Abstract
Although the effects of heavy metals on the behavior, including infectivity, of bacteria have been studied, little information is available about their effects on enteric viruses. We report an investigation of effects on the biosynthesis of human adenoviruses (HAdV) and hepatitis A (HAV) of waters contaminated with mineral waste following an environmental disaster in Mariana City, Minas Gerais State, Brazil. The study area was affected on November 5, 2015, by 60 million m3 of mud (containing very high concentrations of iron salts) from a mining reservoir (Fundão), reaching the Gualaxo do Norte River (sites evaluated in this study), the “Rio Doce” River and finally the Atlantic Ocean. We found substantial counts of infectious HAdV and HAV (by qPCR) in all sampled sites from Gualaxo do Norte River, indicating poor basic sanitation in this area. The effects of iron on viral infection processes were evaluated using HAdV-2 and HAV-175, as DNA and RNA enteric virus models, respectively, propagated in the laboratory and exposed to this contaminated water. Experiments in field and laboratory scales found that the numbers of plaque forming units (PFU) of HAdV and HAV were significantly higher in contaminated water with high iron concentrations than in waters with low iron concentration (< 20 µg/L of iron). These findings indicate that iron can potentiate enteric virus infectivity, posing a potential risk to human and animal health, particularly during pollution disasters such as that described here in Mariana, Brazil.
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Aguilera, E. R., Erickson, A. K., Jesudhasan, P. R., Robinson, C. M., & Pfeiffer, J. K. (2017). Plaques formed by mutagenized viral populations have elevated coinfection frequencies. mBio, 8, e02020–e02016.
APHA. (2012). Standard methods for the examination of water and wastewater (22st ed.). Washington, DC: American Public Health Association.
Boudaudn, M., Fréval-Le Bourdonnec, A., Jossent, J., Bakanga, F., Arnal, C., Jaffrezic, M. P., Oberti, S., & Gantzer, C. (2012). Removal of MS2, Qβ and GA bacteriophages during drinking water treatment at pilot scale. Water Research, 46(8), 2651–2664.
Chaturvedi, U. C., Shrivastava, R., & Upreti, R. K. 2004. Viral infections and trace metals: A complex interaction. Current Science 87(11), 1536–1554.
Cromeans, T. L., Lu, X. Y., Erdman, D. D., Humphrey, C. D., & Hill, V. R. (2008). Development of plaque assays for adenoviruses 40 and 41. Journal of Virological Methods, 151, 140–145.
Deerfield, D. W., Carter, Jr. C. W., & Pedersen, L. G. (2001). Models for protein-zinc ion binding sites. II: The catalytic sites. International Journal of Quantum Chemistry, 83, 150–165.
Dika, C., Duval, J. F., Ly-Chatain, H. M., Merlin, C., & Gantzer, C. (2011). Impact ofinternal RNA on aggregation and electrokinetics of viruses: Comparisonbetween MS2 phage and corresponding virus-like particles. Applied and Environmental Microbiology, 77(14), 4939–4948.
Fernandes, G. W., Goulart, F. F., Ranieri, B., Coelho, B. D., Dales, K., Boesche, N., et al. (2016). Deep into the mud: Ecological and socio-economic impacts of the dam breach in Mariana, Brazil. Natureza & Conservação, 14, 35–45.
Fongaro, G., Nascimento, M. A., Rigotto, C., Ritterbusch, G., da Silva, A. D., Esteves, P. A., & Barardi, C. R. M. (2013). Evaluation and molecular characterization of human adenovirus in drinking water supplies: Viral integrity and viability assays. Virology Journal, 10, 166.
Gassilloud, B., & Gantzer, C. (2005). Adhesion-aggregation and inactivation ofpoliovirus 1 in groundwater stored in a hydrophobic container. Applied and Environmental Microbiology, 71(2), 912–920.
Goh, K. C. M., Tang, C. K., Norton, D. C., et al. (2016). Molecular determinants of plaque size as an indicator of dengue virus attenuation. Scientific Reports, 6, 26100.
Hamza, A., Jurzik, L.. Uberla, K., & Wilhelm, M. (2011). Methods to detect infectious human enteric viruses in environmental water samples. International Journal of Hygiene and Environmental Health, 214, 424–436.
Jothikumar, N., Cromeans, T. L., Sobsey, M. D., & Robertson, H. (2005). Development and evaluation of a broadly reactive TaqMan assay for rapid detection of hepatitis A virus. Applied and Environmental Microbiology, 71, 3359–3363.
Langlet, J., Gaboriaud, F., Duval, J. F. L., & Gantzer, C. (2008). Aggregation and surface properties of F-specific RNA phages: Implication for zembrane filtration processes. Water Research, 42, 2769–2777.
Otth, L., Solís, G., Wilson, M., & Fernández, H. (2005). Susceptibility of Arcobacter butzleri to heavy metals. Brazilian Journal of Microbiology, 36(3), 286–288.
Ruyters, S., Mertens, J., Vassilieva, E., Dehandschutter, B., Poffijn, A., & Smolders, E. (2011). The Red mud accident in Ajka (Hungary): Plant toxicity and trace metal bioavailability in red mud contaminated soil. Environmental Science & Technology, 45, e1616–e1622.
Segura, F. R., Nunes, E. A., Paniz, F. P., et al. (2016). Potential risks of the residue from Samarco’s mine dam burst (Bento Rodrigues, Brazil). Environmental Pollution, 218, 813–825.
Sendner, C., Horinek, D., Bocquet, L., & Netz, R. R. (2009). Interfacial water at hydrophobic and hydrophilic surfaces: Slip, viscosity, and diffusion. Langmuir, 25(18), 10768–10781.
Shrivastava, R., Upreti, R. K., Seth, P. K., & Chaturvedi, U. C. (2002). Effects of chromium on the immune system. FEMS Immunol. Medical Microbiology, 34, 1–7.
Su, X., & D’Souza, D. H. (2011). Grape seed extract for control of human enteric viruses. Applied and Environmental Microbiology, 77(12), 3982–3987.
Viancelli, A., Garcia, L. A. T., Kunz, A., Steinmetz, R., Esteves, P. A., & Barardi, C. R. M. (2011). Detection of circoviruses and porcine adenoviruses in water samples collected from swine manure treatment systems. Research in Veterinary Science, 93, 538–543.
Acknowledgements
This study was financially supported by the Brazilian CNPq Project No. 472804/2013-8, and the CAPES/PDSE, and the RTA2014-00024-C04-01 from the Spanish Ministry of Economy and Innovation. We thank the Geochemistry Laboratory (LGqA/UFOP) for technical assistance.
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Fongaro, G., Viancelli, A., dos Reis, D.A. et al. Mineral Waste Containing High Levels of Iron from an Environmental Disaster (Bento Rodrigues, Mariana, Brazil) is Associated with Higher Titers of Enteric Viruses. Food Environ Virol 11, 178–183 (2019). https://doi.org/10.1007/s12560-019-09373-5
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DOI: https://doi.org/10.1007/s12560-019-09373-5