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Changes of benthic bacteria and meiofauna assemblages during bio-treatments of anthracene-contaminated sediments from Bizerta lagoon (Tunisia)

  • DECAPAGE Project: Hydrocarbon degradation in coastal sediments*
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Abstract

Sediments from Bizerta lagoon were used in an experimental microcosm setup involving three scenarios for the bioremediation of anthracene-polluted sediments, namely bioaugmentation, biostimulation, and a combination of both bioaugmentation and biostimulation. In order to investigate the effect of the biotreatments on the benthic biosphere, 16S rRNA gene-based T-RFLP bacterial community structure and the abundance and diversity of the meiofauna were determined throughout the experiment period. Addition of fresh anthracene drastically reduced the benthic bacterial and meiofaunal abundances. The treatment combining biostimulation and bioaugmentation was most efficient in eliminating anthracene, resulting in a less toxic sedimentary environment, which restored meiofaunal abundance and diversity. Furthermore, canonical correspondence analysis showed that the biostimulation treatment promoted a bacterial community favorable to the development of nematodes while the treatment combining biostimulation and bioaugmentation resulted in a bacterial community that advantaged the development of the other meiofauna taxa (copepods, oligochaetes, polychaetes, and other) restoring thus the meiofaunal structure. The results highlight the importance to take into account the bacteria/meiofauna interactions during the implementation of bioremediation treatment.

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References

  • Abbondanzi F, Bruzzi L, Campisi T, Frezzati A, Guerra R, Lacondini A (2006) Biotreatability of polycyclic aromatic hydrocarbons in brackish sediments: preliminary studies of an integrated monitoring. Int Biodeterior Biodegrad 57:214–221

    Article  CAS  Google Scholar 

  • Agarry SE, Owabor CN (2011) Anaerobic bioremediation of marine sediment artificially contaminated with anthracene and naphthalene. Environ Technol 32:1375–1381

    Article  CAS  Google Scholar 

  • Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265

    Article  CAS  Google Scholar 

  • Alkemade R, Wielemaker A, De Jong SA, Sandee AJJ (1992) Experimental evidence for the role of bioturbation by the marine nematode Diplolaimella dievengatensis in stimulating the mineralization of Spartina anglica leaves. Mar Ecol Prog Ser 90:149–155

    Article  Google Scholar 

  • Aller RC, Aller JY (1992) Meiofauna and solute transport in marine muds. Limnol Oceanogr 37:1018–1033

    Article  CAS  Google Scholar 

  • Angerer J, Mannschreck C, Gũndel J (1997) Biological monitoring and biochemical effect monitoring of exposure to polycyclic aromatic hydrocarbons. J Int Arch Occup Environ Health 70:365–377

    Article  CAS  Google Scholar 

  • Anthony A, Atwood J, August P, Byron C, Cobb S, Foster C, Fry C, Gold A, Hagos K, Heffner L, Kellogg DQ, Lellis-Dibble K, Opaluch JJ, Oviatt C, Pfeiffer-Herbert A, Rohr N, Smith L, Smythe T, Swift J, Vinhateiro N (2009) Coastal lagoons and climate change: ecological and social ramifications in U.S. Atlantic and Gulf Coast ecosystems. Ecol Soc 14:8

    Google Scholar 

  • Atlas R, Bragg J (2009) Bioremediation of marine oil spills: when and when not—the Exxon Valdez experience. Microb Biotechnol 2:213–221

    Article  CAS  Google Scholar 

  • Balba MT, Al-Awadhi N, Al-Daher R (1998) Bioremediation of oil-contaminated soil: microbiological methods for feasibility assessment and field evaluation. J Microbiol Meth 32:155–164

    Article  CAS  Google Scholar 

  • Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736

    Article  CAS  Google Scholar 

  • Ben Said O, Goni-Urriza MS, El Bour M, Dellali M, Aissa P, Duran R (2008) Characterization of aerobic polycyclic aromatic hydrocarbon-degrading bacteria from Bizerte lagoon sediments, Tunisia. J Appl Microbiol 104:987–997

    Article  CAS  Google Scholar 

  • Ben Said O, Goni-Urriza M, El Bour M, Aissa P, Duran R (2010) Bacterial community structure of sediments of the Bizerte Lagoon (Tunisia), a southern Mediterranean coastal anthropized lagoon. Microb Ecol 59:445–456

    Article  Google Scholar 

  • Boonyatumanond R, Wattayakorn G, Togo A, Takada H (2006) Distribution and origins of polycyclic aromatic hydrocarbons (PAHs) in riverine, estuarine, and marine sediments in Thailand. Mar Pollut Bull 52:942–956

    Article  CAS  Google Scholar 

  • Bossert ID, Campeau G (1995) Cleanup of petroleum hydrocarbon contamination in soil. In: Young LY, Cerniglia CE (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss, New York, pp 77–126

    Google Scholar 

  • Brion D, Pelletier E (2005) Modelling PAHs adsorption and sequestration in freshwater and marine sediments. Chemosphere 61:867–876

    Article  CAS  Google Scholar 

  • Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85:207–228

    Article  CAS  Google Scholar 

  • Carman KR, Fleeger JW, Means JC, Pomarico SM, McMillin DJ (1995) Experimental investigation of the effects of polynuclear aromatic hydrocarbons on an estuarine sediment food web. Mar Environ Res 40:289–318

    Article  CAS  Google Scholar 

  • Castro-Silva C, Ruíz-Valdiviezo VM, Valenzuela-Encinas C, Alcántara-Hernández RJ, Navarro-Noya YE, Vázquez-Núñez E, Luna-Guido M, Marsch R, Dendooven L (2013) The bacterial community structure in an alkaline saline soil spiked with anthracene. Electron J Biotechnol. doi:10.2225/vol16-issue5-fulltext-14

    Google Scholar 

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    Article  CAS  Google Scholar 

  • Cheung KC, Zhang JY, Deng HH, Ou YK, Leung HM, Wu SC, Wong MH (2008) Interaction of higher plant (jute), electrofused bacteria and mycorrhiza on anthracene biodegradation. Bioresour Technol 99:2148–2155

    Article  CAS  Google Scholar 

  • Cornelissen G, Rigterink H, Ferdinandy M, van Noort PCM (1998) Rapidly desorbing fractions of PAHs in contaminated sediments as a predictor of the extent of bioremediation. Environ Sci Technol 32:966–970

    Article  CAS  Google Scholar 

  • Cravo-Laureau C, Duran R (2014) Marine coastal sediments microbial hydrocarbon degradation processes: contribution of experimental ecology in the omics’era. Front Microbiol 5:39

    Google Scholar 

  • De Mesel I, Derycke S, Swings J, Vincx M, Moens T (2003) Influence of bacterivorous nematodes on the decomposition of cordgrass. J Exp Mar Biol Ecol 296:227–242

    Article  Google Scholar 

  • De Mesel I, Derycke S, Moens T, Van der Gucht K, Vincx M, Swings J (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6:733–744

    Article  Google Scholar 

  • Dejonghe W, Boon N, Seghers D, Top EM, Verstraete W (2001) Bioaugmentation of soils by increasing microbial richness: missing links. Environ Microbiol 3:649–657

    Article  CAS  Google Scholar 

  • Derouiche A, Sanda YG, Driss MR (2004) Polychlorinated biphenyls in sediments from Bizerte Lagoon, Tunisia. Bull Environ Contam Toxicol 73:810–817

    Article  CAS  Google Scholar 

  • Duhamel S, Jacquet S (2006) Flow cytometric analysis of bacteria- and virus-like particles in lake sediments. J Microbiol Methods 64:316–332

    Article  CAS  Google Scholar 

  • Duran R, Ranchou-Peyruse M, Menuet V, Monperrus M, Bareille G, Goñi MS, Salvado JC, Amouroux D, Guyoneaud R, Donard OFX, Caumette P (2008) Mercury methylation by a microbial community from sediments of the Adour estuary (Bay of Biscay, France). Environ Pollut 156:951–958

    Article  CAS  Google Scholar 

  • Erickson RJ, Ankley GT, DeFoe DL, Kosian PA, Makynen EA (1999) Additive toxicity of binary mixtures of phototoxic polycyclic aromatic hydrocarbons to the oligochaete Lumbriculus variegatus. Toxicol Appl Pharmacol 154:97–105

    Article  CAS  Google Scholar 

  • Flores GP, Badillo CM, Cortazar MH, Hipolito CN, Perez RS, Sanchez IG (2010) Toxic effects of linear alkylbenzene sulfonate, anthracene and their mixture on growth of a microbial consortium isolated from polluted sediment. Rev Int Contam Ambient 26:39–46

    Google Scholar 

  • Forsyth JV, Tsao YM, Bleam RD (1995) Bioremediation: when is augmentation needed. In: Hinchee RE, Fredrickson J, Alleman BC (eds) Bioaugmentation for site remediation. Battelle, Columbus, pp 1–14

    Google Scholar 

  • Gandolfi I, Sicolo M, Franzetti A, Fontanarosa E, Santagostino A, Bestetti G (2010) Influence of compost amendment on microbial community and ecotoxicity of hydrocarbon-contaminated soils. Bioresour Technol 101:568–575

    Article  CAS  Google Scholar 

  • Gomes V, Passos M, Leme NMP, Santos TCA, Campos DYF, Hasue FM, Phan V (2009) Photo-induced toxicity of anthracene in the Antarctic shallow water amphipod, Gondogeneia antarctica. Polar Biol 32:1009–1021

  • Goni-Urriza MS, Duran R (2010) Impact of pollution on microbial mats. Microbes and communities utilizing hydrocarbons, oils and lipids. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer-Verlag, Berlin Heidelberg, p 2339–2348

  • Goni-Urriza M, Cravo-Laureau C, Duran R (2013) Microbial bioremediation of aquatic environments. In: Férard JF, Blaise C (eds) Encyclopedia of aquatic ecotoxicology. Springer Science+Business Media, Dordrecht, p 709–720

  • Guo CL, Zhou HW, Wong YS, Tam NFY (2005) Isolation of PAH degrading bacteria from mangrove sediments and their biodegradation potential. Mar Pollut Bull 51:1054–1061

    Article  CAS  Google Scholar 

  • Guyoneaud R, Mouné S, Eatock C, Bothorel V, Hirschler-Réa A, Willison J, Duran R, Liesack W, Herbert R, Matheron R, Caumette P (2002) Characterization of three spiral-shaped purple nonsulfur bacteria isolated from coastal lagoon sediments, saline sulfur springs, and microbial mats: emended description of the genus Roseospira and description of Roseospira marina sp. nov., Roseospira navarrensis sp. nov., and Roseospira thiosulfatophila sp. nov. Arch Microbiol 178:315–324

  • Gyedu-Ababio TK, Baird D (2006) Response of meiofauna and nematode communities to increased levels of contaminants in a laboratory microcosm experiment. Ecotoxicol Environ Saf 63:443–450

    Article  CAS  Google Scholar 

  • Head IM, Swannell RP (1999) Bioremediation of petroleum hydrocarbon contaminants in marine habitats. Curr Opin Biotechnol 10:234–239

    Article  CAS  Google Scholar 

  • Hughes JB, Beckles DM, Chandra SD, Ward CH (1997) Utilization of bioremediation processes for the treatment of PAH-contaminated sediments. J Microbiol Biotechnol 18:152–160

    Article  CAS  Google Scholar 

  • Jacques RJS, Okeke BC, Bento FM, Teixeira AS, Peralba MCR, Camargo FAO (2008) Microbial consortium bioaugmentation of a polycyclic aromatic hydrocarbons contaminated soil. Bioresour Technol 99:2637–2643

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88

    Article  CAS  Google Scholar 

  • Krivobok S, Miriouchkine E, Seigle-Murandi F, Benoit-Guyod JL (1998) Biodegradation of anthracene by soil fungi. Chemosphere 37:523–530

    Article  CAS  Google Scholar 

  • Launen LA, Buggs VH, Eastep ME, Enriquez RC, Leonard JW, Blaylock MJ, Huang J-W, Häggblom MM (2002) Bioremediation of polyaromatic hydrocarbon-contaminated sediments in aerated bioslurry reactors. Biorem J 6:125–141

    Article  CAS  Google Scholar 

  • Lee K, Tremblay GH, Levy EM (1993) Bioremediation: application of slow-release fertilizers on low-energy shorelines. Proceedings of the 1993 Oil Spill Conference. American Petroleum Institute, Washington, DC, pp 449–454

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology 20. Elsevier, Amsterdam, pp 1–853

    Google Scholar 

  • Lin TC, Pan PT, Young CC, Chang JS, Chang TC, Cheng SS (2011) Evaluation of the optimal strategy for ex situ bioremediation of diesel oil-contaminated soil. Environ Sci Pollut Res 18:1487–1496

    Article  CAS  Google Scholar 

  • Losi V, Ferrero TJ, Moreno M, Gaozza L, Rovere A, Firpo M, Marques JC, Albertelli G (2013) The use of nematodes in assessing ecological conditions in shallow waters surrounding a Mediterranean harbour facility. Estuar Coast Shelf Sci 130:209–221

    Article  Google Scholar 

  • Louati H, Ben Said O, Got P, Soltani A, Mahmoudi E, Cravo-Laureau C, Duran R, Aissa P, Pringault O (2013a) Microbial community responses to bioremediation treatments for the mitigation of low-dose anthracene in marine coastal sediments of Bizerte lagoon (Tunisia). Environ Sci Pollut Res 20:300–310

    Article  CAS  Google Scholar 

  • Louati H, Ben Said O, Soltani A, Got P, Mahmoudi E, Cravo-Laureau C, Duran R, Aissa P, Pringault O (2013b) Roles of biological interactions and pollutant contamination in shaping microbial benthic community structure. Chemosphere 93:2535–2546

    Article  CAS  Google Scholar 

  • Louati H, Ben Said O, Soltani A, Cravo-Laureau C, Preud'Homme H, Duran R, Aissa P, Mahmoudi E, Pringault O (2014a) Impact of low dose anthracene contamination on the diversity of free-living marine benthic nematodes. Ecotoxicology 23:201–211

    Article  CAS  Google Scholar 

  • Louati H, Ben Said O, Soltani A, Got P, Cravo-Laureau C, Duran R, Aissa P, Pringault O, Mahmoudi E (2014b) Biostimulation as an attractive technique to reduce phenanthrene toxicity for meiofauna and bacteria in lagoon sediment. Environ Sci Pollut Res 21:3670–3679

    Article  CAS  Google Scholar 

  • MacNaughton SJ, Stephen JR, Venosa AD, Davis GA, Chang YJ, White DC (1999) Microbial population changes during bioremediation of an experimental oil spill. Appl Environ Microbiol 65:3566–3574

    CAS  Google Scholar 

  • MacRae JD, Hall KJ (1998) Biodegradation of polycyclic aromatic hydrocarbons (PAH) in marine sediment under denitrifying conditions. Water Sci Technol 38:177–185

    Article  CAS  Google Scholar 

  • Mahmoudi E, Essid N, Beyrem H, Hedfi A, Boufahja F, Vitiello P, Aissa P (2005) Effects of hydrocarbon contamination on a free living marine nematode community: results from microcosm experiments. Mar Pollut Bull 50:1197–1204

    Article  CAS  Google Scholar 

  • Mahmoudi E, Essid N, Beyrem H, Hedfi A, Boufahja F, Vitiello P, Aissa P (2007) Individual and combined effects of lead and zinc on a free-living marine nematode community: results from microcosm experiments. J Exp Mar Biol Ecol 343:217–226

    Article  CAS  Google Scholar 

  • Marie D, Partensky F, Jacquet S, Vaulot D (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63:186–193

    CAS  Google Scholar 

  • Meador JP, Stein JE, Reichert WL, Varanasi U (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. Rev Environ Contam Toxicol 143:79–165

    CAS  Google Scholar 

  • Mekenyan OG, Ankley GT, Veith GD, Call DJ (1994) Qsars for photoinduced toxicity. 1. Acute lethality of polycyclic aromatic hydrocarbons to Daphnia magna. Chemosphere 28:567–582

    Article  CAS  Google Scholar 

  • Meysman FJR, Galaktionov OS, Madani S, Middelburg JJ (2005) Modelling biological interactions in aquatic sediments as coupled reactive transport. In: Kristensen E, Haese RR, Kostka JE (eds) Interactions between macro- and microorganisms in marine sediments, coastal and estuarine studies 60, American Geophysical Union, pp 359–388

  • Mills MA, Bonner JS, McDonald TJ, Page CA, Autenrieth RL (2003) Intrinsic bioremediation of a petroleum impacted wetland. Mar Pollut Bull 46:887–899

    Article  CAS  Google Scholar 

  • Miyasaka T, Asami H, Watanabe K (2006) Impacts of bioremediation schemes on bacterial population in naphthalene-contaminated marine sediments. Biodegradation 17:227–235

    Article  CAS  Google Scholar 

  • Moens T, dos Santos GAP, Thompson F, Swings J, Fonseca-Genevois V, Vincx M, De Mesel I (2005) Do nematode mucus secretions affect bacterial growth? Aquat Microb Ecol 40:77–83

    Article  Google Scholar 

  • Morgan P, Watkinson RJ (1989) Hydrocarbon degradation in soils and methods for soil biotreatment. Crit Rev Biotechnol 8:305–333

    Article  CAS  Google Scholar 

  • Muncnerova D, Augustin J (1994) Fungal metabolism and detoxification of polycyclic aromatic hydrocarbons: a review. Bioresour Technol 48:97–106

    Article  Google Scholar 

  • Nascimento FJA, Näslund J, Elmgren R (2012) Meiofauna enhances organic matter mineralization in soft sediment ecosystems. Limnol Oceanogr 57:338–346

    CAS  Google Scholar 

  • Naslund J, Nascimento FJA, Gunnarsson JS (2010) Meiofauna reduces bacterial mineralization of naphthalene in marine sediment. ISME J 4:1421–1430

    Article  Google Scholar 

  • Nkansah MA, Christy AA, Barth T (2011) The use of anthracene as a model compound in a comparative study of hydrous pyrolysis methods for industrial waste remediation. Chemosphere 84:403–408

    Article  CAS  Google Scholar 

  • Onwurah INE, Ogugua VN, Onyike NB, Ochonogor AE, Otitoju OF (2007) Crude oil spills in the environment, effects and some innovative clean-up biotechnologies. Int J Environ Res 1:307–320

    CAS  Google Scholar 

  • Paisse S, Goni-Urriza M, Coulon F, Duran R (2010) How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Microb Ecol 60:394–405

    Article  Google Scholar 

  • Pringault O, Duran R, Jacquet S, Torreton JP (2008) Temporal variations of microbial activity and diversity in marine tropical sediments (New Caledonia lagoon). Microb Ecol 55:247–258

    Article  CAS  Google Scholar 

  • Riser-Roberts E (1998) Remediation of petroleum contaminated soils: biological, physical, and chemical processes. Lewis, Boca Raton, pp 5–313

    Book  Google Scholar 

  • Roling WFM, Milner MG, Jones DM, Fratepietro F, Swannell RPJ, Daniel F, Head IM (2004) Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl Environ Microbiol 70:2603–2613

    Article  Google Scholar 

  • Schratzberger M, Daniel F, Wall CM, Kilbride R, Macnaughton SJ, Boyd SE, Rees HL, Lee K, Swannell RPJ (2003) Response of estuarine meio- and macrofauna to in situ bioremediation of oil-contaminated sediment. Mar Pollut Bull 46:430–443

    Article  CAS  Google Scholar 

  • Schumacher BA (2002) Methods for the determination of total organic carbon (TOC) in soils and sediments. United States Environmental Protection Agency, Environmental Sciences Division National Exposure Research Laboratory, Las Vegas

    Google Scholar 

  • Sese BT, Grant A, Reid BJ (2009) Toxicity of polycyclic aromatic hydrocarbons to the nematode Caenorhabditis elegans. J Toxicol Environ Health A 72:1168–1180

    Article  CAS  Google Scholar 

  • Simarro R, González N, Bautista LF, Molina MC (2013) Assessment of the efficiency of in situ bioremediation techniques in a creosote polluted soil: change in bacterial community. J Hazard Mater 262:158–167

    Article  CAS  Google Scholar 

  • Stauffert M, Cravo-Laureau C, Jézéquel R, Barantal S, Cuny P, Gilbert F, Cagnon C, Militon C, Amouroux D, Mahdaoui F, Bouyssiere B, Stora G, Merlin F-X, Duran R (2013) Impact of oil on bacterial community structure in bioturbated sediments. PLoS ONE 8:e65347

    Article  CAS  Google Scholar 

  • Stauffert M, Duran R, Gassie C, Cravo-Laureau C (2014a) Response of archaeal communities to oil spill in bioturbated mudflat sediments. Microb Ecol 67:108–119

    Article  CAS  Google Scholar 

  • Stauffert M, Cravo-Laureau C, Duran R (2014b) Structure of hydrocarbonoclastic nitrate-reducing bacterial communities in bioturbated coastal marine sediments. FEMS Microbiol Ecol 89(3):580–593

    Article  CAS  Google Scholar 

  • Swannell RP, Lee K, McDonagh M (1996) Field evaluations of marine oil spill bioremediation. Microbiol Rev 60:342–365

    CAS  Google Scholar 

  • Timmermann K, Banta GT, Johnsen AR, Andersen O (2008) Effects of the polychaetes Arenicola marina and Nereis diversicolor on microbial pyrene mineralization. Aquat Microb Ecol 50:197–207

    Article  Google Scholar 

  • Trabelsi S, Driss MR (2005) Polycyclic aromatic hydrocarbons in superficial costal sediments from Bizerte lagoon, Tunisia. Mar Pollut Bull 50:344–359

    Article  CAS  Google Scholar 

  • Traczewska TM (2000) Changes of toxicological properties of biodegradation products of anthracene and phenanthrene. Water Sci Technol 41:31–38

    CAS  Google Scholar 

  • Van Oevelen D, Middelburg JJ, Soetaert K, Moodley L (2006) The fate of bacterial carbon in an intertidal sediment: modeling an in situ isotope tracer experiment. Limnol Oceanogr 51:1302–1314

    Article  Google Scholar 

  • Vinas M, Sabate J, Espuny MJ, Solanas AM (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Appl Environ Microbiol 71:7008–7018

    Article  CAS  Google Scholar 

  • Vogel TM (1996) Bioaugmentation as a soil bioremediation approach. Curr Opin Biotechnol 7:311–316

    Article  CAS  Google Scholar 

  • Yoshida M, Hamdi H, Abdulnasser I, Jedidi N (2002) Contamination of potentially toxic elements (PTEs) in Bizerte lagoon bottom sediments, surface sediment and sediment repository. In: Ghrabi A, Yoshida M (eds) Study on environmental pollution of Bizerte lagoon. INRST-JICA, Tunis, p 139

    Google Scholar 

  • Yu SH, Ke L, Wong YS, Tam NFY (2005a) Degradation of polycyclic aromatic hydrocarbons by a bacterial consortium enriched from mangrove sediments. Environ Int 31:149–154

    Article  CAS  Google Scholar 

  • Yu KSH, Wong AHY, Yau KWY, Wong YS, Tam NFY (2005b) Natural attenuation, biostimulation and bioaugmentation on biodegradation of polycyclic aromatic hydrocarbons (PAHs) in mangrove sediments. Mar Pollut Bull 51:1071–1077

    Article  CAS  Google Scholar 

  • Zhang SY, Wang QF, Xie SG (2011) Microbial community changes in contaminated soils in response to phenanthrene amendment. Int J Environ Sci Technol 8:321–330

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by a funding of the CMCU program (PHC-UTIQUE, n° 09G 0189), Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Développement (IRD), and the Faculté des Sciences de Bizerte (FSB). We acknowledge the Regional Platform for Environmental Microbiology PREMICE supported by the Aquitaine Regional Government Council (France) and the urban community of Pau-Pyrénées (France). Thanks also to anonymous reviewers for their helpful comments and suggestions.

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Ben Said, O., Louati, H., Soltani, A. et al. Changes of benthic bacteria and meiofauna assemblages during bio-treatments of anthracene-contaminated sediments from Bizerta lagoon (Tunisia). Environ Sci Pollut Res 22, 15319–15331 (2015). https://doi.org/10.1007/s11356-015-4105-7

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