Skip to main content

Advertisement

Log in

Microbial Activities and Bioavailable Concentrations of Cu, Zn, and Pb in Sediments from a Tropic and Eutrothicated Bay

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Stressed communities show changes in energetics and nutrient demand and recovery. The evaluation of microbial communities energy demand can be measured by enzyme activities. Thus, by using such approaches, it might be possible to determine the microbial response to metal contaminations. Guanabara Bay surface sediments were sampled in 20 stations. Grain size, bioavailable metals, total organic carbon, total sulfur, dehydrogenase activity, esterase activities, viable bacterial cells, carbohydrates, lipids, and proteins were determined in all samples. Bioavailable metal concentration ranges from below detection limit in sandy stations in the entrance of the bay by up to the same order of magnitude as total concentrations obtained by other authors. Biopolymers were mainly lipids and carbohydrates, and minimum concentrations were also observed in sandy sediments. C:S ratio of 4.4 ± 1.3 (mean ± standard deviation) expresses the reduced tendency conditions of the bay, negatively correlated to viable bacteria cells (in order of 107 cell g−1). Esterase enzyme activities positively correlated with organic and fine sediment content. Stations with the highest metals and organic contents also have the highest esterase activities and dramatic decline of bacterial cells. In these locations occur better water renewal and subsequent aeration, which increases the efficiency of the organic matter oxidation and decreases matrix geochemical sequestration of metals and renders them bioavailable.

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

Similar content being viewed by others

References

  • American Society for Testing and Materials (ASTM), 2008. Standard test methods for Sulfur in the analysis sample of coal and coke using high-temperature tube furnace combustion methods ASTMD 4239. Available on http://engineers.ihs.com/documents/abstract/NWETIBA. Accessed 22 Nov 2013

  • Anderson, T. H., & Domsch, K. H. (2010). Soil microbial biomass: the eco-physiological approach. Soil Biology & Biochemistry, 42, 2039–2043.

    Article  CAS  Google Scholar 

  • 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, 46, 1051–1063.

    Article  Google Scholar 

  • Beelen, P. V., & Doelman, P. (1997). Significance and application of microbial toxicity tests in assessing ecotoxicological risks of contaminants in soil and sediment. Chemosphere, 34, 445–499.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Birch, G. F., & Hogg, T. D. (2011). Sediment quality guidelines for copper and zinc for filter-feeding estuarine oysters? Environmental Pollution, 159, 108–115.

    Article  CAS  Google Scholar 

  • Carreira, R. S., Wagener, A. L. R., Readman, J. W., Fileman, T. W., Macko, S. A., & Veiga, A. (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.

    Article  CAS  Google Scholar 

  • Carreira, R. S., Wagener, A. L. R., & Readman, J. W. (2004). Sterols as markers of sewage contamination in a tropical urban estuary (Guanabara Bay, Brazil): space time evariations. Estuarine, Coastal and Shelf Science, 60, 587–598.

    Article  CAS  Google Scholar 

  • Cezar, A., Pereira, C. D. S., Santos, A. R., Abessa, D. M. S., Choueri, R. B., Riba, I., et al. (2007). Comparative sediment quality assessment in different littoral ecosystems from Spain (Gukf of Cadiz) and Brazil (Santos and São Vicente estuarine system). Environmental International, 33, 429–435.

    Article  Google Scholar 

  • Cividanes, S., Incera, M., & Lopez, J. (2002). Temporal variability in the biochemical composition of sedimentary organic matter in an intertidal flat of the Galician coast (NW Spain). Oceanologica Acta, 25, 1–12.

    Article  CAS  Google Scholar 

  • Cotano, U., & Villate, F. (2006). Anthropogenic influence on the organic fraction of sediments in two contrasting estuaries: a biochemical approach. Marine Pollution Bulletin, 52, 404–414.

    Article  CAS  Google Scholar 

  • 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 (Guanabara Bay). Anuário do Instituto de Geociências – UFRJ, 26, 58–64.

    Google Scholar 

  • Danovaro, R., Fabiano, M., & Della Croce, N. (1993). Labile organic matter and microbial biomasses in deep-sea sediments (Eastern Mediterranean Sea). Deep-Sea Research I, 40, 953–965.

    Article  CAS  Google Scholar 

  • Decho, A. W. (2000). Microbial biofilms in intertidal systems: an overview. Continental Shelf Research, 20, 1257–1273.

    Article  Google Scholar 

  • Dell’ Anno, A., Mei, M. L., Pusceddu, A., & Danovaro, R. (2002). Assessing the thropic state and eutrophication of coastal marine systems. A new approach based on the biochemical composition of sediment organic matter. Marine Pollution Bulletin, 44, 611–622.

    Article  Google Scholar 

  • Demaison, G. J., & Moore, G. T. (1980). Anoxic environments and oil source bed genesis. Organic Geochemistry, 2, 9–13.

    Article  CAS  Google Scholar 

  • Díaz, E., Valencia, V., & Villate, F. (2007). Size-fractionated seston abundance and biochemical composition, over the anchovy spawning period in the Basque shelf (Bay of Biscay), during years 2000 and 2001. Journal of Experimental Marine Biology and Ecology, 341, 45–59.

    Article  Google Scholar 

  • Dubois, M., Gilles, K., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.

    Article  CAS  Google Scholar 

  • Edwards, K. J., Bach, W., & McCollom, T. M. (2005). Geomicrobiology in oceanography: microbe–mineral interactions at and below the seafloor. Trends Microbiology, 13, 449–455.

    Article  CAS  Google Scholar 

  • Fabiano, M., Danovaro, R., & Fraschetti, S. (1995). A three-year time series of elemental and biochemical composition of organic matter in subtidal sediments of the Ligurian Sea (northwestern Mediterranean). Continental Shelf Research, 15, 1453–1469.

    Article  Google Scholar 

  • FEEMA (2000). Qualidade de Água da Baía de Guanabara. Estatística Básica 1990/1999. Rio de Janeiro: Secretaria de Estado de Meio Ambiente e Desenvolvimento Sustentável.

  • Fenchel, T., King, G. M. & Blackburn, T. H. (1988). Bacterial biogeochemistry: the ecophysiology of mineral cycling. 2ª ed. Academic Press.

  • Flemming, H. C., & Wingender, J. (2010). The Biofilm Matrix. Nature Reviews, 8, 623–633.

    CAS  Google Scholar 

  • Fonseca, E. M., Baptista Neto, J. A., Silva, C. G., McAlister, J. J., Smith, B. J., & Fernandez, M. A. (2013). Sotrmwater impact in Guanabara Bay (Rio de Janeiro): evidences of seasonal variability in the dynamic of the sediment heavy metals. Estuarine, Coastal and Self Science, 130, 161–168.

    Article  CAS  Google Scholar 

  • Fontana, L. F., Mendonça-Filho, J. G., Pereira Netto, A. D., Sabadini-Santos, E., Figueiredo, A. G., Jr., & Crapez, M. A. C. (2010a). Geomicrobiology of cores from Suruí Mangrove – Guanabara Bay – Brazil. Marine Pollution Bulletin, 60, 1674–1681.

    Article  CAS  Google Scholar 

  • Fontana, L. F., Silva, F. S., Figueiredo, N. G., Brum, D. M., Pereira Netto, A. D., Figueiredo, A. G., Jr., et al. (2010b). Superficial distribution of aromatic compounds and geomicrobiology of sediments from Suruí Mangrove, Guanabara Bay, RJ, Brazil. Anais da Academia Brasileira de Ciências, 82, 1013–1030.

    Article  Google Scholar 

  • Forstner, U., & Salomons, W. (1980). Trace element analysis on polluted sediments, part I: assessment of sources and intensities. Environmental Technology Letters, 1, 494–505.

    Article  Google Scholar 

  • Fundação Superintendência Estadual de Rios e Lagoas -SERLA (2005). Plano diretor de recursos hídricos da região hidrográfica da Baía de Guanabara. Rio de Janeiro, RJ: SERLA.

  • Gerchacov, S. M., & Hachter, P. G. (1972). Improved technique for analysis of carbohydrates in sediment. Limnology and Oceanography, 17, 938–943.

    Article  Google Scholar 

  • Harrison, J. J., Turner, R. J., Marques, L. L. R., & Ceri, H. (2005). Biofilms: a new understanding of these microbial communities is driving a revolution that may transform the science of microbiology. American Scientist, 93, 508–515.

    Article  Google Scholar 

  • Harrison, J. J., Ceri, H., & Turner, R. J. (2007). Multimetal resistance and tolerance in microbial biofilms. Nature, 5, 928–938.

    CAS  Google Scholar 

  • Hartree, E. F. (1972). Determination of proteins: a modification of the Lowry method that give a linear photometric response. Analytical Biochemistry, 48, 422–427.

    Article  CAS  Google Scholar 

  • Huerta-Diaz, M. A., & Morse, J. W. (1990). A quantitative method for determination of trace metal concentration in sedimentary pyrite. Marine Chemistry, 29, 119–144.

    Article  CAS  Google Scholar 

  • Japan Internacional Cooperation Agency - JICA (2003). The study on management and improvement of the environmental conditions of Guanabara bay of Rio de Janeiro, The Federative Republic of Brazil Rio de Janeiro,RJ: JICA and the State Secretariat of Environment and Urban Developmen.

  • Keil, R. G., & Kirchman, D. L. (1994). Abiotic transformation of labile protein to refractory protein in seawater. Marine Chemistry, 45, 187–196.

    Article  CAS  Google Scholar 

  • Kepner, J., & Pratt, J. R. (1994). Use of fluorochromes for direct enumerations of total bacteria in environmental samples: past and present. Microbiological Reviews, 58, 603–615.

    CAS  Google Scholar 

  • Kjerfve, B., Ribeiro, C. H. A., Dias, G. T. M., FiLPDpo, A. M., & Quaresma, V. S. (1997). Oceanographic characteristics of an impacted coastal bay: Baía de Guanabara, Rio de Janeiro, Brazil. Continental Shelf Research, 17, 1609–1643.

    Article  Google Scholar 

  • Kjerfve, B., Lacerda, D. & Dias, G. T. M. (2001). Baia de Guanabara, Rio De Janeiro, Brazil. In: U. Seeliger & B. Kjerfve, (Eds.), Coastal marine ecosystems of Latin America: Ecological studies Berlin: Springer, p. 107– 117.

  • Lewis, K. (2007). Persister cells, dormancy and infectious disease. Nature Reviews Microbiology, 5, 48–56.

    Article  CAS  Google Scholar 

  • Machado, W. T. V., Rodrigues, A. P. C., Bidone, E. D., Sella, S. M., & Santelli, R. E. (2011). Evaluation of Cu potential bioavailability changes upon coastal sediment resuspension: an example on how to improve the assessment of sediment dredging environmental risks. Environmental Science and Pollution Research, 18, 1033–1036.

    Article  CAS  Google Scholar 

  • Maranho, L. A., Abreu, I., Santelli, R. E., Cordeiro, R. C., Soares-Gomes, A., Moreira, L. B., et al. (2009). Sediment toxicity assessment of Guanabara Bay, Rio de Janeiro, Brazil. Journal of Coastal Research, 56, 851–855.

    Google Scholar 

  • Marques, A. N., Jr., Crapez, M. A. C., & Barboza, C. D. N. (2006). Impact of the Icaraí Sewage Outfall in Guanabara Bay, Brazil. Brazilian Archives Biology and Technology, 49, 643–650.

    Article  CAS  Google Scholar 

  • Marsh, B. J., & Weinstein, D. B. (1966). Simple charring method for determination of LPDids. Journal of LPDid Research, 7, 574–576.

    CAS  Google Scholar 

  • Meyer-Reil, L. A. (1994). Microbial life in sedimentary biofilms – the challenge to microbial ecologists. Marine Ecology Progress Series, 112, 303–311.

    Article  Google Scholar 

  • Meyer-Reil, L. A., & Köster, M. (2000). Eutrophication of marine waters: effects on benthic microbial communities. Marine Pollution Bulletin, 41, 255–263.

    Article  CAS  Google Scholar 

  • Milligan, G. W., & Cooper, M. C. (1985). An examination of procedures for determining the number of clusters in a data set. Psychometrika, 50, 159–179.

    Article  Google Scholar 

  • Monteiro, F. F., Cordeiro, R. C., Santelli, R. E., Machado, W., Evangelista, E., Villar, L. S., et al. (2012). Sedimentary geochemical record of historical anthropogenic activities affecting Guanabara Bay (Brazil) environmental quality. Environmental Earth and Science, 65, 1661–1669.

    Article  CAS  Google Scholar 

  • Morse, J. W. (1994). Interactions of trace metals with authigenic sulfide minerals: implications for their bioavailability. Marine Chemistry, 46, 1–6.

    Article  CAS  Google Scholar 

  • Newell, R. C., & Field, J. G. (1983). The contribution of bacteria and detritus to carbon and nitrogen flow in a benthic community. Marine Biological Letters, 4, 23–36.

    Google Scholar 

  • Odum, E. P. (1969). The strategy of ecosystem development. Science, 164, 262–270.

    Article  CAS  Google Scholar 

  • Odum, E. P. (1985). Trends expected in stressed ecosystems. Bioscience, 35, 419–422.

    Article  Google Scholar 

  • Peres-Neto, P. R., Jackson, D. A., & Somers, K. M. (2003). Giving meaningful interpretation to ordination axes: assessing loading significance in principal component analysis. Ecology, 84, 2347–2363.

    Article  Google Scholar 

  • Perez, T., Longet, D., Schembri, T., Rebouillon, P., & Vacelet, J. (2005). Effects of 12 years operation of a sewage treatment plant on trace metal occurrence within a Mediterranean commercial sponge (Spongia officinalis, Demospongiae). Marine Pollution Bulletin, 50, 301–309.

    Article  CAS  Google Scholar 

  • Perin, G., Fabris, R., Manente, S., Rebello, A. W., Hamacher, C., & Scotto, S. (1997). A five-year study on the heavy-metal pollution of Guanabara Bay sediments (Rio de Janeiro, Brazil) and evaluation of the metal bioavailability by averages of geochemical speciation. Water Research, 31, 3017–3028.

    Article  CAS  Google Scholar 

  • Pinturier-Geiss, L. L., Mejanelle, L., Dale, B., & Karlsen, D. A. (2002). LPDids as indicators of eutrophication in marine coastal sediments. Journal of Microbiological Methods, 48, 239–257.

    Article  CAS  Google Scholar 

  • Pusceddu, A., Dell’Anno, A., Danovarto, R., Manini, E., Sara, G., & Fabiano, M. (2003). Enzymatically hydrolysable protein and carbohydrate sedimentary pools as indicators of the trophic state of detritus sink systems: a case study in a Mediterranean Coastal Lagoon. Estuaries, 26, 641–650.

    Article  CAS  Google Scholar 

  • Rebello, A. L., & Van Den Berg, C. (1986). Organic copper interaction in Guanabara Bay. The Science of the Total Environment, 58, 37–45.

    Article  Google Scholar 

  • Rebello, A. L., Haekel, W., Moreira, I., & Santelli, R. (1986). The fate of heavy metals in an estuarine tropical system. Marine Chemistry, 18, 215–225.

    Article  CAS  Google Scholar 

  • Relexans, J. C., Lin, R. G., Castel, J., Etcheber, H., & Laborde, P. (1992). Response of biota to sedimentary organic matter quality of the West Gironde mud patch, Bay of Biscay (France). Oceanologica Acta, 15, 639–649.

    CAS  Google Scholar 

  • Roszak, D. B., & Coldwell, R. R. (1987). Survival strategies of bacteria in the natural environment. Microbiological Reviews, 51, 365–379.

    CAS  Google Scholar 

  • Ruiz, F. (2001). Trace metals in estuarine sediments from the southwestern Spanish coast. Marine Pollution Bulletin, 42, 482–490.

    CAS  Google Scholar 

  • Santos, E. S., Carreira, R. C., & Knoppers, B. A. (2008). Sedimentary sterols as indicators of environmental conditions in Southeastern Guanabara Bay, Brazil. Brazilian Journal of Oceanography, 56, 97–113.

    Google Scholar 

  • Silva, F. S., Pereira, D. C., Nuñez, L. S., Krepsk, N., Fontana, L. F., Baptista-Neto, J. A., et al. (2008). Bacteriological study of the superficial sediments of Guanabara bay, RJ, Brazil. Brazilian Journal of Oceanography, 56, 13–22.

    Article  Google Scholar 

  • Silveira, R. P., Rodrigues, A. P. C., Santelli, R. E., Cordeiro, R. E., Cordeiro, R. C., & Bidone, E. D. (2011). Mass balance in the monitoring of pollutants in tidal rivers of the Guanabara Bay, Rio de Janeiro, Brazil. Environmental Monitoring and Assessment, 181, 165–173.

    Article  CAS  Google Scholar 

  • Snape, I., Scouller, R. C., Stark, S. C., Stark, J., Riddle, M. J., & Gore, D. B. (2004). Characterisation of the dilute HCl extraction method for the identification of metal contamination in Antarctic marine sediments. Chemosphere, 57, 491–504.

    Article  CAS  Google Scholar 

  • Sokolowski, A., Wolowicz, M., & Hummel, H. (2007). Metal sources to the Baltic clam Macoma balthica (Mollusca: Bivalvia) in the southern Baltic Sea (the Gulf of Gdansk). Marine Environmental Research, 63, 236–256.

    Article  CAS  Google Scholar 

  • Spencer, K. L. (2002). Spatial variability of metals in the inter-tidal sediments of the meadway estuary, Kent, UK. Marine Pollution Bulletin, 44, 933–944.

    Article  CAS  Google Scholar 

  • Stubberfield, L. C. F., & Shaw, P. J. A. (1990). Enzymatically hydrolyzable protein and carbohydrate sedimentary pools as indicators of the trophic state of detritus sink systems: a case study in a Mediterranean Coastal Lagoon. Journal of Microbial Methods, 12, 151–162.

    Article  CAS  Google Scholar 

  • Trevors, J. (1984). Effect of substrate concentration, inorganic nitrogen, O2 concentration, temperature and pH on dehydrogenase activity in soil. Water Research, 77, 285–293.

    CAS  Google Scholar 

  • United States Environmental Protection Agency (U.S.EPA) (2002). Methods for the determination of total organic carbon (TOC) in soils and sediments. Ecological Risk Assessment Support Center. NCEA-C-1282. Office of Research and Development, Las Vegas.

  • Vezzulli, L., & Fabiano, M. (2006). Sediment biochemical and microbial variables for the evaluation of trophic status along the Italian and Albanian continental shelves. Journal of Marine Biological Association of the United Kingdom, 86, 27–37.

    Article  CAS  Google Scholar 

  • Ziervogel, K., Karlsson, E., & Arnosti, C. (2007). Surface associations of enzymes and of organic matter: consequences for hydrolytic activity and organic matter remineralization in marine systems. Marine Chemistry, 104, 241–252.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the staff of the Laboratory of Marine Microbiology from Fluminense Federal University by microbial analysis in sampling data. The authors also thank a master grant from the Brazilian Research Council (CNPq) to T. S. da Silva and two anonymous reviewers that provided valuable comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elisamara Sabadini-Santos.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sabadini-Santos, E., da Silva, T.S., Lopes-Rosa, T.D. et al. Microbial Activities and Bioavailable Concentrations of Cu, Zn, and Pb in Sediments from a Tropic and Eutrothicated Bay. Water Air Soil Pollut 225, 1949 (2014). https://doi.org/10.1007/s11270-014-1949-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-014-1949-2

Keywords

Navigation