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Removal and Biodegradation of Phenanthrene, Fluoranthene and Pyrene by the Marine Algae Rhodomonas baltica Enriched from North Atlantic Coasts

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Abstract

This study is focused on the removal, accumulation and degradation of three environmental ubiquitous polycyclic aromatic hydrocarbons (PAHs), phenanthrene (PHE), fluoranthene (FLA) and pyrene (PYR), by the marine alga Rhodomonas baltica enriched from the English Channel. After separation, purification and culture in several phases, R. baltica was exposed to PAH concentrations that are frequently encountered in the field in several anthropized environments. The results showed that R. baltica can grow under PAH stress, efficiently remove up to 70% of these compounds from the medium by 216 h of culture and selectively bioaccumulate PAHs by their hydrophobicity. Between PHE, FLA and PYR, phenanthrene was the compound with higher degradation rates throughout incubation. The equilibrium partitioning theoretical approach showed that physico-chemical partitioning, rather than active bioconcentration, was the major factor governing the bioaccumulation, outlying a potential application in decontamination processes for this species.

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References

  • Aksu Z (2005) Application of biosorption for the removal of organic pollutants: a review. Proc Biochem 40(3):997–1026

    Article  CAS  Google Scholar 

  • Aksu Z, Kutsal T (1990) A comparative study for biosorption characteristics of heavy metal ions with C. vulgaris. Environ Technol 11(10):979–987

    Article  CAS  Google Scholar 

  • Bajt O (2014) Aliphatic and polycyclic aromatic hydrocarbons in Gulf of Trieste sediments (northern Adriatic): potential impacts of maritime traffic. Bull Environ Contam Toxicol 93:299–305

    Article  CAS  Google Scholar 

  • Berrojalbiz N, Lacorte S, Calbet A, Saiz E, Barata C, Dachs J (2009) Accumulation and cycling of polycyclic aromatic hydrocarbons in zooplankton. Environ Sci Technol 43(7):2295–2301

    Article  CAS  Google Scholar 

  • Mackay D, Boethling RS (eds) (2000) Handbook of property estimation methods for chemicals: environmental and health sciences. CRC press

  • Burgess RM, Ahrens MJ, Hickey CW, Den Besten PJ, Ten Hulscher D, Van Hattum Meador J, Douben PE (2003) An overview of the partitioning and bioavailability of PAHs in sediments and soils. In: Douben PE (ed) PAHs: an ecotoxicological perspective, ecological and environmental toxicology series. Wiley, West Sussex, p 99

    Google Scholar 

  • Cailleaud K, Forget-Leray J, Souissi S, Lardy S, Augagneur S, Budzinski H (2007) Seasonal variation of hydrophobic organic contaminant concentrations in the water-column of the seine estuary and their transfer to a planktonic species Eurytemora affinis (Calanoid, copepod). Part 2: alkylphenol-polyethoxylates. Chemosphere 70(2):281–287

    Article  CAS  Google Scholar 

  • Cailleaud K, Budzinski H, Menach KL, Souissi S, Forget-Leray J (2009) Uptake and elimination of hydrophobic organic contaminants in estuarine copepods: an experimental study. Environ Toxicol Chem 28(2):239–246

    Article  CAS  Google Scholar 

  • Chan SMN, Luan T, Wong MH, Tam NFY (2006) Removal and biodegradation of polycyclic aromatic hydrocarbons by Selenastrum capricornutum. Environ Toxicol Chem 25(7):1772–1779

    Article  CAS  Google Scholar 

  • Di Toro, DM, McGrath JA, Hansen DJ (2000) Technical basis for narcotic chemicals and polycyclic aromatic hydrocarbon criteria. I. Water and tissue. Environ Toxicol Chem 19(8):1951–1970

    Article  CAS  Google Scholar 

  • Farrington JW, Goldberg ED, Risebrough RW, Martin JH, Bowen VT (1983) U.S. “Mussel Watch” 1976–1978: an overview of the trace-metal, DDE, PCB, hydrocarbon and artificial radionuclide data. Environ Sci Technol 17:490–496

    Article  CAS  Google Scholar 

  • Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl Environ Microbiol 64(9):3352–3358

    CAS  Google Scholar 

  • Gerofke A, Kömp P, McLachlan MS (2005) Bioconcentration of persistent organic pollutants in four species of marine phytoplankton. Environ Toxicol Chem 24(11):2908–2917

    Article  CAS  Google Scholar 

  • Guillard RR, Sieracki MS (2005) Counting cells in cultures with the light microscope. In: Andersen RA (ed) Algal culturing techniques, 1st edn. Academic Press, pp 239–252

  • Gustafsson O, Gschwend PM (1997) Soot as a strong partition medium for polycyclic aromatic hydrocarbons in aquatic systems. In: Eganhouse RP (ed) Molecular markers in environmental geochemistry. American Chemical Society, Washington, pp 365–381

    Chapter  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1):1–15

    Article  CAS  Google Scholar 

  • Harms H, Bosma TNP (1997) Mass transfer limitation of microbial growth and pollutant degradation. J Ind Microbiol Biotechnol 18(2–3):97–105

    Article  CAS  Google Scholar 

  • Hong YW, Yuan DX, Lin QM, Yang TL (2008) Accumulation and biodegradation of phenanthrene and fluoranthene by the algae enriched from a mangrove aquatic ecosystem. Mar Pollut Bull 56(8):1400–1405

    Article  CAS  Google Scholar 

  • Iwasawa K, Murata A, Taguchi S (2009) Cell shrinkage of Isochrysis galbana (Prymneshiophyceae) during storage with preservatives. Plankton Benthos Res 4(3):120–121

    Article  Google Scholar 

  • Karickhoff SW (1981) Semi-empirical estimation of sorption of hydrophobic pollutants on natural sediments and soils. Chemosphere 10(8):833–846

    Article  CAS  Google Scholar 

  • Kowaleska G, Konat J (1997) The role of phytoplankton in the transport and distribution of polynuclear aromatic hydrocarbons in the southern Baltic environment. Oceanologia 39:267–277

    Google Scholar 

  • Lotufo GR (1998) Bioaccumulation of sediment-associated fluoranthene in benthic copepods: uptake, elimination and biotransformation. Aquat Toxicol 44(1):1–15

    Article  CAS  Google Scholar 

  • Lukitaningsih E, Sudarmanto A (2010) Bioaccumulation of poly-aromatic hydrocarbons in plankton, algae and fish in south sea waters in Jogjakarta. Indones J Pharm 21:18–26

    CAS  Google Scholar 

  • Mackie PR, Hardy R, Butler E, Holligan PM, Spooner MF (1978) Early samples of oil in water and some analyses of zooplankton. Mar Pollut Bull 9:296–299

    Article  Google Scholar 

  • Magnusson K, Tiselius P (2010) The importance of uptake from food for the bioaccumulation of PCB and PBDE in the marine planktonic copepod Acartia clausi. Aquat Toxicol 98(4):374–380

    Article  CAS  Google Scholar 

  • McCready S, Birch GF, Long ER (2006) Metallic and organic contaminants in sediments of Sydney Harbour, Australia and vicinity: a chemical dataset for evaluating sediment quality guidelines. Environ Int 32:455–465

    Article  Google Scholar 

  • Meador JP, Stein JE, Reichert WL, Varanasi U (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 79–165

  • Middleditch BS, Chang ES, Basile B (1979) Alkanes in plankton from the Buccaneer oilfield. Bull Environ Contam Toxicol 21:421–427

    Article  CAS  Google Scholar 

  • Narbonne JF, Aarab N, Clerandeau C, Daubeze M, Narbonne J, Champeau O, Garrigues P (2005) Scale of classification based on biochemical markers in mussels: application to pollution monitoring in Mediterranean coasts and temporal trends. Biomarkers 10:58–71

    Article  CAS  Google Scholar 

  • Othman HB, Leboulanger C, Le Floc’h E, Mabrouk HH, Hlaili AS (2012) Toxicity of benz (a) anthracene and fluoranthene to marine phytoplankton in culture: does cell size really matter?. J Hazard Mater 243:204–211

    Article  CAS  Google Scholar 

  • Sadovskaya I, Souissi A, Souissi S, Grard T, Lencel P, Greene CM, Usov AI (2014) Chemical structure and biological activity of a highly branched (1→ 3, 1→ 6)-β-d-glucan from Isochrysis galbana. Carbohydr Polym 111:139–148

    Article  CAS  Google Scholar 

  • Schantz MM (2006) Pressurized liquid extraction in environmental analysis. Anal Bioanal Chem 386(4):1043–1047

    Article  CAS  Google Scholar 

  • Serrazanetti GP, Conte LS, Carpené E, Bergami C, Fonda-Umani S (1991) Distribution of aliphatic hydrocarbons in plankton of Adriatic Sea open waters. Chemosphere 23:925–938

    Article  CAS  Google Scholar 

  • Sibley PK, Harris ML, Bestari KT, Steele TA, Robinson RD, Gensemer RW, Day KE, Solomon KR (2004) Response of zooplankton and phytoplankton communities to creosote-impregnated Douglas Fir pilings in freshwater microcosms. Arch Environ Contam Toxicol 47:56–66

    Article  CAS  Google Scholar 

  • Skjoldal HR, Dale T, Haldorsen H, Pengerud B, Thingstad TF, Tjessem K, Aberg A (1982) Oil pollution and plankton dynamics. 1. Controlled ecosystem experiments during the 1980 spring bloom in Lindaspollene, Norway. Neth J Sea Res 16:511–523

    Article  CAS  Google Scholar 

  • Soto C, Hellebust JA, Hutchinson TC, Sawa T (1975) Effect of naphthalene and aqueous crude oil extracts on the green flagellate Chlamydomonas angulosa. I. Growth. Can J Bot 53(2):109–117

    Article  CAS  Google Scholar 

  • Stange K, Swackhamer DL (1994) Factors affecting phytoplankton species: specific differences in accumulation of 40 polychlorinated biphenyls (PCBs). Environ Toxicol Chem 13(11):1849–1860

    Article  CAS  Google Scholar 

  • Stephanou EG (2005) Contribution of biomass burning to atmospheric polycyclic aromatic hydrocarbons at three European background sites. Environ Sci Technol 39:2976–2982

    Article  Google Scholar 

  • Tam NF, Chong AMY, Wong YS (2002) Removal of tributyltin (TBT) by live and dead microalgal cells. Mar Pollut Bull 45(1):362–371

    Article  CAS  Google Scholar 

  • Tanacredi JT (1977) Petroleum hydrocarbons from effluents: detection in marine environment. J Water Pollut Control Fed 49:216–226

    CAS  Google Scholar 

  • Tlili S, Ovaert J, Souissi A, Ouddane B, Souissi S (2016) Acute toxicity, uptake and accumulation kinetics of nickel in an invasive copepod species: Pseudodiaptomus marinus. Chemosphere 144:1729–1737

    Article  CAS  Google Scholar 

  • Tobin JM, Cooney JJ (1999) Action of inorganic tin and organotins on a hydrocarbon-using yeast, Candida maltosa. Arch Environ Contam Toxicol 36(1):7–12

    Article  CAS  Google Scholar 

  • Tsezos M, Bell JP (1989) Comparison of the biosorption and desorption of hazardous organic pollutants by live and dead biomass. Water Res 23(5):561–568

    Article  CAS  Google Scholar 

  • Wetzel DL, Van Vleet ES (2004) Accumulation and distribution of petroleum hydrocarbons found in mussels (Mytilus galloprovincialis) in the canals of Venice, Italy. Mar Pollut Bull 48:927–936

    Article  CAS  Google Scholar 

  • Yin F, John GF, Hayworth JS, Clement TP (2015) Long-term monitoring data to describe the fate of polycyclic aromatic hydrocarbons in deepwater horizon oil submerged off Alabama’s beaches. Sci Total Environ 508:46–56

    Article  CAS  Google Scholar 

  • Zhang Q, Yang L, Wang WX (2011) Bioaccumulation and trophic transfer of dioxins in marine copepods and fish. Environ Pollut 159(12):3390–3397

    Article  CAS  Google Scholar 

  • Zhu LZ, Wang J (2005) PAHs pollution from traffic sources in air of Hangzhou, China: trend and influencing factors. J Environ Sci (China) 17:365–370

    CAS  Google Scholar 

Download references

Acknowledgements

Our sincere gratitude to the Erasmus Mundus mobility program staff (UE). We thank the financial support obtained from the research federation FED 4129 IREPSE (Institut de Recherches Pluridisciplinaires en Sciences de l’Environnement) of Lille 1 university and Fondo para la Investigación Científica y Tecnológica (Grant No. 1302).

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Correspondence to Andrés H. Arias.

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Arias, A.H., Souissi, A., Glippa, O. et al. Removal and Biodegradation of Phenanthrene, Fluoranthene and Pyrene by the Marine Algae Rhodomonas baltica Enriched from North Atlantic Coasts. Bull Environ Contam Toxicol 98, 392–399 (2017). https://doi.org/10.1007/s00128-016-1967-4

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  • DOI: https://doi.org/10.1007/s00128-016-1967-4

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