Abstract
The bioremediation potential of microorganisms from a saltmarsh plant rhizosphere and application of bioaugmentation in estuarine sediment co-contaminated were investigated. Rhizosediment (sediment in contact with plant roots) of Juncus maritimus was contaminated with copper and/or petroleum, inoculated with different autochthonous microbial consortia (resistant to copper and/or with petroleum degraders) and put in vessels to which plants were transplanted. Vessels were irrigated through a system that simulated estuarine tides. After 5 months, vessels were dismantled and copper and petroleum content in rhizosediments were determined. Copper’s presence reduced the potential of the microorganisms associated to J. maritimus rhizosphere for bioremediation of petroleum hydrocarbons in co-contaminated sediment. Indeed, hydrocarbons removal decreased from 39 to 25% when copper was present. In addition, bioaugmentation was not effective to overcome metal negative effects on petroleum hydrocarbons degradation, and the same removal rate was being observed (ca. 25%). Different methodologies for the formulation of consortia must be tested in this situation of co-contamination. Obtained results should be taken in consideration when planning the recovery of moderately impacted estuaries, aiming an effective protection and management of these areas, in the case of co-contamination.
Similar content being viewed by others
References
Agarwal A, Liu Y (2015) Remediation technologies for oil-contaminated sediments. Mar Pollut Bull 101:483–490
Akpoveta OV, Egharevba F, Medjor GW (2011) A pilot study on the biodegradation of hydrocarbon and its kinetics on kerosene simulated soil. Intern J Environ Sci 2:54–67
Alisi C, Musella R, Tasso F, Ubaldi C, Manzo S, Cremisni C, Sprocati NA (2009) Bioremediation with a microbial formula tailored with native strains selected for heavy metals resistance. Sci Total Environ 407:3024–3032
Almeida CMR, Mucha AP, Vasconcelos MTSD (2004) Influence of the sea rush Juncus maritimus on metal concentration and speciation in estuarine sediment colonized by the plant. Environ Sci Technol 38:3112–3118
Almeida CMR, Mucha AP, Delgado MFC, Caçador M, Bordalo AA, Vasconcelos MTSD (2008) Can PAHs influence Cu accumulation by salt marsh plants? Mar Environ Res 66:311–318
Almeida CMR, Mucha AP, Vasconcelos MT (2011) Role of different salt marsh plants on metal retention in an urban estuary (Lima estuary, NW Portugal). Estuar Coast Shelf Sci 91:243–249
Almeida R, Mucha AP, Teixeira C, Bordalo AA, Almeida CMR (2013) Bioremediation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24:111–123
Almeida CMR, Couto N, Ribeiro H, Mucha AP, Bordalo A, Basto MC, Vasconcelos MTSD (2015) Salt marsh plants’ potential for the remediation of hydrocarbons-contaminated environments. In: Ansari AA, Gill SS, Gill R, Lanza GR, Newman L (eds) Phytoremediation: management of environmental contaminants, vol 1. Springer, Berlin, pp 323–331. doi:10.1007/978-3-319-10395-2_23
Amor L, Kennes C, Veiga MC (2001) Kinetics of inhibition in the biodegradation of monoaromatic hydrocarbons in presence of heavy metals. Bioresour Technol 78:181–185
Atagana HI (2006) Bioremediation of polycyclic aromatic hydrocarbons in contaminated soil by biostimulation and biaugmention in the presence of copper(II) ions. World J Microb Biot 22:1145–1153
Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of high-molecular-weight polycyclic aromatic hydrocarbons by defined fungal–bacterial cocultures. Appl Environ Microb 66:1007–1019
Bouchez M, Blanchet D, Bardin V, Haeseler F, Vandecasteele JP (1999) Efficiency of defined strains and of soil consortia in the biodegradation of polycyclic aromatic hydrocarbon (PAH) mixtures. Biodegradation 10:429–435
Chigbo C, Batty L, Bartlett R (2013) Interactions of copper and pyrene on phytoremediation potential of Brassica juncea in copper–pyrene co-contaminated soil. Chemosphere 90:2542–2548
Colombo M, Cavalca L, Bernasconi S, Andreoni V (2011) Bioremediation of polyaromatic hydrocarbon contaminated soils by microflora and bioaugmentation with Sphingobium chlorophenolicum strain C3R: a feasibility study in solid- and slurry-phase microcosms. Int Biodeter Biodegr 65:191–197
Couto MN, Borges JR, Guedes P, Almeida R, Monteiro E, Almeida CMR, Basto MCP, Vasconcelos MTSD (2014) An improved method for determination of petroleum hydrocarbons from soil using a simple ultrasonic extraction and Fourier transform infrared spectrophotometry. Pet Sci Technol 32:426–432
Dobler R, Saner M, Bachofen R (2000) Population changes of soil microbial communities induced by hydrocarbon and metal contamination. Bioremediat J 4:41–56
Doelman P, Jansen E, Michels M, Van Til M (1994) Effect of heavy metals in soil on microbial diversity and activity as shown by the sensitivity-resistance index, an ecologically relevant parameter. Biol Fert Soils 17:177–184
Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30
Gutiérrez-Ginés MJ, Hernández AJ, Pérez-Leblic MI, Vangronsveld J (2014) Phytoremediation of soils co-contaminated by organic compounds and heavy metals: biossays with Lupinus luteus L. and associated endophytic bacteria. J Environ Manag 143:197–207
Hechmi N, Aissa NB, Abdenaceur H, Jedidi N (2015) Uptake and bioaccumulation of pentachlorophenol by emergent wetland plant Phragmites australis (Common reed) in cadmium co-contaminated soil. Int J Phytoremediat 17:109–116
Hoffman DR, Okon JL, Sandrin TR (2005) Medium composition affects the degree and pattern of cadmium inhibition of naphthalene biodegradation. Chemosphere 59:919–927
Hoffman DR, Anderson PP, Schubert CM, Gault MB, Blanford WJ, Sandrin TR (2010) Carboxymethyl-β-cyclodextrin mitigates toxicity of cadmium, cobalt, and copper during naphthalene biodegradation. Bioresour Technol 101:2672–2677
Hosokawa R, Nagai M, Morikawa M, Okuyama H (2009) Autochthonous bioaugmentation and its possible application to oil spills. World J Microb Biotechnol 25:1519–1528
Karthikeyan R, Kulakow PA (2003) Soil plant microbe interactions in phytoremediation. In: Scheper T (ed) Phytoremediation: advances in biochemical engineering/biotechnology, vol 78. Springer, Berlin, pp 53–64
Kuppusamy S, Thavamani P, Megharaj M, Naidu R (2016) Biodegradation of polycyclic aromatic hydrocabons (PAHS) by novel bacterial consortia tolerant to diverse physical settings—assessments in liquid- and slurry-phase systems. Int Biodeterior Biodegrad 108:149–153
Lefeuvre J-C, Laffaille P, Feunteun E, Bouchard V, Radureau A (2003) Biodiversity in salt marshes: from patrimonial value to ecosystem functioning. The case study of the Mont-Saint-Michel bay. C R Biol 326:125–131
Lin Q, Wang Z, Ma S, Chen Y (2006) Evaluation of dissipation mechanisms by Lolium perenne L., and Raphanus sativus for pentachlorophenol (PCP) in copper co-contaminated soil. Sci Total Environ 368:814–822
Lin Q, Shen KL, Zhao HM, Li WH (2008) Growth response of Zea mays L. in pyrene-copper co-contaminated soil and the fate of the pollutants. J Hazard Mater 150:515–521
Long ER, MacDonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manag 19:81–97
Lorah MM, Majcher EH, Jones EJ, Voytek MA (2008) Microbial consortia development and microcosm and column experiments for enhanced bioremediation of chlorinated volatile organic compounds, west branch canal creek wetland area, Aberdeen Proving Ground, Maryland, U.S. Geological Survey Scientific Investigations Report 2007-5165. http://md.water.usgs.gov/publications/sir.html
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Nadia R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:1357–1362
Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14:10197–10228
Oliveira T, Mucha AP, Reis I, Rodrigues P, Gomes CR, Almeida CMR (2014) Copper phytoremediation by salt marsh plant (Phragmites australis) enhanced by autochthonous bioaugmentation. Mar Pollut Bull 88:231–238
Peixoto RS, Vermelho AB, Rosado AS (2011) Petroleum-degrading enzymes: bioremediation and new prospects. Enzyme Res 2011:1–7
Pepper IL, Gentry TJ, Newby DT, Roane TM, Josephson KL (2002) The role of cell bioaugmentation and gene bioaugmentation in the remediation of co-contaminated soils. Environ Health Perspect 110:943–946
Pontes J, Mucha AP, Santos H, Reis I, Bordalo A, Bastos MC, Bernabeu A, Almeida CMR (2013) Potential of bioremediation for buried oil removal in beaches after an oil spill. Mar Pollut Bull 76:258–265
Rani R, Juwarkar A (2013) Interactions between plant growth promoting microbes and plants: implications for microbe-assisted phytoremediation of metal-contaminated soil. In: Leung DWM (ed) Recent advances towards improved phytoremediation of heavy metal pollution. Bentham Science Publishers, Sharjah, pp 3–39
Rauret G, López-Sánchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller Ph (1999) Improvement of the BCR three step sequential extraction procedure prior to the certification of the new sediment and soil reference materials. J Environ Monitor 1:57–61
Ribeiro H, Mucha AP, Almeida CMR, Bordalo AA (2011) Hydrocarbon degradation potential of salt marsh plant–microorganisms associations. Biodegradation 224:729–739
Ribeiro H, Almeida CMR, Mucha AP, Teixeira C, Bordalo AA (2013) Influence of natural rhizosediments characteristics on hydrocarbons degradation potential of microorganisms associated to Juncus maritimus roots. Int Biodeterior Biodegrad 84:86–96
Ribeiro H, Mucha AP, Almeida CMR, Bordalo AA (2014) Potential of phytoremediation for the removal of petroleum hydrocarbons in contaminated salt marsh sediments. J Environ Manag 137:10–15
Riis V, Babel W, Pucci OH (2002) Influence of heavy metals on the microbial degradation of diesel fuel. Chemosphere 49:559–568
Roane TM, Josephson KL, Pepper IL (2001) Dual-bioaugmentation strategy to enhance remediation of co-contaminated soil. Appl Environ Microb 67:3208–3215
Said WA, Lewis DL (1991) Quantitative assessment of the effects of metals on microbial degradation of organic chemicals. Appl Environ Microb 57:1498–1503
Sandrin TR, Hoffman DR (2007) Bioremediation of organic and metal co-contaminated environments: effects of metal toxicity, speciation and bioavailability on biodegradation. In: Singh SN, Tripathi RD (eds) Environmental bioremediation technologies. Springer, Berlin, pp 1–34
Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101
Sandrin TR, Chech AM, Maier RM (2000) A rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microb 66:4585–4588
Shilev S, Kuzmanova I, Sancho E (2009) Phytotechnologies: how plants and bacteria work together. In: Baveye P, Laba M, Mysiak J (eds) Uncertainties in environmental modelling and consequences for policy making. Springer, Netherlands, pp 385–397
Singer AC, Bell T, Heywood CA, Smith JAC, Thompson IP (2007) Phytoremediation of mixed-contaminated soil using the hyperaccumulator plant Alyssum lesbiacum: evidence of histidine as a measure of phytoextractable nickel. Environ Pollut 147:74–82
Sprocati AR, Alisi C, Tasso F, Marconi P, Sciullo A, Pinto V, Chiavarini S, Ubaldi C, Cremisini C (2012) Effectiveness of a microbial formula, as a biaugmentation agent, tailored for bioremediation of diesel oil and heavy metal co-contaminated soil. Process Biochem 47:1649–1655
Sun YB, Zhou QX, Xu YM, Wang L, Liang XF (2011) Phytoremediation for co-contaminated soils of benzo[a]pyrene (B[a]P) and heavy metals using ornamental plant Tagetes patula. J Hazard Mater 186:2075–2082
Teixeira C, Almeida CMR, Nunes da Silva M, Bordalo AA, Mucha AP (2014) Development of autochthonous microbial consortium of enhanced of salt-marsh sediments contaminated with cadmium. Sci Total Environ 493:757–765
Thompson IP, Van Der Gast CJ, Ciric L, Singuer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915
Vogel TM (1996) Bioaugmentation as a soil bioremediation approach. Curr Opin Biotechnol 7:311–316
Wang J, Zhang Z, Su Y, He F, Song H (2008) Phytoremediation of petroleum polluted soil. Pet Sci 5:167–171
Wang K, Zhu Z, Huang H, Li T, He Z, Yang X, Alva A (2012) Interactive effects of Cd and PAHs on contaminants removal from co-contaminated soil planted with hyperaccumulator plant Sedum alfredii. J Soils Sedim 12:554–564
Weyens N, Truyens S, Saenen E, Boulet J, Dupae J, Taghavi S, van der Lelie D, Carleer R, Vangronsveld J (2011) Endophytes and their potential to deal with co-contamination of organic contaminants (Toluene) and toxic metals (Nickel) during phytoremediation. Int J Phytoremediat 13:244–255
Young LY, Liang W, Shor L, Kosson D, Rochne K, Taghon G (2002) Bioavailability of PAHs to bacteria in estuarine sediment. Soil Sediment Contam 11:488
Zhang H, Dang Z, Zheng LC, Yi XY (2009) Remediation of soil co-contaminated with pyrene and cadmium by growing maize (Zea mays L.). Int J Environ Sci Technol 6:249–258
Zhang ZH, Rengel Z, Meney K, Pantelic L, Tamanovic R (2011) Polynuclear aromatic hydrocarbons (PAHs) mediate cadmium toxicity to an emergent wetland species. J Hazard Mater 189:119–126
Acknowledgements
To Rayra Santiago, Tânia Oliveira, Tatiana Necrasov, Catarina Magalhães for their help in the experiments assembling and dismantling of the vessels. This research was partially supported by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020 and by the structured Program of R&D&I INNOVMAR—Innovation and Sustainability in the Management and Exploitation of Marine Resources, reference NORTE-01-0145-FEDER-000035, namely within the Research Line ECOSERVICES (Assessing the environmental quality, vulnerability and risks for the sustainable management of the NW coast natural resources and ecosystem services in a changing world) within the R&D Institution CIIMAR (Interdisciplinary Centre of Marine and Environmental Research), supported by the Northern Regional Operational Programme (NORTE2020), through the European Regional Development Fund (ERDF).
Author information
Authors and Affiliations
Corresponding author
Additional information
Editorial responsibility: J Aravind, M.Tech.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Montenegro, I.P.F.M., Mucha, A.P., Reis, I. et al. Copper effect in petroleum hydrocarbons biodegradation by microorganisms associated to Juncus maritimus: role of autochthonous bioaugmentation. Int. J. Environ. Sci. Technol. 14, 943–955 (2017). https://doi.org/10.1007/s13762-016-1215-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-016-1215-9