Abstract
Sediments represent complex mixtures and the impacts of their physical and chemical processes on biota are important for assessing potential health risks. We aimed to rank sediment samples from Guanabara Bay by developing an algorithm (quality ratio—QR), focusing on key sediment parameters (fine grain size, total organic carbon (TOC), metal concentrations) and enzymatic activities (dehydrogenase (DHA-energy production into cell) and esterases (EST-hydrolase organic matter outside the cell membrane)) of in situ microbial communities. Our QR is supported by quantitative information and significant correlations between geochemical and microbial processes. The QR is a function of the dependent term DHA/EST and the geochemical term (TOC×∑CF)/fine-grained sediment, where ∑CF is the sum of contamination factors (ratio between actual and background metal concentrations). We could rank our sampling sites into three risk classes based on QR: low, medium, and high. Our findings suggest altered homeostasis due to the development of contamination resistance. We applied a sensitivity analysis, using Brazilian law for sediment quality assessment, to calibrate our risk index. Our QR is suitable for measuring the potential health risk of any sediment, especially in developing countries with serious technical limitations, since its evaluated parameters are cheap, fast, and easy to obtain.
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References
Aguiar, V. M., de Lima, M. N., Abuchacra, R. C., et al. (2016). Ecological risks of trace metals in Guanabara Bay, Rio de Janeiro, Brazil: an index analysis approach. Ecotoxicology and Environmental Safety, 133, 306–315. https://doi.org/10.1016/j.ecoenv.2016.07.012.
Allison, S. D., & Martiny, J. B. H. (2008). Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences, 105, 11512–11519. https://doi.org/10.1073/pnas.0801925105.
ASTM International. (2008). Standard test methods for sulfur in the analysis sample of coal and coke using high-temperature tube furnace combustion methods. ASTM D 4239. American Society for Testing and Materials, 552, 6. https://doi.org/10.1520/D4239-14.2.
Babich, H., & Stotzky, G. (1985). Heavy metal toxicity to microbe-mediated ecologic processes: a review and potential application to regulatory policies. Environmental Research., 36, 111–137.
Baptista-Neto, J. A., Gingele, F. X., Leipe, T., & Brehme, I. (2006). Spatial distribution of heavy metals in surficial sediments from Guanabara Bay: Rio de Janeiro, Brazil. Environmental Geology, 49, 1051–1063. https://doi.org/10.1007/s00254-005-0149-1.
Baptista-Neto, J. A., Barreto, C. F., Vilela, C. G., et al. (2015). Environmental change in Guanabara Bay, SE Brazil, based in microfaunal, pollen and geochemical proxies in sedimentary cores. Ocean and Coastal Management, 143, 4–15. https://doi.org/10.1016/j.ocecoaman.2016.04.010.
Bidone, E. D., & Lacerda, L. D. (2004). The use of DPSIR framework to evaluate sustainability in coastal areas. Case study: Guanabara Bay basin, Rio de Janeiro, Brazil. Regional Environmental Change, 4, 5–16. https://doi.org/10.1007/s10113-003-0059-2.
Bidone, E. D., Fiori, R. P., Rodrigues, A. P., et al. (2009). Custo sócio-econômico de dragagens portuárias. In Gestão Ambient Portuária-Subsídios para o licenciamento das dragagens (pp. 75–88).
Brasil. (2012). Resolução CONAMA No 454. 1o de Novembro 2012. In Estabelece as diretrizes gerais e os procedimentos referenciais para o gerenciamento do material a ser dragado em águas sob jurisdição nacional (pp. 66–69) Seção 1.
Burton, G. A. (2002). Sediment quality criteria in use around the world. Limnology, 3, 65–75. https://doi.org/10.1007/s102010200008.
Busch, J., Nascimento, J. R., Magalhães, A. C. R., Dutilh, B. E., & Dinsdale, E. (2015). Copper tolerance and distribution of epibiotic bacteria associated with giant kelp Macrocystis pyrifera in southern California. Ecotoxicology, 24, 1131–1140. https://doi.org/10.1007/s10646-015-1460-6.
Carreira, R. S., Wagener, A. L. R., Readman, J. W., Fileman, T. W., Macko, S. A., & Veiga, Á. (2002). Changes in the sedimentary organic carbon pool of a fertilized tropical estuary, Guanabara Bay, Brazil: an elemental, isotopic and molecular marker approach. Marine Chemistry, 79, 207–227. https://doi.org/10.1016/S0304-4203(02)00065-8.
Chapman, P. M. (2018). Negatives and positives: contaminants and other stressors in aquatic ecosystems. Bulletin of Environmental Contamination and Toxicology, 100, 3–7. https://doi.org/10.1007/s00128-017-2229-9.
Cordeiro, R. C., Machado, W., Santelli, R. E., Figueiredo, A. G., Seoane, J. C. S., Oliveira, E. P., Freire, A. S., Bidone, E. D., Monteiro, F. F., Silva, F. T., & Meniconi, M. F. G. (2015). Geochemical fractionation of metals and semimetals in surface sediments from tropical impacted estuary (Guanabara Bay, Brazil). Environment and Earth Science, 74, 1363–1378. https://doi.org/10.1007/s12665-015-4127-y.
Cornall, A., Rose, A., Streten, C., McGuinness, K., Parry, D., & Gibb, K. (2016). Molecular screening of microbial communities for candidate indicators of multiple metal impacts in marine sediments from northern Australia. Environmental Toxicology and Chemistry, 35, 468–484. https://doi.org/10.1002/etc.3205.
Crapez, M. A. C., Baptista-Neto, J. A., & Bispo, M. G. S. (2003). Bacterial enzymatic activity and bioavailability of heavy metals in sediments from Boa Viagem Beach. Anuário Inst Geociências - UFRJ, 26, 60–68.
de Aguiar, V. M. C., Neto, J. A. B., & Rangel, C. M. (2011). Eutrophication and hypoxia in four streams discharging in Guanabara Bay, RJ, Brazil, a case study. Marine Pollution Bulletin, 62, 1915–1919. https://doi.org/10.1016/j.marpolbul.2011.04.035.
Decho, AW. (2000). Microbial biofilms in intertidal systems: an overview. Continental Shelf Research, 20, 1257–1273.
Demaison, G. J., & Moore, G. T. (1980). Anoxic environment and oil source bed genesis. Organic Geochemistry, 2, 9–31.
Fiori, C. S. F., Rodrigues, A. P. C., Santelli, R. E., et al. (2013). Ecological risk index for aquatic pollution control: a case study of coastal water bodies from the Rio de Janeiro state, southeastern Brazil. Geochimica Brasiliensis, 2, 24–36. https://doi.org/10.5327/Z0102-9800201300010003.
Fistarol, G. O., Coutinho, F. H., Moreira, A. P. B., Venas, T., Cánovas, A., de Paula, S. E. M., Coutinho, R., de Moura, R. L., Valentin, J. L., Tenenbaum, D. R., Paranhos, R., do Valle, R. A. B., Vicente, A. C. P., Amado Filho, G. M., Pereira, R. C., Kruger, R., Rezende, C. E., Thompson, C. C., Salomon, P. S., & Thompson, F. L. (2015). Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro. Frontiers in Microbiology, 6, 1–17. https://doi.org/10.3389/fmicb.2015.01232.
Flemming, H.-C. (2016). EPS—Then and now. Microorganisms, 4, 41. https://doi.org/10.3390/microorganisms4040041.
Flemming, H.-C., & Wingender, J. (2010). The biofilm matrix. Nature Reviews. Microbiology, 19, 139–150. https://doi.org/10.1038/nrmicro2415.
Fonseca, E. M., Baptista-Neto, J. A., Crapez, M. C., et al. (2009). Bioavailability of heavy metals in Guanabara Bay, Rio de Janeiro (Brazil). Journal of Coastal Research, 2009, 802–806. https://doi.org/10.2112/JCOASTRES-D-12-00.
Fonseca, E. M., Baptista, Neto J. A., Silva, C. G., et al (2013) Stormwater impact in Guanabara Bay (Rio de Janeiro): Evidences of seasonal variability in the dynamic of the sediment heavy metals. Estuar Coast Shelf Sci 130:161–168. https://doi.org/10.1016/j.ecss.2013.04.022
Fontana, L. F., Mendonça Filho, J. G., Pereira Netto, A. D., Sabadini-Santos, E., de Figueiredo, A. G., Jr., & Crapez, M. A. C. (2010). Geomicrobiology of cores from Suruí mangrove - Guanabara Bay - Brazil. Marine Pollution Bulletin, 60, 1674–1681. https://doi.org/10.1016/j.marpolbul.2010.06.049.
Franco, L., Romero, D., García-Navarro, J. A., Teles, M., & Tvarijonaviciute, A. (2016). Esterase activity (EA), total oxidant status (TOS) and total antioxidant capacity (TAC) in gills of Mytilus galloprovincialis exposed to pollutants: Analytical validation and effects evaluation by single and mixed heavy metal exposure. Marine Pollution Bulletin, 102, 30–35. https://doi.org/10.1016/j.marpolbul.2015.12.010.
Gough, D. (2007). Weight of evidence: a framework for the appraisal of the quality and relevance of evidence. Research Papers in Education, 22, 213–228. https://doi.org/10.1080/02671520701296189.
Gregoracci, G. B., Nascimento, J. R., Cabral, A. S., Paranhos, R., Valentin, J. L., Thompson, C. C., & Thompson, F. L. (2012). Structuring of bacterioplankton diversity in a large tropical bay. PLoS One, 7, e31408. https://doi.org/10.1371/journal.pone.0031408.
Guo, W., Liu, X., Liu, Z., & Li, G. (2010). Pollution and potential ecological risk evaluation of heavy metals in the sediments around Dongjiang Harbor, Tianjin. Procedia Environmental Sciences, 2, 729–736. https://doi.org/10.1016/j.proenv.2010.10.084.
Hakanson, L. (1980). An ecological risk index for aquatic pollution control. A sedimentological approach. Water Research, 14, 975–1001. https://doi.org/10.1016/0043-1354(80)90143-8.
Harrison, J. J., Ceri, H., & Turner, R. J. (2007). Multimetal resistance and tolerance in microbial biofilms. Nature Reviews. Microbiology, 5, 928–938. https://doi.org/10.1038/nrmicro1774.
Huerta-Diaz, M. A., & Morse, J. W. (1990). A quantitative method for determination of trace metal concentrations in sedimentary pyrite. Marine Chemistry, 29, 119–144. https://doi.org/10.1016/0304-4203(90)90009-2.
Irha, N., Slet, J., & Petersell, V. (2003). Effect of heavy metals and PAH on soil assessed via dehydrogenase assay. No title. Environment International, 28, 779–782.
Kepner, R. L., & Pratt, J. R. (1994). Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Microbiological Reviews, 58, 603–615.
Kjerfve, B., Ribeiro, C. H. A., Dias, G. T. M., Filippo, A. M., & da Silva Quaresma, V. (1997). Oceanographic characteristics of an impacted coastal bay: Baía de Guanabara, Rio de Janeiro, Brazil. Continental Shelf Research, 17, 1609–1643. https://doi.org/10.1016/S0278-4343(97)00028-9.
Løkke, H., Ragas, A. M. J., & Holmstrup, M. (2013). Tools and perspectives for assessing chemical mixtures and multiple stressors. Toxicology, 314, 73–82. https://doi.org/10.1016/j.tox.2012.11.009.
Manap, N., & Voulvoulis, N. (2014). Risk-based decision-making framework for the selection of sediment dredging option. Science of The Total Environment, 496, 607–623. https://doi.org/10.1016/j.scitotenv.2014.07.009.
Manap, N., & Voulvoulis, N. (2015). Environmental management for dredging sediments - the requirement of developing nations. Journal of Environmental Management, 147, 338–348. https://doi.org/10.1016/j.jenvman.2014.09.024.
Marques, A. N., Crapez, M. A. C., & Barboza, C. D. N. (2006). Impact of the Icarai Sewage Outfall in Guanabara Bay, Brazil. Brazilian Archives of Biology and Technology, 49, 643–650. https://doi.org/10.1590/S1516-89132006000500014.
Maranho, LA., Abreu, I., Santelli, R., et al (2009) Sediment toxicity assessment of Guanabara Bay, Rio de Janeiro, Brazil. J Coast Res SI:851–855
Mauad, C. R., Wagener A de, L. R., Massone, C. G., et al. (2015). Urban rivers as conveyors of hydrocarbons to sediments of estuarine areas: source characterization, flow rates and mass accumulation. Science of the Total Environment, 506–507, 656–666. https://doi.org/10.1016/j.scitotenv.2014.11.033.
Meniconi, G. M. (2002). Brazilian oil spills chemical characterization—case studies. Environmental Forensics, 3, 303–321. https://doi.org/10.1006/enfo.2002.0101.
Meyer-Reil, L.-L. (1994). Microbial life in sedimentary biofilms the challenge to microbial ecologists. Marine Ecology Progress Series, 112, 303–311. https://doi.org/10.3354/meps112303.
Meyer-Reil, L. A., & Köster, M. (2000). Eutrophication of marine waters: effects on benthic microbial communities. Marine Pollution Bulletin, 41, 255–263.
Miao, L., Wang, C., Hou, J., Wang, P., Ao, Y., Li, Y., Yao, Y., Lv, B., Yang, Y., You, G., Xu, Y., & Gu, Q. (2017). Response of wastewater biofilm to CuO nanoparticle exposure in terms of extracellular polymeric substances and microbial community structure. Science of the Total Environment, 579, 588–597. https://doi.org/10.1016/j.scitotenv.2016.11.056.
Monte, C. N., Rodrigues, A. P. C., Cordeiro, R. C., Freire, A. S., Santelli, R. E., & Machado, W. (2015). Changes in Cd and Zn bioavailability upon an experimental resuspension of highly contaminated coastal sediments from a tropical estuary. Sustainable Water Resources Management, 1, 335–342. https://doi.org/10.1007/s40899-015-0034-3.
Mora, A. P. d., Ortega-Calvo, J. J., Cabrera, F., & Madejón, E. (2005). Changes in enzyme activities and microbial biomass after “in situ” remediation of a heavy metal-contaminated soil. Applied Soil Ecology, 28, 125–137.
Moreau, J. W., Gionfriddo, C. M., Krabbenhoft, D. P., Ogorek, J. M., DeWild, J. F., Aiken, G. R., & Roden, E. E. (2015). The effect of natural organic matter on mercury methylation by Desulfobulbus propionicus 1pr3. Frontiers in Microbiology, 6. https://doi.org/10.3389/fmicb.2015.01389.
Mumtaz Moiz, M., Suk, W. A., & Yang, R. S. H. (2010). Introduction to mixtures toxicology and risk assessment. Principles and Practice of Mixtures Toxicology, 1–25. https://doi.org/10.1002/9783527630196.ch1.
Mustapha, M. U., & Halimoon, N. (2015). Microbial & biochemical technology microorganisms and biosorption of heavy metals in the environment: a review paper. Journal of Microbial & Biochemical Technology, 7, 253–256. https://doi.org/10.4172/1948-5948.1000219.
Nascimento, J. R., Bidone, E. D., Rolão-Araripe, D., Keunecke, K. A., & Sabadini-Santos, E. (2016a). Trace metal distribution in white shrimp (Litopenaeus schmitti) tissues from a Brazilian coastal area. Environment and Earth Science, 75. https://doi.org/10.1007/s12665-016-5798-8.
Nascimento, J. R., Sabadini-Santos, E., Carvalho, C., Keunecke, K. A., César, R., & Bidone, E. D. (2016b). Bioaccumulation of heavy metals by shrimp (Litopenaeus schmitti): a dose–response approach for coastal resources management. Marine Pollution Bulletin, 114, 1007–1013. https://doi.org/10.1016/j.marpolbul.2016.11.013.
Obbard, J. P., Sauerbeck, D., & Jones, K. C. (1994). Dehydrogenase activity of the microbial biomass in soils from a field experiment amended with heavy metal contaminated sewage sludges. Science of the Total Environment, 142, 157–162. https://doi.org/10.1016/0048-9697(94)90323-9.
Odum, E. P. (1985). Trends expected in stressed ecosystems. Bioscience, 35, 419–422. https://doi.org/10.2307/1310021.
Pianosi, F., Beven, K., Freer, J., Hall, J. W., Rougier, J., Stephenson, D. B., & Wagener, T. (2016). Environmental Modelling & Software Sensitivity analysis of environmental models : a systematic review with practical work flow. Environmental Modelling and Software, 79, 214–232. https://doi.org/10.1016/j.envsoft.2016.02.008.
Relexans, J. C., Lin, R. G., Castel, J., et al. (1992). Response of biota to sedimentary organic-matter quality of the west Gironde mud patch, Bay of Biscay (France). Oceanologica Acta, 15, 639–649.
Rosado, D., Usero, J., & Morillo, J. (2015). Application of a new integrated sediment quality assessment method to Huelva estuary and its littoral of influence (Southwestern Spain). Marine Pollution Bulletin, 98, 106–114. https://doi.org/10.1016/j.marpolbul.2015.07.008.
Sabadini-Santos, E., Silva, T. S., Lopes-Rosa, T. D., et al. (2014a). Microbial activities and bioavailable concentrations of Cu, Zn, and Pb in sediments from a tropic and eutrothicated bay. Water, Air, and Soil Pollution, 225. https://doi.org/10.1007/s11270-014-1949-2.
Sabadini-Santos, E., Senez, T. M., Silva, T. S., Moreira, M. R., Mendonça-Filho, J. G., Santelli, R. E., & Crapez, M. A. C. (2014b). Organic matter and pyritization relationship in recent sediments from a tropical and eutrophic bay. Marine Pollution Bulletin, 89, 220–228. https://doi.org/10.1016/j.marpolbul.2014.09.055.
Said, W. A., & Lewis, D. L. (1991). Quantitative assessment of the effects of metals on microbial degradation of organic chemicals. Applied and Environmental Microbiology, 57, 1498–1503.
Saxena, G., Marzinelli, E. M., Naing, N. N., He, Z., Liang, Y., Tom, L., Mitra, S., Ping, H., Joshi, U. M., Reuben, S., Mynampati, K. C., Mishra, S., Umashankar, S., Zhou, J., Andersen, G. L., Kjelleberg, S., & Swarup, S. (2015). Ecogenomics reveals metals and land-use pressures on microbial communities in the waterways of a megacity. Environmental Science & Technology, 49, 1462–1471. https://doi.org/10.1021/es504531s.
Shen G, Lu Y, Zhou Q, Hong J (2005) Hydrocarbons, interaction of polycyclic aromatic enzyme., and heavy metals on soil, Interaction of polycyclic aromatic hydrocarbons and heavy metals on soil enzyme.
Silva, F. S., da Costa Pereira, D., Nunez, L. S., et al. (2008). Bacteriological study of the superficial sediments of Guanabara Bay, RJ, Brazil AN - prod.academic_MSTAR_20208154; 8231133. Brazilian Journal of Oceanography, 56, 13–22. https://doi.org/10.1590/S1679-87592008000100002.
Silveira, A. E. F., Nascimento, J. R., Sabadini-santos, E., & Bidone, E. D. (2017). Screening-level risk assessment applied to dredging of polluted sediments from. Marine Pollution Bulletin, 118, 368–375. https://doi.org/10.1016/j.marpolbul.2017.03.016.
Soares-Gomes, A., da Gama, B. A. P., Baptista-Neto, J. A., et al. (2015). An environmental overview of Guanabara Bay, Rio de Janeiro. Regional Studies in Marine Science, 8, 319–330. https://doi.org/10.1016/j.rsma.2016.01.009.
Steffan, S. A., Chikaraishi, Y., Currie, C. R., Horn, H., Gaines-Day, H. R., Pauli, J. N., Zalapa, J. E., & Ohkouchi, N. (2015). Microbes are trophic analogs of animals. Proceedings of the National Academy of Sciences, 112, 15119–15124. https://doi.org/10.1073/pnas.1508782112.
Stubberfield, L. C. E., & Shaw, P. J. A. (1990). A comparison of tetrazolium reduction and FDA\nhydrolysis with other measures of microbial\nactivity. Journal of Microbiological Methods, 12, 151–162.
Su, H., Pan, C., Ying, G., et al. (2014). Contamination profiles of antibiotic resistance genes in the sediments at a catchment scale. Science of the Total Environment, 490, 708–714. https://doi.org/10.1016/j.scitotenv.2014.05.060.
Trevors, J. T., Mayfield, C. I., & Inniss, W. E. (1982). Measurement of electron transport system (ETS) activity in soil. Microbial Ecology, 8, 163–168. https://doi.org/10.1007/BF02010449.
US EPA. (2002). Methods for the determination of total organic carbon in soils and sediments. United States Environ Prot Agency, 32, 25 http://epa.gov/esd/cmb/research/papers/bs116.pdf Accessed 20 September 2018.
Van Beelen, P., & Doelman, P. (1997). Significance and application of microbial toxicity tests in assessing ecotoxicological risks of contaminants in soil and sediment. Chemosphere, 34, 455–499. https://doi.org/10.1016/S0045-6535(96)00388-8.
Waite, C. C. d. C., da Silva, G. O. A., Bitencourt, J. A. P., Sabadini-Santos, E., & Crapez, M. A. C. (2016). Copper and lead removal from aqueous solutions by bacterial consortia acting as biosorbents. Marine Pollution Bulletin, 109, 386–392. https://doi.org/10.1016/j.marpolbul.2016.05.044.
Wang, Y., Shi, J., Wang, H., Lin, Q., Chen, X. C., & Chen, Y. X. (2007). The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicology and Environmental Safety, 67, 75–81. https://doi.org/10.1016/j.ecoenv.2006.03.007.
WHO – World Health Organization (2018) International programme on chemical safety. https://www.who.int/ipcs/en/ Accessed 26 April 2018.
Wilken, R.-D., Moreira, I., & Rebello, A. (1986). 210Pb and 137Cs fluxes in a sediment core from Guanabara Bay, Brazil. Science of The Total Environment, 58, 195–198. https://doi.org/10.1016/0048-9697(86)90088-4.
Acknowledgments
The authors appreciate the support from the staff of Laboratorio de Processos em Ecologia Microbiana (Universidade Federal Fluminense-UFF), Laboratorio de Palinofacies e Facies Orgânicas, and Laboratorio de Desenvolvimento Analítico (both from Universidade Federal do Rio de Janeiro-UFRJ) during data acquisition.
Funding
The authors are thankful to the National Council for Scientific and Technological Development (CNPq) for financial support (universal process no. 449631/2014-1) and for providing a doctoral fellowship to the first author. The authors also thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support.
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Nascimento, J.R., Silveira, A.E.F., Bidone, E.D. et al. Microbial community activity in response to multiple contaminant exposure: a feasible tool for sediment quality assessment. Environ Monit Assess 191, 392 (2019). https://doi.org/10.1007/s10661-019-7532-y
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DOI: https://doi.org/10.1007/s10661-019-7532-y