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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Aksu Z (2005) Application of biosorption for the removal of organic pollutants: a review. Proc Biochem 40(3):997–1026
Aksu Z, Kutsal T (1990) A comparative study for biosorption characteristics of heavy metal ions with C. vulgaris. Environ Technol 11(10):979–987
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
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
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
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
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
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
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
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
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
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
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
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169(1):1–15
Harms H, Bosma TNP (1997) Mass transfer limitation of microbial growth and pollutant degradation. J Ind Microbiol Biotechnol 18(2–3):97–105
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
Iwasawa K, Murata A, Taguchi S (2009) Cell shrinkage of Isochrysis galbana (Prymneshiophyceae) during storage with preservatives. Plankton Benthos Res 4(3):120–121
Karickhoff SW (1981) Semi-empirical estimation of sorption of hydrophobic pollutants on natural sediments and soils. Chemosphere 10(8):833–846
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
Lotufo GR (1998) Bioaccumulation of sediment-associated fluoranthene in benthic copepods: uptake, elimination and biotransformation. Aquat Toxicol 44(1):1–15
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
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
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
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
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
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
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
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
Schantz MM (2006) Pressurized liquid extraction in environmental analysis. Anal Bioanal Chem 386(4):1043–1047
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
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
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
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
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
Stephanou EG (2005) Contribution of biomass burning to atmospheric polycyclic aromatic hydrocarbons at three European background sites. Environ Sci Technol 39:2976–2982
Tam NF, Chong AMY, Wong YS (2002) Removal of tributyltin (TBT) by live and dead microalgal cells. Mar Pollut Bull 45(1):362–371
Tanacredi JT (1977) Petroleum hydrocarbons from effluents: detection in marine environment. J Water Pollut Control Fed 49:216–226
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
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
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
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
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
Zhang Q, Yang L, Wang WX (2011) Bioaccumulation and trophic transfer of dioxins in marine copepods and fish. Environ Pollut 159(12):3390–3397
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
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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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