Oil-polluted Seawater Research Articles

Compositional change of bacterial communities in oil-polluted seawater amid varying degrees of nanoplankton bacterivory

Petroleum hydrocarbons are being released into the marine environment continuously. They will undergo weathering and may eventually be biodegraded by bacteria and other microbes. While nanoplankton (2–20 μm) are the major consumers of marine bacteria, their effect on the process of biodegradation of oil hydrocarbons is still debated. A 14-day microcosm experiment was conducted to investigate the effects of crude oil hydrocarbons on nanoplankton bacterivory and bacterial community in coastal waters. The coefficients of population growth (0.56–1.80 d−1 for all treatments considered) and grazing mortality (0.38–1.65 d−1 for all treatment considered) of bacteria estimated with the dilution method did not differ among the treatments of control (Ctrl), low dose chemically dispersed oil (LDOil, 2 μL L−1 of crude oil), and high dose chemically dispersed oil (HDOil, 8 μL L−1 of crude oil). Bacterial abundance ranged between 0.21–0.86 × 106 cells mL−1 on average for all treatments. The lack of drastic increases in the cell density of bacterial cells in the oil-loaded treatments was observed throughout the experiment period. Sequencing analysis of the 16S rRNA gene revealed the progressive changes in the community compositions of bacteria in all treatments. The relatively high abundance of oil-degrading bacteria, including Cycloclasticus and Alcanivorax on Days 3–14 of the experiment reflected the presence of biodegradation of oil in the LDOil and HDOil treatments. Throughout the 14 days, the community composition of bacteria in the LDOil and HDOil treatments became more similar and they both differed from that in the Ctrl treatment. This study concluded that, in oil-polluted seawater, the changes in the bacterial community composition were mainly resulting from the addition of chemically dispersed crude oil.

Bio-sorptive remediation of crude oil polluted sea water using plantain (Musa parasidiaca) leaves as bio-based sorbent: Parametric optimization by Taguchi technique, equilibrium isotherm and kinetic modelling studies

This study investigated the potential of employing plantain leaves as a natural bio-based sorbent for crude oil spill polluted seawater remediation. Type L9(34) Taguchi orthogonal array technique was used to evaluate the effect of four independent bio-sorption factors at three different levels (crude oil initial concentration (X1 7.8, 11.5 and 15.6 g/L), seawater-crude oil temperature (X2 25, 35 and 45 °C), bio-sorbent dosage (X3 1, 2 and 3 g) and bio-sorbent particle size (X4 1.18, 2.36 and 4.72 mm) on two response indices (bio-sorption efficiency (%) and bio-sorption capacity (g/g)). Taguchi optimization technique, numerical-desirability index function optimization technique and a proposed optimization method were utilized to determine the optimum bio-sorption factors needed for the optimum bio-sorption efficiency and bio-sorption capacity. The results demonstrated that the crude oil bio-sorption efficiency of the plantain leaves was significantly influenced by X1, X3 and X4 and the bio-sorption capacity was mainly influenced by X1 and X3. The optimum bio-sorption efficiency and the optimum bio-sorption capacity were 99.05 % and 12.82 g/g, respectively, obtained at optimum combination of factors and levels of X11 (7.8 g/L), X33 (3 g) and X41 (1.18 mm) for bio-sorption efficiency and X13 (15.6 g/L) X31 (1 g) for bio-sorption capacity. The Freundlich and Dubinin-Rudeshkevich isotherm models best explain the equilibrium bio-sorption data, while the pseudo-second order kinetic model best describes the bio-sorption kinetics. The bio-sorptive remediation mechanism followed dual mechanism of physical and chemical bio-sorption and the mass transfer controlled by film diffusion. The maximum bio-sorption capacity (Kf) was 14.0 gg-1.

Zinc detection in oil-polluted marine environment by stripping voltammetry with mercury-free nanoporous gold electrode

Detection of Zn(II) in oil-polluted seawater via square-wave anodic stripping voltammetry (SW-ASV) utilizing thin gold electrodes sputtered onto nanoporous poly(acrylic acid)-grafted-poly(vinylidene difluoride) (PAA-g-PVDF) membrane is herein reported. Prior to SW-ASV, PAA grafted nanopores demonstrated to efficiently trap Zn(II) ions at open circuit. This passive adsorption followed a Langmuir law. An affinity constant of 1.41 L upmu mol^{-1} and a maximum Zn(II) adsorbed mass q_{max} of 1.21 upmu mol g^{-1} were found. Applied SW-ASV protocol implied an accumulation step (− 1.2 V for 120 s) followed by a stripping step (− 1.2 to 1 V; 25 Hz; step: 4 mV; amplitude: 25 mV; acetate buffer (pH 5.5)). It revealed a Zn redox potential at − 0.8 V (Ag/AgCl pseudo-reference). Multiple measurements in synthetic waters close to the composition of production waters exhibited a decreasing precision with the number of readings R (1.65% (R = 2) and 6.56% (R = 3)). These membrane-electrodes should be used as disposable. The intra-batch mean precision was 14% (n = 3) while inter-batches precision was 20% (n = 15). Linear and linear-log calibrations allow exploitation of Zn(II) concentrations ranging from 10 to 500 upmu g L^{-1} and 100 to 1000 upmu g L^{-1} respectively. The LOD was 4.2 upmu g L^{-1} (3S/N). Thanks to obtained calibration, a detected Zn(II) content of 1 ppm in a raw production water from North Sea oil platform was determined.

Oil degradation ability difference and microbial community successions by Ochrobactrum and Shewanella in different oil-polluted seawater

Bioaugmentation is a green technology for oil pollution remediation, and its potential to oil-polluted seawater with different deep-sea microorganisms has not been investigated. The present study aimed to comprehensively analyze the oil degradation ability difference and the microbial community successions to oil-polluted seawater with different deep-sea microorganisms by bioaugmentation through the construction of original overlying seawater, natural restored oil-polluted overlying seawater, and bioaugmented oil-polluted overlying seawater from four different sites. Results showed that bioaugmentation was valid for the treatment of oil-polluted seawater with different deep-sea microorganisms, and the highest oil degradation efficiency was 61.15% after 50 days, which was 50% higher than that of natural restoration. In addition, bioaugmentation of oil-polluted seawater played a driving role in increasing the relative abundance of indigenous bacterial genera, such as Cycloclasticus, Alcanivorax, Ulvibacter, and Erythrobacter and they all contributed to crude oil degradation. Furthermore, the microbial changes influenced by environmental factors can lead to differences in oil degradation rates, especially for Cycloclasticus, which is positively correlated with longitude. This work can improve the understanding of bioaugmentation remediation strategy development in deep-sea environment.

Management Strategies to Protect Coastal Areas from Oil-Polluted Seawater (A Case Study of Coastal Areas in Bekasi Regency)

Following an oil spill in the western Java Sea, in July 2019, the issue of oil pollution has received heightened interest. More and more people in Indonesia are increasingly aware that environmental damage will be a severe threat to the sustainability of ecosystems and environmental services. Given that oil pollution does endanger not only the aquatic ecosystem but also the surrounding terrestrial ecosystem, it is essential to encourage the involvement of stakeholders to contribute to efforts to prevent and minimize the impact of oil pollution in coastal areas that may arise in the future. Thus, since oil pollution is extremely harmful not only to aquatic ecosystems but also terrestrial ecosystems, coastal management strategies are urgently required to minimize the impact of oil pollution in the future. The overall aim of this research is to provide recommendations for policy formulations that may be adopted by the relevant local government to protect coastal areas from seawater contaminated with oil. This research uses both qualitative and quantitative approaches, including Statistical analysis, Strength-Weakness-Opportunity-Threat (SWOT) analysis and Analytical Hierarchy Process (AHP). The type of data collected will be primary data and secondary data which are sourced from experts and agencies engaged in the management of the coastal and marine environments.

Effectiveness of a bio-catalytic agent used in the bioremediation of crude oil-polluted seawater

Oil spillage contamination has been one of the most common and challenging problems in marine ecosystems over the years due to frequent petroleum exploitation, washing, and transportation activities. The use of nature-derived surfactants has become an attractive approach to restore the sites affected by oil spillage. Several studies have demonstrated that nutrient addition is an efficient strategy to enhance oil biodegradation since microorganisms can use petroleum hydrocarbons as their carbon and energy source, thus favoring and increasing the hydrocarbons degradation rate. This study aimed to assess the effectiveness of a commercial bio-catalytic agent used in the biological remediation of crude oil-contaminated sites through the qualitative analysis of its properties. The tests applied to this bio-catalyst showed excellent results. For instance, the emulsification (E24) and critical micellar concentration (CMC) assays displayed average values of 74.47% and 40 mg L−1, respectively. A significant reduction of Chemical Oxygen Demand (COD), turbidity, and Total Petroleum Hydrocarbon Content (TPHC) were observed in all the samples with bio-catalytic agent solution and aeration system. The best water quality was achieved by the sample with the highest concentration (10000 ppm) of bio-catalytic agent solution. It displayed a Total Petroleum Hydrocarbon removal efficiency (RTPH) of 81.537% after 30 days of the remediation time.

Metal-phenolic network coated cellulose foams for solar-driven clean water production

Solar-driven water steam generation is a promising strategy for seawater desalination and wastewater purification. However, oil contaminants commonly exist in real water resources, which drives us to design and fabricate photothermal materials with high efficient water steam generation and outstanding anti-oil-fouling ability. Herein, we developed a metal-phenolic network-coated cellulose foam (Fe3+/TA@CF), which exhibits not only superb hydrophilicity and underwater lipophobicity, but also achieves high water evaporation rate of ∼1.3 kg m−2 h-1 even in oil-polluted seawater under one sun illumination. In addition, Fe3+/TA@CF is demonstrated to be both anti-oil-fouling and anti-salt-fouling, which benefits to long-term evaporation in practical utilizations. Metal ions and oil contaminants in the condensed water vapor are almost eliminated after purification. We believe that this low-cost, biodegradable Fe3+/TA@CF paves a way for rationally designing and fabricating high-performance evaporator for oil contaminated water purification.

Removal of uranium by immobilized biomass of a tropical marine yeast Yarrowia lipolytica

A marine yeast, Yarrowia lipolytica isolated from an oil polluted sea water and shown earlier to sequester dissolved uranium (U) at pH 7.5, was utilized in the present study for developing an immobilized-cell process for U removal from aqueous solutions under batch and continuous flow through systems. In batch system, optimum biosorption conditions for U removal were assessed by investigating the effects of biomass dose, initial U concentration, contact time and pH of solution using Y. lipolytica cells immobilized in calcium alginate beads. Appreciable uranium-binding capabilities over a wide pH range (3–9) were observed with the alginate beads bearing yeast cells. Out of Langmuir and Freundlich models employed for describing the sorption equilibrium data under batch mode, uranyl adsorption followed Langmuir approach with satisfactory correlation coefficient higher than 0.9. Uranyl adsorption kinetics by Y. lipolytica entrapped in alginate beads was best described by the pseudo-second-order model. While the environmental scanning electron microscopy established the immobilization and the uniform distribution of Y. lipolytica cells in the alginate beads, the Energy Dispersive X-ray spectroscopy analysis confirmed the deposition of U in the beads following their exposure to uranyl solution. Fixed bed flow-through column comprising of Y. lipolytica biomass immobilized in polyacrylamide matrix displayed high efficacy for continuous removal of uranium at pH 7.5 up to five adsorption-desorption cycles. Adsorbed U by immobilized cells could be significantly desorbed using 0.1 N HCl. Overall, our results present the superior efficiency of immobilized Y. lipolytica biomass for U removal using batch and regenerative approaches.

Microbial bioremediation of oil contaminated seawater: A survey of patent deposits and the characterization of the top genera applied

Petroleum has been the world's major source of energy since the middle of the twentieth century, leading to positive changes but also social, political, and environmental problems worldwide. Oil contamination affects all ecosystems, and the remediation of polluted sites using environmentally friendly strategies is crucial. Here, we report an analysis of the patent documents of potential petroleum bioremediation techniques that use microbes to clean seawater. The patent search was performed using Orbit Intelligence®, SciFinder® and the Derwent World Patents Index®. A group of 500 patent documents were validated according to the search objective and carefully studied. Increases in patent deposits coincide with periods following widely reported oil spills, suggesting a relationship between media disclosure and stimulation of innovation activities. China leads the list of countries with patent applications in bioremediation with 152 deposits, followed by Russia with 133 and the US with 48. These three countries have completely different temporal deposit profiles, influenced by their historical, political, and economic scenarios. A total of 368 patents described degradation of the oil compounds exclusively by bacteria, 24 by fungi and yeasts, 1 by Archaea, 1 using a microalgal strain, and 32 by mixed consortia. The leading microbial genera found in the patents are Pseudomonas (114 patents), Bacillus (75), and Rhodococcus (60). In the top-10 list of microbial strains mostly cited/claimed, no genera are obligate hydrocarbonoclastic bacteria. This fact, together with the broad pattern found in the main International Patent Classification (IPC) codes, suggest that most of the documents are general bioremediation approaches and not focused on oil-polluted seawater. This work highlights the importance of stimulating the development of innovative environmentally friendly strategies focused on the degradation of oil hydrocarbons in marine ecosystems.

Dendritic copolymer electrode for second harmonic alternating current voltammetric signalling of pyrene in oil-polluted wastewater

A sensitive dendritic star copolymer-based sensor for pyrene (PY), was developed by in situ electrosynthesis of generation 3 poly(propylene thiophenoimine)-co-poly(3-hexylthiophene) (G3PPT-co-P3HT) on a gold disk electrode (Au). The electrochemical reactivity and the signal transduction properties of the Au|G3PPT-co-P3HT co-polymer electrode were studied by second harmonic alternating current voltammetry (SHACV) and alternating current voltammetry (ACV), respectively. SHACV analysis confirmed the occurrence of Faradaic electrode process (with a standard rate constant, k0 value of 3.36 cm s−1), possibly originating from the surface-confined thiophene groups of the co-polymer electrode. The ACV responses of the Au|G3PPT-co-P3HT electrode to pyrene gave a linear range (LR) of 2.73–26.86 nM and a limit of detection (LOD) of 1.34 nM PY. The low LOD value suggests that the PY sensor has promise for monitoring compliance to the World Health Organization (WHO) approved limit for polyaromatic hydrocarbons (PAHs) in wastewater, which is 3.93 nM. The sensor was used to determine PY levels in oil-polluted wastewater samples, which were found to contain 4.93–23.49 nM PY, depending on how far into the sea the samples were collected. The high recovery rate obtained for the oil-polluted seawater samples, indicate that ACV signalling protocol makes the Au|G3PPT-co-P3HT electrode very suitable for application in samples that have complex matrices.

Isolation, screening, and characterization of surface-active agent-producing, oil-degrading marine bacteria of Mumbai Harbor

Diverse marine bacterial species predominantly found in oil-polluted seawater produce diverse surface-active agents. Surface-active agents produced by bacteria are classified into two groups based on their molecular weights, namely biosurfactants and bioemulsifiers. In this study, surface-active agent-producing, oil-degrading marine bacteria were isolated using a modified Bushnell–Haas medium with high-speed diesel as a carbon source from three oil-polluted sites of Mumbai Harbor. Surface-active agent-producing bacterial strains were screened using nine widely used methods. The nineteen bacterial strains showed positive results for more than four surface-active agent screening methods; further, these strains were characterized using biochemical and nucleic acid sequencing methods. Based on the results, the organisms belonged to the genera Acinetobacter, Alcanivorax, Bacillus, Comamonas, Chryseomicrobium, Halomonas, Marinobacter, Nesterenkonia, Pseudomonas, and Serratia. The present study confirmed the prevalence of surface-active agent-producing bacteria in the oil-polluted waters of Mumbai Harbor.

Draft genome sequence of the marine Rhodobacteraceae strain O3.65, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill

Draft genome sequence of the marine Rhodobacteraceae strain O3.65, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill

Quick stimulation of Alcanivorax sp. by bioemulsificant EPS₂₀₀₃ on microcosm oil spill simulation.

Oil spill microcosms experiments were carried out to evaluate the effect of bioemulsificant exopolysaccharide (EPS₂₀₀₃) on quick stimulation of hydrocarbonoclastic bacteria. Early hours of oil spill, were stimulated using an experimental seawater microcosm, supplemented with crude oil and EPS₂₀₀₃ (SW+OIL+EPS₂₀₀₃); this system was monitored for 2 days and compared to control microcosm (only oil-polluted seawater, SW+OIL). Determination of bacterial abundance, heterotrophic cultivable and hydrocarbon-degrading bacteria were carried out. Community composition of marine bacterioplankton was determined by 16S rRNA gene clone libraries. Data obtained indicated that bioemulsificant addition stimulated an increase of total bacterial abundance and, in particular, selection of bacteria related to Alcanivorax genus; confirming that EPS₂₀₀₃ could be used for the dispersion of oil slicks and could stimulate the selection of marine hydrocarbon degraders thus increasing bioremediation process.

The Biotreatment of Oil-Polluted Seawater by Biosurfactant Producer Halotolerant Pseudomonas aeruginosa Asph2

In this study, a halotolerant Pseudomonas aeruginosa Asph2 was used to bioremediate oil polluted seawater with total petroleum hydrocarbon content of 5 g/L in a batch system using a local, readily available, and commercial nutrient, corn steep liquor. P. aeruginosa Asph2 expressed good biodegradation capabilities for different petroleum hydrocarbon components, recording ≈ 58, 64, 56, 55, and 53% for total petroleum hydrocarbon, saturates, aromatics, asphaltenes, and resins, respectively, within 21 days of incubation at 30°C, pH 7, and 150 rpm. P. aeruginosa Asph2 proved good uptake of crude oil with high production of rhamnolipid biosurfactant. The produced biosurfactant exhibited low surface tension of 36 dyne/cm, low critical micelle concentration of 20 mg/L, and good emulsification index E24 of 55%.

Oil-polluted Sea Water Purification by Carbonized Rice Hull

In recent years, marine oil pollution resulting from exploitation spills and accidents during oil transportation and use has affected the marine ecosystem safety, and oil polluted sea water remediation becomes a global problem. Rice hull possesses a good property of adsorption pollutants and it can be easily obtained from the abundant produce of rice all around the world. This experiment used carbonized rice hull (CRH) as adsorbent, aiming to purify oil polluted sea water and explore optimal adsorption conditions and effects. Six sets of experiments were done under the initial oil concentration of 1.35 mg/L and CRH dosages of 0, 6.67, 13.33, 20, 26.67, 33.33 g/L, separately. Seventy percent of oil was removed under the ideal dosage of 13.33 g/L, getting the minimum oil concentration of 0.39 mg/L. Another six sets of experiments were also done under the adsorption time of 0 h, 1 h, 2 h, 3 h, 4 h, 5 h and the same CRH dosage of 13.33 mg/L. The ideal removals of COD (35.5%) and oil (71%) were obtained after 3 hours adsorption, while the highest COD removal gets to 47.5%.

Bioremediation of Heavily Oil-Polluted Seawater by a Bacterial Consortium Immobilized in Cocopeat and Rice Hull Powder

We examined the effectiveness of cocopeat and rice hull powder obtained from agricultural wastes as biocarriers for an oil-degrading bacterial consortium. Scanning electron microscopy revealed colonization and strong attachment of bacterial cells on the surface of both carriers. Results of a 60-day in vitro seawater bioremediation trial showed significant oil reduction and high cultivable bacterial counts in treatments augmented with the carrier-attached bacterial consortia compared to treatments supplemented with the same consortium in free living and encapsulated forms. Significant degradations in both aliphatic and aromatic fractions were obtained in treatments augmented with carrier-immobilized consortia. The developed immobilized cells showed sustained activities and viabilities during storage for six months. Results of this study demonstrated that inexpensive waste materials can be utilized as biocarriers of an oil-degrading consortium and that immobilization on biocarriers can enhance the bioremediation of oil-contaminated seawater.

Modeling the bidirectional reflectance distribution function of seawater with spilt oil

Study on the bidirectional reflectance distribution function (BRDF) of seawater with spilt oil will provide a theoretical basis for detection of oil film on sea surface and oil emulsion in sea water, which will be of great significance for protection of marine environment and marine ecological balance. In this paper a model of BRDF for oil-polluted seawater has been developed by applying Monte Carlo method and Mie scattering theory. The BRDFs of clean seawater, oil-covered seawater, and oil-emulsion seawater are investigated at wavelengths of 532 nm and 355 nm. Simulation results of different film thicknesses and oil emulsion concentrations are presented. Results show that the BRDF is rather sensitive to the degree of pollution in seawater. The presence of oil film or oil emulsion will cause a decrease of the BRDF. At the same angles of observation, the BRDF value of seawater decreases with the increase of oil film thickness and oil emulsion concentration. Oil spill detecting and monitoring can potentially be achieved using BRDF data from optical sensors.

Bioremediation (bioaugmentation/biostimulation) trials of oil polluted seawater: A mesocosm simulation study

Bioaugmentation (amendment with selected bacterial strains) and/or biostimulation (nutrients addition and/or air supply) are relatively new fields in environmental microbiology for preventing pollution and cleanup contamination. In this study, the efficiency of application of bioaugmentation/biostimulation treatments, for recovery of crude oil-polluted seawater, was evaluated. Three different series of experiments were performed in a “Mesocosm Facility” (10.000 L). Natural seawater was artificially polluted with crude oil (1000 ppm) and was amended with inorganic nutrients (Mesocosm 1, M1), inorganic nutrient and an inoculum of Alcanivorax borkumensis SK2T (Mesocosm 2, M2) and inorganic nutrient and an inoculum of A. borkumensis SK2T and Thalassolituus oleivorans MIL-1T (Mesocosm 3, M3), respectively. During the experimental period (20 days) bacterial abundance (DAPI count), culturable heterotrophic bacteria (CFU count), MPN, microbial metabolic activity [Biochemical Oxygen Demand and enzymatic activity (leucine aminopeptidase LAP, β-glucosidase BG, alkaline phosphatase AP)] and quali-, quantitative analysis of the composition of total extracted and resolved hydrocarbons and their derivates (TERHCs) were carried out. The microbiological and physiological analysis of marine microbial community found during the three different biostimulation and bioaugmentation assays performed in mesocosms show that the load of crude oil increases total microbial abundance, inhibits the activity of some enzymes such as LAP while stimulates both AP and BG activities. The biodegradation results show that bioaugmentation with A. borkumensis SK2T alone is able to produce the highest percentage of degradation (95%) in comparison with the biostimulation treatment (80%) and bioaugmentation using an Alcanivorax-Thalassolituus bacterial consortium (70%). This result highlights the reduced biodegradation capability of the consortium used in this study, suggesting an unfavourable interaction between the two bacterial genera.

Effect of different bioremediation techniques on petroleum biomarkers and asphaltene fraction in oil-polluted sea water

The present study has clearly demonstrated that seeding a petroleum hydrocarbon polluted sea water with a halotolerant Pseudomonas aeruginosa Asph2 and corn steep liquor as a cheap and readily available source of nutrients significantly enhances the progress of biodegradation BD of petroleum hydrocarbon pollutants. There was a statistically high significant difference between natural weathering NW and both bioaugmentation BA (p = 2.92e-14) and biostimulation BS (p = 3.56e-13) at 95% confidence interval (α = 0.05). BA significantly improved the efficiency of total petroleum hydrocarbon TPH and the recalcitrant asphaltene degradation by ≈ 23 and 17% compared to BS process (p = 2.0693e-5 and p = 1.4e-3, respectively). The BD of biomarkers; pristane Pr, phytane Ph, and terpanes were very apparent. The BD of C28 tricyclic terpane, C27 13β, 17α- diasterane (20S), and C30 17α, 21β-hopane were higher than that of C35 17α,21β-homohopane. The BD of C27 18α(H)-22,29,30-trisnorneohopane (Ts) was higher than that of C27 17α(H)-22,29,30-trisnorhopane (Tm). The BD of sterane was higher than that of hopane. C30 18α-Oleanane was more resistant to degradation than other compounds.

Study on the Adsorption Efficiency of Carbonized Rice Hull Adsorption Bag for the Removal of Oil from Sea Water

With the increasing incidence of accidental oil spills, there is now a growing worldwide concern about the urgent need to purify oil-polluted sea water and conserve the marine ecosystem. Carbonized rice hull (CRH) prepared in the open air has been studied as adsorbent for purification of oil-polluted sea water. The adsorption effects of CRH and CRH absorption bag were both investigated. The results showed that under the dosage of 20 g/L and initial oil concentration of 746, 520 and 380 μg/L, the obtained oil removal efficiencies were 59.0%，78.8% and 67.1%, respectively. The adsorption bag counterpart indicated that under the initial oil concentration of 546 μg/L, an equilibrium state was reached for all the three kinds of package bags. The obtained adsorption amounts were 21.7, 25.5, 22.8 μg/g and the corresponding removal efficiencies were 59.7%, 70.0% and 62.6%, respectively.