 protein family (hsp70) due to heavy metal contamination in the slug, Deroceras reticulatum: an approach to monitor sublethal stress conditions. Chemosphere 33(7):1327–1340

    Article  Google Scholar 

  • Kumar S, Gopal K (2001) Impact of distellery effluent on physiological consequences in the freshwater teleost Channa punctatus. Bull Environ Contam Toxicol 66:617–622

    CAS  Google Scholar 

  • Lara AI, Andreoli CV, Pegorini ES (2007) Environmental impact assessment and monitoring of final sludge disposal. In: Andreoli CV, Von Sperling M, Fernandes F (eds) Sludge Treatment and Disposal. Iwa Publishing, London, pp 226–236

    Google Scholar 

  • Liu T, Pan L, Cai Y, Miao J (2015) Molecular cloning and sequence analysis of heat shock proteins 70 (HSP70) and 90 (HSP90) and their expression analysis when exposed to benzo(a)pyrene in the clam Ruditapes philippinarum. Gene 555(2):108–118

    Article  CAS  Google Scholar 

  • Lüchmann KH, Clark MS, Bainy AC, Gilbert JA, Craft JA, Chipman JK, Thorne MAS, Mattos JJ, Siebert MN, Schroeder DC (2015) Key metabolic pathways involved in xenobiotic biotransformation and stress responses revealed by transcriptomics of the mangrove oyster Crassostrea brasiliana. Aquat Toxicol 166:10–20

    Article  Google Scholar 

  • Mahmood K, Jadoon S, Mahmood Q, Irshad M, Hussain J (2014) Synergistic effects of toxic elements on heat shock proteins. Biomed Res Int 2014:1–17

    Google Scholar 

  • Malaspina O, Silva-Zacarin ECM (2006) Cell markers for ecotoxicological studies in target organs of bees. Braz J Morphol Sci 23(3/4):303–309

    Google Scholar 

  • Marinho JFU, Correia JE, Marcato ACC, Pedro-Escher J, Fontanetti CS (2014) Sugar cane vinasse in water bodies: impact assessed by liver histopathology in tilapia. Ecotox Environ Saf 110:239–245

    Article  CAS  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684

    Article  CAS  Google Scholar 

  • Merlini VV, Nogarol LR, Marin-Morales MA, Fontanetti CS (2012) Toxicity of trifluralin herbicide in a representative of the edaphic fauna: histopathology of the midgut of Rhinocricus padbergi (Diplopoda). Microsc Res Tech 75:1361–1369

    Article  CAS  Google Scholar 

  • Mondal S, Singhb RD, Patra AK, Dwivedi BS (2015) Changes in soil quality in response to short-term application of municipal sewage sludge in a typic haplustept under cowpea-wheat cropping system. Environ Nanotechnol Monit Manag 4:37–41

    Article  Google Scholar 

  • Mukhopadhyay I, Nazir A, Saxena DK, Chowdhuri DK (2003) Heat shock response: hsp 70 in environmental monitoring. J Biochem Mol Toxicol 17(5):249–254

    Article  CAS  Google Scholar 

  • Nadeau D, Plante I, Morrow G, Tanguay RM (2001) Evaluation for Hsp70 as a biomarker of effect of pollutants on the earthworm Lumbricus terrestres. Cell Stress Chaperon 6:153–163

    Article  CAS  Google Scholar 

  • Nascimento CWA, Barros DAS, Melo EEC, Oliveira AB (2004) Alterações químicas em solos e crescimento de milho e feijoeiro após aplicação de lodo de esgoto. R Bras Ci Solo 28:385–392 (in Portuguese)

    Article  CAS  Google Scholar 

  • Nascimento IA, Pereira SA, Leite MBNL (2008) Biomarcadores como instrumentos preventivos de poluição. In: Zagatto PA, Betoletti E (eds) Ecotoxicologia: Princípios e Aplicações. RiMa, São Carlos, pp 413–432 (in Portuguese)

    Google Scholar 

  • Natal-da-luz T, Tidona S, Van Gestel CAM, Morais PV, Sousa JP (2009) The use of collembola avoidance tests to characterize sewage sludges as soil amendments. Chemosphere 77(11):1526–1533

    Article  CAS  Google Scholar 

  • Natal-da-Luz T, Ojeda G, Costa M, Pratas J, Lanno RP, Van Gestel CAM, Sousa JP (2011) Shortterm changes of metal availability in soil. II: the influence of earthworm activity. Appl Soil Ecol 49:178–186

  • Nogarol LR, Fontanetti CS (2010) Acute and subchronic exposure of diplopods to substrate containing sewage mud: Tissular responses of the midgut. Micron 41:239–246

    Article  CAS  Google Scholar 

  • Pedro-Escher J, Maziviero GT, Fontanetti CS (2014) Mutagenic action of sugarcane vinasse in the Tradescantia pallida test system. J Ecosys Ecograph 4:145. doi:10.4172/2157-7625.10001

    Article  Google Scholar 

  • Pedro-Escher J, Christofoletti CA, Ansoar-Rodríguez Y, Fontanetti CS (2016) Sugarcane vinasse, a residue of ethanol industry: toxic, cytotoxic and genotoxic potential using the Allium cepa test. J Environ Prot 7:602–612

    Article  CAS  Google Scholar 

  • Perez DG, Fontanetti CS (2011) Assessment of the toxic potential of sewage sludge in the midgut of the diplopod Rhinocricus padbergi. Water Air Soil Poll (Print) 128:437–444

    Article  Google Scholar 

  • Polla BS, Kantengwa S, Francois D, Salvioli S, Franceschi C, Marsac C, Cossarizza A (1996) Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci U S A 93:6458–6463

    Article  CAS  Google Scholar 

  • Rahul JS, Naz F, Siddique YH (2015) Evaluation of the toxic potential of cefatoxamine in the third instar larvae of transgenic Drosophila melanogaster. Chem Biolo Interact 233:71–80

    Article  CAS  Google Scholar 

  • Raij BV, Cantarella HM (1997) In: Raij B, Van Cantarella H, Quaggio JA, AMC F (eds) Recomendações de adubação e calagem para o Estado de São Paulo, 2nd edn. Rev Atual. Instituto Agronômico, Campinas, pp 56–59 (in Portugese)

    Google Scholar 

  • Ryan JA, Hightower LE (1996) Stress proteins as molecular biomarkers for environmental toxicology. Stress-Inducible Cell Responses 77:411–424

    Article  CAS  Google Scholar 

  • Santamaría J, Toranzos GA (2003) Enteric pathogens and soil: a short review. Int Microbiol 6:5–9

    Google Scholar 

  • Sharma SK, Goloubinoff P, Christen P (2008) Heavy metal ions are potent inhibitors of protein folding. Biochem Biophys Res Commun 372(2):341–345

    Article  CAS  Google Scholar 

  • Silva-Zacarin ECM, Chauzat MP, Zeggane S, Drajnudel P, Schurr F, Faucon JP, Malaspina O, Engler JA (2012) Protocol for optimization of histological, histochemical and immunohistochemical analyses of larval tissues: application in histopathology of honey bee. Curr Microsc Contrib Adv Sci Technol 1:696–703

    Google Scholar 

  • Silveira MLA, Alleoni LRF, Guilherme LRG (2003) Biosolids and heavy metals in soils. Sci Agric 60(4):793–806

    Article  CAS  Google Scholar 

  • Sosinka A, Rost-Roszkowska MM, Vilimova J, Tajovský K, Kszuk-Jendrysik M, Chajec L, Sonakowska L, Kaminska K, Hyra M, Poprawa I (2014) The ultrastructure of the midgut epithelium in millipedes (Myriapoda, Diplopoda). Arthropod Struct Dev 43:477–492

    Article  CAS  Google Scholar 

  • Souza TS, Fontanetti CS (2011) Morphological biomarkers in the Rhinocricus padbergi midgut exposed to contaminated soil. Ecotoxicol Environ Saf 74:10–18

    Article  CAS  Google Scholar 

  • Souza TS, Christofoletti CA, Bozzatto V, Fontanetti CS (2014) The use of diplopods in soil ecotoxicology—a review. Ecotoxicol Environ Saf 103:68–73

    Article  Google Scholar 

  • Sreedhar AS, Csermely P (2004) Heat shock proteins in the regulation of apoptosis: new strategies in tumour therapy. Pharmacol Ther 101:227–257

    Article  CAS  Google Scholar 

  • Tamás MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomol Ther 4(1):252–267

    Google Scholar 

  • Urani C, Melchioretto P, Morazzoni F, Canevali C, Camatini M (2001) Copper and zinc uptake and HSP70 expression in HepG2 cells. Toxicol in Vitro 15(4–5):497–502

    Article  CAS  Google Scholar 

  • Valko MMHCM, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208

    Article  CAS  Google Scholar 

  • Wang L, Yang C, Song L (2013) The molluscan HSP70s and their expression in hemocytes. I S J 10:77–83

    Google Scholar 

  • Zanger M, Alberti G, Kuhn M, Kölher HR (1996) The stress-70 protein family in diplopods: induction and characterization. J Comp Physiol B 165:622–627

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, process no. 2012/50197-2 and 2014/12646-5) for financial support, and Gerson Mello de Souza for his help in the laboratory.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carmem Silvia Fontanetti.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coelho, M.P.M., Moreira-de-Sousa, C., de Souza, R.B. et al. Toxicity evaluation of vinasse and biosolid samples in diplopod midgut: heat shock protein in situ localization. Environ Sci Pollut Res 24, 22007–22017 (2017). https://doi.org/10.1007/s11356-017-9754-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9754-2

Keywords

Navigation