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Electronic Journal of Biotechnology

versão On-line ISSN 0717-3458

Electron. J. Biotechnol. vol.19 no.5 Valparaíso set. 2016

http://dx.doi.org/10.1016/j.ejbt.2016.07.003 

 

REVIEW

 

Natural carriers in bioremediation: A review

 

Anna Dzionek, Danuta Wojcieszyńska, Urszula Guzik*

Department of Biochemistry, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Jagiellonska 28,40-032 Katowice, Poland


ABSTRACT

Bioremediation of contaminated groundwater or soil is currently the cheapest and the least harmful method of removing xenobiotics from the environment. Immobilization of microorganisms capable of degrading specific contaminants significantly promotes bioremediation processes, reduces their costs, and also allows for the multiple use of biocatalysts. Among the developed methods of immobilization, adsorption on the surface is the most common method in bioremediation, due to the simplicity of the procedure and its non-toxicity. The choice of carrier is an essential element for successful bioremediation. It is also important to consider the type of process ( n s tu or ex s tu), type of pollution, and properties of immobilized microorganisms. For these reasons, the article summarizes recent scientific reports about the use of natural carriers in bioremediation, including efficiency, the impact of the carrier on microorganisms and contamination, and the nature of the conducted research.

Keywords: Adsorption, Bioethanol production, Contamination, Heavy metals, Immobilization, Immobilized microorganisms, Natural carriers, Wine alterations, Wood barrels, Xenobiotics


 

1. Introduction

The twentieth century went down in history as a period of extremely dynamic civilizational and technological development. Industrialization, wars, and intensive use of large-scale heavy metals and synthetic xenobiotics led to many environmental problems.

The contamination of the environment by petroleum products, pharmaceutical compounds, chloro- and nitrophenols and their derivatives, polycyclic aromatic hydrocarbons, organic dyes, pesticides and heavy metals is a serious problem. These pollutants enter the environment by different ways. For example, one of the major consequences of the armed conflict between Iraq and Kuwait was the release into the environment millions of barrels of crude oil. After the war ended, scientists began numerous studies aimed at the removal of oil from the contaminated environment. Other sources of crude oil in ecosystems are accidental oil spills. One of the biggest marine disasters took place in Mexico in 2010, and it resulted in the spewing out of about 2.8 million barrels of crude oil from the British Petroleum (BP) oil rig Deepwater Horizon into the sea.

Pesticides are other serious pollutants present in soils. USEPA reported that in 2007, global consumption of pesticides for agricultural purposes was 2.36 million tonnes. These compounds, used in bulk for long periods of time in a limited area, lead to serious disorders in indigenous microflora and humans, because pesticides are also toxic to non-target organisms. Moreover, many metabolites of pesticide biodegradation are also toxic and constitute priority pollutants. For example, the major metabolites of parathion and 2,4-dichloropenoxy acetic acid biodegradation are p-nitrophenol and 2,4-dichlorophenol, respectively.

It has been reported that many microorganisms are able to biodegrade different pollutants. However, the biodegradation rate depends on the physiological state of the microorganisms, which are sensitive to variable environmental factors. It is known that immobilization improves microorganisms' resistance to unfavourable environmental impacts.

The main purpose of this review is to present and discuss the latest reports about the natural carriers in the processes of bioremediation by immobilized cells. In the article immobilization methods for bioremediation are also presented.

2. Bioremediation methods

In 1930 Tausz and Donath presented the idea of using microorganism to clean soil contaminated with petroleum derivatives, giving rise to biodegradation processes. Today, bioremediation is a commonly used method to restore the natural and useful values of contaminated sites by microorganism able to degrade, transform, or chelate various toxic compounds. Microorganisms can break down organic pollutants by using them as a source of carbon and energy, or by cometabolism. Heavy metals cannot be degraded or destroyed biologically and undergo transformation from one oxidative state or organic complex to another. It changes their water solubility and decreases their toxicity.

Bioremediation is eco-friendly, non-invasive, cheaper than conventional methods, and it is a permanent solution that can end with degradation or transformation of environmental contaminants into harmless or less toxic forms. Soil bioremediation can be carried out at the place of contamination (in situ), or in a specially prepared place (ex situ). in situ technology is used when there is no possibility to transfer polluted soil, for example when contamination affects an extensive area.

There are three basic methods of in situ bioremediation with microorganisms: natural attenuation, biostimulation, and bioaugmentation.

Natural attenuation is connected with the degradation activities of indigenous microorganisms. This method avoids damaging the habitat, allows ecosystem revert to its original condition and enables detoxification of toxic compounds.

Removal of contaminations by the natural attenuation takes a long time because degrading microorganisms in soil represent only about 10% of the total population. The increase of bioremediation efficiency in situ may be realized in the bioaugmentation process, in which the specific degraders are introduced into the soil. This method is applied when the indigenous microflora are unable to break down pollutants, or when the population of microorganisms capable of degrading contaminants is not sufficiently large. To make the process of bioaugmentation successful, microorganisms introduced into the polluted environment as a free or immobilized inoculum should be able to degrade specific contamination and survive in a foreign and unfriendly habitat, be genetically stable and viable, and move through the pores in the soil. Microorganisms can be previously isolated from the contaminated soil and propagated, or their functional ability can be enhanced in the laboratory. Nonindigenous strains or genetically modified microorganisms (GMM) can also be incorporated into the remediated soil. However, the result of bioaugmentation depends on the interaction between exogenous and indigenous populations of microorganisms because of the competition, mainly for nutrients.

To accelerate in situ bioremediation processes, biostimulation is used in order to modify the physical and chemical parameters of the soil. For this purpose, compounds such as nutrients (e.g. biogas slurry, manure, spent mushroom compost, rice straw and corncob) or electron acceptors (phosphorus, nitrogen, oxygen, carbon) are introduced into the soil.

Because in situ processes are out of hand it is difficult to predict the effect of remediation of contaminated sitesEx situ methods allow more efficient removal of pollutants, by controlling the physico-chemical parameters, resulting in a shortening of the total time of reclamation. These advantages outweigh ex situmethods' disadvantages such as additional cost and risk connected with the possibility of dispersion of the contamination during transport. During the ex situ processes contaminated medium is excavated or extracted and moved to the process location. Liquids can be clean in constructed wetlands while semi-solid or solid wastes in slurry bioreactors. Solid contaminations are biodegraded through land farming, composting and biopiles.

Constructed wetlands are used with success in the treatment of wastewater derived from domestic, industrial or agricultural sources. They require the competition of microbes (bioremediation) and plant (phytoremediation). Microorganisms degrade or sorb organic substance present in the water undergoing treatment. Plants are used to remove, transfer or stabilize contaminants through metabolism, accumulation, phytoextraction or immobilization at interface of roots and soil. Bioremediation processes in slurry bioreactors can be performed under aerobic or anaerobic conditions. These systems utilize naturally occurring microorganisms or strains possessing specific metabolic capabilities to transform toxic compounds. Slurry bioreactors are one of the best applied technologies used in the bioremediation of contaminated soils because they undergo under controlled operating conditions. It allows for the enhancement of microorganisms activity.

Landfarming is one of the most widely used soil bioremediation technologies. In this technology, excavated contaminated soils are spread out in a thin layer on the ground surface. Aerobic microbial activity within the soil is stimulated through the aeration and addition of minerals, nutrients and moisture. Landfarming is a relatively simple technology however it is inexpensive and effective for easily biodegradable contaminants only at low concentration. Composting is a controlled biological process that treats of agricultural and municipal solid wastes and sewage sludge using microorganisms under thermophilic and aerobic conditions. Through composting, it is possible to reduce the volume of residues in landfills.

Biodegradation of solid contaminants takes place mainly as a result of oxidation and hydrolysis. The optimum temperature for growth of microorganisms engaged in composting is in the range of 40 to 70°C. The risk of contamination by pathogens is small, because most of them are inactivated at 70°C. A key factor during composting is microbial accessibility to the pollutants and the characteristics of the amending agents. This method is eco-friendly, has simple protocols, allows the control of large volumes of waste and ends with the total mineralization of pollutants. Composting has been applied to bioremediation of soils contaminated with petroleum hydrocarbons, solvents, chlorophenols, pesticides, herbicides, polycyclic aromatic hydrocarbons and nitro-aromatic derivatives. Moreadvanced systems of composting are biopiles that are more expensive but enable more effective control of the process and its higher efficiency. It is possible as the aerated composted piles are equipped with the dissolved oxygen, moisture and nutrient control systems and the proper aeration is forced by vacuum or injection system. This technology has been used for remediation of petroleum-contaminated soil.

3. Immobilization methods

In recent times, bioremediation processes more and more often employ immobilization methods. Immobilization is defined as limiting the mobility of the microbial cells or their enzymes with a simultaneous preservation of their viability and catalytic functions. This process may use the natural ability of microorganisms to form biofilms on the surface of various materials, which is commonly observed in the environment. Immobilization significantly reduces costs of bioremediation processes and improves their efficiency. This method brings many benefits to bioremediation, such as higher efficiency of pollutant degradation, multiple use of biocatalysts, reduced costs — the stage of cell filtration is eliminated, ensuring a stable microenvironment for cells/enzymes, a reduced risk of genetic mutations, ensured resistance to shear forces present in bioreactors, increased resistance of biocatalysts to adverse environmental conditions and heavy metals, increased biocatalyst survival during storage, and increased tolerance to high pollutant concentrations.

There are five main techniques of immobilization: adsorption, binding on a surface (electrostatic or covalent), flocculation (natural or artificial), entrapment, and encapsulation (Fig. 1). Flocculation does not require carriers, and therefore will not be discussed.

3.1. Adsorption

Immobilization of microbial cells and enzymes by adsorption takes place through their physical interaction with the surface of water-insoluble carriers. This method, commonly used in bioremediation processes, is quick, simple, eco-friendly and cost-effective. Adsorption on a carrier surface is achieved by the formation of weak bonds. For that reason there is a high probability of cells leaking from the carrier into the environment, and this method is not used for GMM immobilization.

3.2. Binding on a surface

Electrostatic binding on a surface is very similar to physical adsorption, but the probability of microorganisms leaking is lower. This method requires washing the surface of the carrier with a buffer solution to obtain a hydrophilic surface that can attract the negatively charged cells or enzymes.

The procedure for immobilization is different in the case of covalent binding, because it requires the presence of a binding agent. Immobilization can be performed only on chemically activated carriers enriched with amide, ether and carbamate bonds. This method is mainly used for the immobilization of enzymes, because binding agents are often toxic to cells, and for that reason microbial viability and activity are lowered. The advantage of the covalent bonds is that they are strong enough to prevent the leaking of molecules into the environment.

 

Fig. 1. Methods of immobilization.

3.3. Entrapment in porous matrix

Entrapment of microorganisms is well-known and widely used in bioremediation. After the entrapment, microbial cells are able to move only within a carrier. This prevents the cells from leaking into the environment but may limit the exchange of nutrients and metabolites. Microorganisms entrapped in the heterogeneous carrier are physiologically diverse. The cells located near the surface have high metabolic activity in contrast to starved cells in the interior of the carrier. Entrapment is a rapid, nontoxic, inexpensive and versatile method. Entrapped microorganisms are protected against environmental factors. The most important parameter in entrapment of microorganisms is the ratio of the size of the pores of the carrier to the size of the cells. In a situation where the pores are larger than the immobilized cells, they leak into the environment.

3.4. Encapsulation

Encapsulation is very similar to the entrapment, but in this case immobilized particles are separated from the external environment with a semi-permeable membrane. The biggest advantage of this method is the significant protection of biological material against the adverse conditions of the external environment. However, due to the limited permeability of the used membrane and the probability of its damage by growing cells, encapsulation is rarely used in ex situ bioremediation.

4. Support materials

Not every material is suitable for immobilization. A good carrier should be insoluble, non-toxic, both for the immobilized material and the environment, easily accessible, inexpensive, stable and suitable for regeneration. The immobilization process should be simple and harmless. Another important aspect is that different immobilization methods require carriers with specific properties. For example, carriers used for adsorption or binding on the surface should have a high porosity to ensure that the contact area of the immobilized material and the carrier is as large as possible. The nature of performed bioremediation processes also has an impact on the choice of the carrier. Carriers used in bioaugmentation ought to be readily biodegradable. In wastewater treatment processes the carrier should have a high mechanical resistance because it may be exposed to different kinds of physical forces.

Carriers are classified as organic and inorganic or natural or synthetic. Natural organic carriers have many functional groups which stabilize biocatalysts. This class of carriers includes: alginate, K-carrageenan, chitosan, sawdust, straw, charcoal, plant fibres, corncob, bagasse, rice, husks of sunflower seeds, diatomite and mycelium. These supports are hydrophilic, biodegradable, biocompatible, and inexpensive because they are mostly waste from the food industry. However, the possibility of their application in bioremediation processes is limited because of low resistance to biodegradation, sensitivity to organic solvents, and stability in a narrow pH range.

Synthetic organic carriers have numerous functional groups with diversified characters. This class includes polypropylene, polyvinyl chloride, polystyrene, polyurethane foam, polyacrylonitrite and polyvinyl alcohol. Their advantage is the possibility to regulate their structure at the macromolecular level — the selection of the proper molecular weight, the spatial structure and the manner and arrangement order of each active functional group in the chain. Moreover, during synthesis, the porosity, pore diameter, polarity and hydrophobicity of the carrier may be controlled. Furthermore, synthetic supports can be formed into various shapes (tubes, membranes, coatings, carriers of various shapes from spherical to oval), and they are easily available and relatively inexpensive.

Inorganic carriers (natural and synthetic) have a high chemical, physical and biological resistance. They are represented by magnetite, volcanic rocks, vermiculite, porous glass, silica-based materials, ceramics and nanoparticles. Asignificant disadvantage of these carriers is the presence of a small number of functional groups, which prevents sufficient bonding of the biocatalyst. For that reason they are used in the formation of hybrid carriers, combining natural polymers and synthetic nanoparticles.

5. Immobilization in bioremediation

Higher biodegradation efficiency observed after the use of immobilized microorganisms in comparison to free ones caused the increase interest in their application in bioremediation processes. It is assumed that carrier protects and hinders the spread of organic pollutants and in this way reduces the surface contaminants concentration on the immobilized microorganisms. Moreover, changes in microenvironment after immobilization may lead to changes in cell morphology, physiology and metabolic activity. Wastes from the food industry are very good and inexpensive candidates for carriers. Some researchers have also started to explore inorganic adsorbents, such as expanded perlite or tezontle. Table 1 presents a list of carriers used in bioremediation processes.

5.1. Plant fibres

The most often applied vegetable fibre in immobilization is a sponge derived from Luffa cylindrica or Luffa aegyptiaca. These plants grow in tropical and subtropical climates. The loofah sponge shows important advantages required for immobilization processes: high porosity (85-95%) with simultaneous low density (0.018-0.05 g/cm3). The sponge is composed of fibre networks that form an open and free space for the exchange of matter.

The first usage of the loofah sponge was reported in 2003. Microalgal-luffa sponge immobilized discs were applied in nickel biosorption processes. It has been shown that loofah sponge restricts the leaking of the immobilized biomass into the environment. It is an extremely stable carrier and can be regenerated at least 7 times. Mazmanci et al. reported that the loofah sponge was a source of carbon and energy for white rot fungi, and therefore should not be used for their immobilization (long-term bioremediation). On the other hand, it provides an excellent support for in situ or short-term bioremediation (without a source of carbon and energy) with these fungi.

5.2. Sugarcane bagasse

Sugarcane bagasse, derived from the extrusion of a plant Saccharum officinarum, is widely used for the production of ethanol, and is an excellent biosorbent. Bagasse is rich in carbohydrates, mainly lignin and cellulose. The spatial structure of bagasse is formed by parallel-arranged fibres and micropores (0.5-5 µm). It is an ideal place to attachment bacteria and fungal hyphae. Another advantage of this carrier is its mechanical strength. After centrifugation at 1500 rpm no disintegration or microorganism leaking into the medium were observed.

Mohammadi and Nasernejad demonstrated that immobilization of Phanerochaete chrysosporium on sugarcane bagasse significantly increased the production and activity of manganese peroxidase during the biodegradation of anthracene. After the immobilization of Acinetobacter venetianus on this carrier, a higher rate of tetradecane degradation was observed. This was probably connected with binding of the contaminant on the hydrophobic surface of the carrier, and in consequence the easier access of microorganisms to hydrocarbon. Increased efficiency of phenol degradation by immobilized Candida tropicalis PHB5 was also observed. The microorganisms immobilized on the bagasse are suitable for bioremediation in bioreactors because they remain active for up to 8 bioremediation cycles.

Table 1
Natural carriers used in bioremediation.

..

5.3. Sawdust

One of the most common agro-wastes is sawdust, which has been successfully used for the immobilization of bacterial cells. Arthrobacter sp. immobilized on sawdust did not lose their enzymatic activity after 6 weeks of storage (at 25°C and 45°C) and was still able to degrade

similar quantities of crude oil. Sawdust possesses a labyrinthine structure providing very high surface area for cellular attachment. High hydrophilicity of this carrier may hamper the adsorption of oil-degrading microorganisms on the carrier. However, this difficulty may be overcome by non-toxic hydrophobic coating of sawdust. Hazaimeh et al. during studies on degradation of oil by a bacterial immobilized consortium, demonstrated that immobilization significantly increased the production of biosurfactants by bacteria. This was to increase the solubility, and thus the bioavailability of hydrophobic hydrocarbons.

5.4. Corncob

Materials derived from agro-industrial residues (AIR), such as corncobs, offer many advantages over synthetic matrices. Corncobs are robust, porous and perforated. This increases the attachment area for organisms and allows their growth without limiting diffusion. Corncobs have a high water holding capacity, improve soil structure and oxygen diffusion, are readily available in maize processing plants, and their usage in the processes of bioremediation provides an alternative method of AIR disposal.

The first study of corncobs used as a carrier in bioremediation showed that they are a good carrier for the bioaugmentation of soil contaminated with oily-sludge. It was also noted that after the introduction of immobilized bacteria, the degree of oxygenation of the lower layers of the soil had increased as a result of the creation of air pockets by corncobs. Plangklang et al. showed that Burkholderia cepacia PCL3 bacteria grow very well on the surface of the corncob, and thereby leaked into the medium due to the lack of space on the carrier. Rivelli et al. observed the increased degradative activity after immobilization of bacteria on corncob powder. Additionally, this carrier stabilized soil and improved the oxygen diffusion and the water-mass transfer.

5.5. Expanded perlite

Volcanic rocks are known for their sorption and mechanical properties. They are widely used in construction, filters and hydroponics. One of these rocks is perlite which is excavated worldwide. Because crude perlite has a relatively high density and small surface area, it is subjected to heat treatment, resulting in a significant extension and the forming of air bubbles inside. Expanded perlite obtained in this way has a low density (0.032-0.4 g/cm3), high porosity, and high surface area.

For the first time, expanded perlite was used for the bioremediation studies by Paca et al.. It was shown that biofilter consisted of perlite particles with immobilized cells of Pseudomonas aeruginosa was more effective in styrene biodegradation. Emtiazi et al. demonstrated that the transformed cells ofEscherichia coli immobilized on perlite were more genetically stable than in other carriers, and they were able to produce biosurfactants, which increased the solubility of petroleum hydrocarbons, and therefore the degree of their biodegradation.

5.6. Tezontle

Tezontle is a volcanic rock tested recently as a carrier in bioremediation. This rock is commonly used in Mexico as a building material, and has a characteristic reddish colour (due to the presence of iron ions). The surface is highly porous and perforated, which provides a good place for biofilm formation by microorganisms.

Santacruz et al. demonstrated that Pseudomonas fluorescens immobilized on a tezontle biofilter is able to degrade DDT up to 999.8 mg/L per day and 2,4-dichlorophenoxyacetic acid up to 2634 mg/L per day. Yáñez-Ocampo et al. observed biodegradation of a methyl-parathion and tetrachlorvinphos mixture by a consortium of bacteria immobilized on tezontle. They showed a decrease in the optical density of bacteria after 13 d of the experiment, whereas the death of free cells occurred after 6 d. In addition, the immobilized cells did not require supplementation with glucose during pollutant breakdown. This demonstrates that after immobilization the new environment is more friendly for bacteria which are able to degrade greater amounts of insecticides. Similar results were obtained by Abdel-Razek et al. during research on methyl-parathion biodegradation by transformed E. coli RAZEK immobilized on tezontle.

5.7. Other carriers

Recently, increasing interest is observed in the usage of coco-peat, husks of sunflower seeds and cotton fibres as carriers in bioremediation. These carriers have not gained popularity yet, but so far studies have shown their promising possibilities in bioremediation.

Nunal et al., during the biodegradation of heavy-oil by a bacterial consortium immobilized on coco-peat, showed that the carrier, because of its porous and perforated surface, is a good place to create a stable biofilm. Moreover, they observed that the immobilized bacteria, after 60 d of the experiment, degraded 86.6% of the heavy-oil, while the free cells decomposed only 51.2% of it. After 90 d of storage, bacteria immobilized on the coco-peat had a greater survival rate than those encapsulated in sodium alginate. This makes coco-peat an excellent candidate carrier in bioaugmentation.

Bioremediation of crude oil by Rhodococcus spp. QBTo immobilized on sunflower seed husks, also shown that immobilization improves the survival and enzymatic activity of microorganisms. After 120 d of storage at 10°C the bacterial survival rate was about 76%, and therefore sunflower seed husks are an appropriate carrier for the bioaugmentation of contaminated soils.

Lin et al. noted that the negative charge and the presence of hydroxyl and carboxylic acid groups make cotton fibres a good carrier for immobilization of microorganisms. It was shown that Acinetobacter sp. HC8-3S degraded more than 70% of the crude oil with 90 g/L NaCl, whereas free cells degraded about only 15% under the same conditions. This opens up the possibility of inexpensive bioremediation in areas of high salinity by immobilized microorganisms. The authors showed that the adsorption properties of cotton fibres allow the use of this carrier for the biodegradation of floating oil from oil spills.

5.8. Pros and cons ofnatural and synthetic carriers

Application of immobilized cell systems in bioremediation indicates several advantages over the usage of free microorganisms: prolonged activity, stability of biocatalyst, feasibility of continuous processing, increased tolerance to high toxic compounds concentration, easier recovery, possibility of regeneration and reuse of biocatalyst, reduction of microbial contamination risk and ability to use smaller bioreactors with simplified process. Because each support has its own requirements in terms of the microorganisms used and the degraded compounds, the support selection is a key step which influences the success of bioremediation process.

The main feature of the carriers is mechanical resistance, which allows to the recovery, regeneration and reuse of biocatalyst in bioremediation processes. This feature is typical for sawdust, wood chips, shavings, loofah sponge and polyvinyl alcohol beads, polyurethane foam, among from natural and synthetic carriers, respectively. In bioremediation processes very important is the use of low-price and easy accessible carriers because only than they may be applied on the large scale. This condition fulfils plant residue, polyvinyl alcohol beads, polyurethane foam, different ceramics, and natural polymers such as agarose, K-carrageenan, alginate, agar, and chitosan. However, most of the natural polymers are non-mechanically resistant. One of the most often described natural carriers is alginate. It is cheap, biocompatible, non-toxic and easy to use. Unfortunately, it cannot be used in continuous conditions because of the problems with gel degradation and low physical strength resulting in the leakage of immobilized microorganisms from the matrix.

Equally important carriers potentially useful in bioremediation have to meet other requirements of good matrices: non-toxicity and insolubility. These features characterize both natural (chitosan, loofah sponge,corncob,sawdust,tezontle,sugarcanebagasse,woodchips) and synthetic (polyvinyl alcohol, polyurethane, polypropylene, polystyrene) carriers.

It is possible to find among both natural and synthetic carriers almost ideal one, which may be used with success in bioremediation. However, the predominance in the usage of natural carriers is connected with their biodegradability, renewability and availability in nature. Moreover, many of natural carriers are agro-waste that may be further used in biotechnological processes. The immobilization of microorganisms on natural carriers is environmentally friendly because it causes less disposal problems that may occur for synthetic ones.

6. Conclusions

Interest in organic carriers, which are wastes from the agricultural and food industries, increases continuously, because they are very good material for immobilization. All of them have many functional groups, which positively affect the degree of colonization by microorganisms. Moreover, volcanic rocks (expanded perlite and tezontle) are also known as carriers which have good sorption properties and high mechanical resistance.

Carriers such as the loofah sponge and corncob have been used with success in bioremediation in situ, and the former has also shown the greatest support for pesticide biodegradation. In ex situ bioremediation the best results have been obtained using carriers such as bagasse, sawdust, expanded perlite and tezontle. Coco-peat, sunflower seed husks, cotton fibres and porous glass seem to be promising materials for immobilization, although their application requires further studies.

Conflict of interest

The authors declare no conflict of interest. 

Financial support

This work was financed by the Ministry of Science and Higher Education (Poland).

 

References

1. Bayat Z, Hassanshahian M, Cappello S. Immobilization of microbes for bioremediation of crude oil polluted environments: A mini review. Open Microbiol J 2015;9:48-54. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4676050/pdf/TOMICROJ-9-48.pdf.         [ Links ]

2. Akhtar N, Iqbal J, Iqbal M. Microalgal-luffa sponge immobilized disc: A new efficient biosorbent for the removal of Ni(II) from aqueous solution. Lett Appl Microbiol 2003;37:149-53. http://onlinelibrary.wiley.com/doi/10.1046/j.1472-765X.2003.01366.x/epdf.         [ Links ]

3. Mohamed A, El-Sayed R Osman TA, Toprak MS, Muhammed M, Uheida A. Composite nanofibers for highly efficient photocatalytic degradation of organic dyes from contaminated water. Environ Res 2016;145:18-25. http://dx.doi.org/10.1016/j.envres.2015.09.024.         [ Links ]

4. Rodgers-Vieira EA, Zhang Z, Adrion AC, Gold A, Aitken MD. Identification of anthraquinone-degrading bacteria in soil contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 2015;81:3775-81. http://dx.doi.org/10.1128/AEM.00033-15.         [ Links ]

5. Smutek W, Zdarta A, Guzik U, Dudziñska-Bajorek B, Kaczorek E. Rahnella sp. strain EK12: Cell surface properties and diesel oil biodegradation after long-term contact with natural surfactants and diesel oil. Microbiol Res 2015;176:38-47. http://dx.doi.org/10.1016/j.micres.2015.04.008.         [ Links ]

6. Wasilkowski D, Mrozik A, Piotrowska-Seget Z, Krzyzak J, Pogrzeba M, Plaza G. Changes in enzyme activities and microbial community structure in heavy metal-contaminated soil under in situ aided phytostabilization. Clean Soil Air Water 2014;42:1618-25. http://dx.doi.org/10.1002/clen.201300631.         [ Links ]

7. Wojcieszyńska D, Domaradzka D, Hupert-Kocurek K, Guzik U. Bacterial degradation of naproxen - Undisclosed pollutant in the environment. J Environ Manage 2014;145:157-61. http://dx.doi.org/10.1016/j.jenvman.2014.06.023.         [ Links ]

8. Wojcieszyńska D, Hupert-Kocurek K, Guzik U. Factors affecting activity of catechol 2,3-dioxygenase from 2-chlorophenol-degrading Stenotrophomonas maltophilia strain KB2. Biocatal Biotransform 2013;31:141-7. http://dx.doi.org/10.3109/10242422.2013.796456.         [ Links ]

9. Greñ I, Wojcieszyńska D, Guzik U, Perkosz M, Hupert-Kocurek K. Enhanced bio-transformation of mononitrophenols by Stenotrophomonas maltophilia KB2 in the presence of aromatic compounds of plant origin. World J Microbiol Biotechnol 2010;26:289-95. http://dx.doi.org/10.1007/s11274-009-0172-6.         [ Links ]

10. Belanger M. The Gulf of Mexico oil spill response: A blueprint of disaster for Canadian wildlife. J Mar Anim Ecol 2010;3:3-4. http://www.oers.ca/journal/Volume3/Invited_Commentary_Final.pdf.         [ Links ]

11. Chatterjee C, Lefcovitch A. Gulf of Mexico oil disaster: Some legal issues. Amicus Curiae 2010;84:17-24. http://sas-space.sas.ac.uk/2902/1/Amicus84_Chatterjee.pdf.         [ Links ]

12. Moreno-Medina DA, Sánchez-Salinas E, Ortiz-Hernández ML. Removal of methyl parathion and coumaphos pesticides by a bacterial consortium immobilized in Luffa cylindrica. Rev Int Contam Ambiental 2014;30:51-63. http://scielo.unam.mx/pdf/rica/v30n1/v30n1a5.pdf.         [ Links ]

13. Mesnage R Defarge N, Spiroux de Vendômois J, Séralini GE. Major pesticides are more toxic to human cells than their declared active principles. Biomed Res Int 2014;2014:1-8. http://dx.doi.org/10.1155/2014/179691.         [ Links ]

14. Roberts JR Karr CJ. Pesticide exposure in children. Pediatrics 2012;130:e1757-63. http://dx.doi.org/10.1542/peds.2012-2757.         [ Links ]

15. Herrera Y, Okoh AI, Alvarez L, Robledo N, Trejo-Hernández MR. Biodegradation of 2,4-dichlorophenol by a Bacillus consortium. World J Microbiol Biotechnol 2008; 24:55-60. http://dx.doi.org/10.1007/s11274-007-9437-0.         [ Links ]

16. Wojcieszyńska D, Greñ I, Guzik U. New pathway of dichlorophenols degradation by Pseudomonas sp. strain US1 in aerobic conditions. Ecol Chem Eng A 2008;15:703-10. https://www.infona.pl/resource/bwmeta1.element.baztech-article-BPG4-0045-0011.         [ Links ]

17. Liu Z, Yang C, Qiao C. Biodegradation ofp-nitrophenol and 4-chlorophenol by Stenotrophomonas sp. FEMS Microbiol Lett 2007;277:150-6. http://dx.doi.org/10.1111/j.1574-6968.2007.00940.x.         [ Links ]

18. Gallizia I, McClean S, Banat IM. Bacterial biodegradation of phenol and 2,4- dichlorophenol.J ChemTechnol Biotechnol 2003;78:959-63. http: //dx.doi.org/10.1002/jctb.890.         [ Links ]

19. Lade H, Kadam A, Paul D, Govindwar S. Biodegradation and detoxification of textile azo dyes by bacterial consortium under sequential microaerophilic/aerobic processes. EXCLIJ 2015;14:158-74. http://dx.doi.org/10.17179/excli2014-642.         [ Links ]

20. Kaczorek E, Salek K, Guzik U, Jesionowski T, Cybulski Z. Biodegradation of alkyl derivatives of aromatic hydrocarbons and cell surface properties of a strain of Pseudomonas stutzeri. Chemosphere 2013;90:471 -8. http://dx.doi.org/10.1016/j.chemosphere.2012.07.065.         [ Links ]

21. Tausz J, Donath P. Über die Oxydation des Wasserstoffs und der Kohlenwasserstoffe Mittels Bakterien. Hoppe Seylers Z Physiol Chem 1930;190: 141-68. http://dx.doi.org/10.1515/bchm2.1930.190.3-6.141.         [ Links ]

22. Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP. Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front Plant Sci 2016;7: 303. http://dx.doi.org/10.3389/fpls.2016.00303.         [ Links ]

23. Garbisu C, Alkorta I. Basic concepts on heavy metal soil bioremediation. Eur J Miner Process EnvironProt2003;3:58-66.http://www.ejmpep.com/garbisu_and_alkorta.pdf.         [ Links ]

24. Perelo LW. Review: In situ and bioremediation oforganic pollutants in aquatic sed-iments.J Hazard Mater 2010;177:81-9.http://dxdoi.org/10.1016/johazmat2009.12.090.         [ Links ]

25. Kulik N, Goi A, Trapido M, Tuhkanen T. Degradation ofpolycyclic aromatic hydrocarbons by combined chemical pre-oxidation and bioremediation in creosote contaminated soil. J Environ Manage 2006;78:382-91.http://dx.doi.org/10.1016/j.jenvman.2005.05.005.         [ Links ]

26. Xu Y, Lu M. Bioremediation ofcrude oil-contaminated soil: Comparison ofdifferent biostimulation and bioaugmentation treatments. J Hazard Mater 2010;183: 395-401. http://dx.doi.org/10.1016/j.jhazmat.2010.07.038.         [ Links ]

27. Angelucci DM, Tomei MC. Ex-situ bioremediation of chlorophenol contaminated soil: Comparison of slurry and solid-phase bioreactors with the two-step polymer extraction-bioregeneration process. JChem Technol Biotechnol 2016;91:1577-84.http://dx.doi.org/10.1002/jctb.4882.         [ Links ]

28. Tomei MC, Daugulis AJ. Ex situ bioremediation of contaminated soils: An overview ofconventional an innovative technologies. Crit Rev Environ Sci Technol 2013;43: 2107-39. http://dx.doi.org/m1080/10643389.2012.672056.         [ Links ]

29. Suja F, Rahim F, Taha MR, Hambali N, Razali MR, Khalid A, et al. Effects of local microbial bioaugmentation and biostimulation on the bioremediation of total petroleum hydrocarbons (TPH) in crude oil contaminated soil based on laboratory and field observations. Int Biodeter Biodegr 2014;90:115-22. http://dx.doi.org/10.1016/j.ibiod.2014.03.006.         [ Links ]

30. Pimmata P, Reungsang A, Plangklang P. Comparative bioremediation ofcarbofuran contaminated soil by natural attenuation, bioaugmentation and biostimulation. Int Biodeter Biodegr 2013;85:196-204. http://dx.doi.org/10.1016/j.ibiod.2013.07.009.         [ Links ]

31. Simarro R González N, Bautista LF, Molina MC. Assessment of the efficiency of in situ bioremediation techniques in a creosote polluted soil: Change in bacterial community. J Hazard Mater 2013;262:158-67. http://dx.doi.org/10.1016/j.jhazmat.2013.08.025.         [ Links ]

32. Hamdi H, Benzarti S, Manusadzianas L, Aoyama I, Jedidi N. Bioaugmentation and biostimulation effects on PAH dissipation and soil ecotoxicity under controlled conditions. Soil Biol Biochem 2007;39:1926-35.http://dx.doi.org/10.1016/j.soilbio.2007.02.008.         [ Links ]

33. Alisi C, Musella R, Tasso F, Ubaldi C, Manzo S, Cremisini C, et al. Bioremediation of diesel oil in a co-contaminated soil by bioaugmentation with a microbial formula tailored with native strains selected for heavy metals resistance. Sci Total Environ 2009;407:3024-32. http: //dx.doi.org/10.1016/j.scitotenv.2009.01.011.         [ Links ]

34. Ueno A, Ito Y, Yumoto I, Okuyama H. Isolation and characterization of bacteria from soil contaminated with diesel oil and the possible use of these in autochthonous bioaugmentation. World J Microbiol Biotechnol 2007;23:1739-15.http://dx.doi.org/10.1007/s11274-007-9423-6.         [ Links ]

35. Kauppi S, Sinkkonen A, Romantschuk M. Enhancing bioremediation of diesel-fuel-contaminated soil in a boreal climate: Comparison of biostimulation and bioaug-mentation. Int Biodeter Biodegr 2011;65:359-68.http://dx.doi.org/10.1016/j.ibiod.2010.10.011.         [ Links ]

36. Georgieva S, Godjevargova T, Mita DG, Diano N, Menale C, Nicolucci C, et al. Non-isothermal bioremediation of waters polluted by phenol and some of its derivatives by laccase covalently immobilized on polypropylene membranes. J Mol Catal B: Enzym 2010;66:210-8. http://dx.doi.org/10.1016/jmolcatb.2010.05.011.         [ Links ]

37. EPA. in situ and ex situ biodegradation technologies for remediation of contaminated sites. Engineering issue 2006, EPA/625/R-06/015. http://clu-in.org/download/contaminantfocus/dnapl/Treatment_Technologies/ epa_2006_engin_issue_bio.pdf.         [ Links ]

38. Chen J, Wei XD, Liu YS, Ying GG, Liu SS, He LY, et al. Removal of antibiotics and antibiotic resistance genes from domestic sewage by constructed wetlands: Optimization of wetland substrates and hydraulic loading. Sci Total Environ 2016;565: 240-8.http://dx.doi.org/10.1016/j.scitotenv.2016.04.176.         [ Links ]

39. Mohan SV, Reddy BP, Sarma PN. Ex situ slurry phase bioremediation of chrysene contaminated soil with the function of metabolic function: Process evaluation by data enveloping analysis (DEA) and Taguchi design of experimental methodology (DOE). Bioresour Technol 2009;100:164-72. http://dx.doi.org/10.1016/j.biortech.2008.06.020.         [ Links ]

40. Prasanna D, Mohan SV, Reddy BP, Sarma PN. Bioremediation of anthracene contaminated soil in bio-slurry phase reactor operated in periodic discontinuous batch mode. J Hazard Mater 2008;153:244-51. http://dx.doi.org/10.1016/jjhazmat.2007.08.063.         [ Links ]

41. Silva-Castro GA, Uad I, Rodríguez-Calvo A, González-López J, Calvo C. Response of autochthonous microbiota of diesel polluted soils to land-farming treatments. Environ Res 2015;137:49-58. http://dx.doi.org/10.1016/j.envres.2014.11.009.         [ Links ]

42. Paudyn K, Rutter A, Rowe RK, Poland JS. Remediation of hydrocarbon contaminated soils in the Canadian Arctic by landfarming. Cold Reg Sci Technol 2008;3:102-14. http://dxdoi.org/10.1016/jxoldregions.2007.07.006.         [ Links ]

43. Maila MP, Cloete TE. Bioremediation of petroleum hydrocarbons through landfarming: Are simplicity and cost-effectiveness the only advantages? Rev Environ Sci Bio/Technol 2004;3:349-60. http://dx.doi.org/10.1007/s11157-004-6653-z.         [ Links ]

44. Antizar-Ladislao B, Beck AJ, Spanova K, Lopez-Real J, Russell NJ. The influence of different temperature programmes on the bioremediation of polycyclic aromatic hydrocarbons (PAHs) in a coal-tar contaminated soil by in-vessel composting. J Hazard Mater 2007;144:340-7. http://dx.doi.org/10.1016/jjhazmat.2006.10.031.         [ Links ]

45. Cai QY, Mo CH, Wu QT, Zeng QY, Katsoyiannis A, Férard JF. Bioremediation of polycyclic aromatic hydrocarbons (PAHs)-contaminated sewage sludge by different composting processes. J Hazard Mater 2007;142:535-42.http://dxdoi.org/10.1016/jjhazmat.2006.08.062.         [ Links ]

46. Golodyaev GP, Kostenkov Nm, Oznobikhin VI. Bioremediation of oil-contaminated soils by composting. Eurasian Soil Sci 2009;42:926-35. http://dxdoi.org/10.1134/S1064229309080110.         [ Links ]

47. Kourkoutas Y, Bekatorou A, Banat IM, Marchant R Koutinas AA Immobilization technologies and support materials suitable in alcohol beverages production: A review. Food Microbiol 2004;21:377-97. http://dx.doi.org/10.1016/j.fm.2003.10.005.         [ Links ]

48. Guzik U, Hupert-Kocurek K, Krysiak M, Wojcieszyńska D. Degradation potential of protocatechuate 3,4-dioxygenase from crude extract of Stenotrophomonas maltophilia strain KB2 immobilized in calcium alginate hydrogels and on glyoxyl agarose. Biomed Res Int 2014;2014:1-8. http://dx.doi.org/10.1155/2014/138768.         [ Links ]

49. Guzik U, Hupert-Kocurek K, Marchlewicz A, Wojcieszyńska D. Enhancement of biodegradation potential of catechol 1, 2-dioxygenase through its immobilization in calcium alginate gel. Electron J Biotechnol 2014;17:83-8.http://dxdoi.org/10.1016/j.ejbt2014.02.001.         [ Links ]

50. Guzik U, Hupert-Kocurek K, Wojcieszyńska D. Immobilization as a strategy for improving enzyme properties-Application to oxidoreductases. Molecules 2014;19: 8995-9018. http://dx.doi.org/10.3390/molecules19078995.         [ Links ]

51. Wojcieszyńska D, Hupert-Kocurek K, Jankowska A, Guzik U. Properties of catechol 2,3-dioxygenase from crude extract ofStenotrophomonas maltophilia strain KB2 immobilized in calcium alginate hydrogels. Biochem Eng J 2012;66:1-7.http://dxdoi.org/10.1016/j.bej.2012.04.008.         [ Links ]

52. Rivelli V, Franzetti A, Gandolfi I, Cordoni S, Bestetti G. Persistence and degrading activity of free and immobilised allochthonous bacteria during bioremediation of hydrocarbon-contaminated soils. Biodegradation 2013;24:1-11.http://dx.doi.org/10.1007/s10532-012-9553-x.         [ Links ]

53. Cristóvão RO, Tavares AP, Brígida AI, Loureiro JM, Boaventura RA, Macedo EA, et al. Immobilization of commercial laccase onto green coconut fiber by adsorption and its application for reactive textile dyes degradation. J Mol Catal B: Enzym 2011 ;72: 6-12. http://dx.doi.org/10.1016/j.molcatb.2011.04.014.         [ Links ]

54. Hou J, Dong G, Ye Y, Chen V. Laccase immobilization on titania nanoparticles and titania-functionalized membranes. J Membr Sci 2014;452:229-40. http://dx.doi.org/10.1016/j.memsci.2013.10.019.         [ Links ]

55. Hudson S, Magner E, Cooney J, Hodnett BK Methodology for the immobilization of enzymes onto mesoporous materials. J Phys Chem B 2005;109:19496-506. http://dx.doi.org/10.1021 /jp052102n.         [ Links ]

56. Lee CA, Tsai YC. Preparation of multiwalled carbon nanotube-chitosan-alcohol dehydrogenase nanobiocomposite for amperometric detection of ethanol. Sens Actuators B 2009;138:518-23. http://dx.doi.org/10.1016/j.snb.2009.01.001.         [ Links ]

57. Cabana H, Alexandre C, Agathos SN, Jones JP. Immobilization of laccase from the white rot fungus Coriolopsis polyzona and use of the immobilized biocatalyst for the continuous elimination of endocrine disrupting chemicals. Bioresour Technol 2009;100:3447-58. http://dx.doi.org/10.1016/j.biortech.2009.02.052.         [ Links ]

58. Yu CM, Yen MJ, Chen LC. A bioanode based on MWCNT/protein-assisted co-immobilization of glucose oxidase and 2,5-dihydroxybenzaldehyde for glucose fuel cells. Biosens Bioelectron 2010;25:2515-21. http://dx.doi.org/10.1016/j.bios.2010.04.016.         [ Links ]

59. Bleve G, Lezzi C, Chiriatti MA, D'Ostuni I, Tristezza M, Di Venere D, et al. Selection of non-conventional yeasts and their use in immobilized form for the bioremediation of olive oil mill wastewaters. Bioresour Technol 2011;102:982-9.http://dxdoi.org/10.1016/j.biortech.2010.09.059.         [ Links ]

60. Klein S, Avrahami R Zussman E, Beliavski M, Tarre S, Green M. Encapsulation of Pseudomonas sp. ADP cells in electrospun microtubes for atrazine bioremediation. J Ind Microbiol Biotechnol 2012;39:1605-13. http://dx.doi.org/10.1007/s10295-012-1164-3.         [ Links ]

61. Martins SCS, Martins CM, Fiuza LMC. Immobilization of microbial cells: A promising tool for treatment of toxic pollutants in industrial wastewater. Afr J Biotechnol 2013;12:4412-8. http://dx.doi.org/10.5897/AJB12.2677.         [ Links ]

62. Kariminiaae-Hamedaani HR, Kanda K, Kato F. Wastewater treatment with bacteria immobilized onto a ceramic carrier in an aerated system. J Biosci Bioeng 2003;95: 128-32. http://dx.doi.org/10.1016/S1389-1723(03)80117-2.         [ Links ]

63. Hou D, Shen X, Luo Q He Y, Wang Q Liu Q. Enhancement of the diesel oil degradation ability of a marine bacterial strain by immobilization on a novel compound carrier material. Mar Pollut Bull 2013;67:146-51.http://dx.doi.org/10.1016/j.marpolbul.2012.11.021.         [ Links ]

64. Sinha A, Pant KK, Khare SK. Studies on mercury bioremediation by alginate immobilized mercury tolerant Bacillus cereuscells. Int Biodeter Biodegr 2012;71: 1-8. http://dxdoi.org/10.1016/jjbiod.2011.12.014.         [ Links ]

65. Wojcieszyńska D, Hupert-Kocurek K, Guzik U. Influence of the entrapment of catechol 2,3-dioxygenase in K-carrageenan on its properties. Pol J Environ Stud 2013;22: 1219-25. http://www.pjoes.com/pdf/22.4/PolJ.Environ.Stud.Vol.22.No.4.1219-1225.pdf.         [ Links ]

66. Gentili AR, Cubitto MA, Ferrero M, Rodriguéz MS. Bioremediation of crude oil polluted seawater by a hydrocarbon-degrading bacterial strain immobilized on chitin and chitosan flakes. Int Biodeter Biodegr 2006;57:222-8. http://dx.doi.org/10.1016/j.ibiod.2006.02.009.         [ Links ]

67. Obuekwe CO, Al-Muttawa EM. Self-immobilized bacterial cultures with potential for application as ready-to-use seeds for petroleum bioremediation. Biotechnol Lett 2001;23:1025-32. http://dx.doi.org/10.1023/A:1010544320118.         [ Links ]

68. Huang DL, Zeng GM, Jiang XY, Feng CL, Yu HY, Huang GH, et al. Bioremediation of Pb-contaminated soil by incubating with Phanerochaete chrysosporium and straw. J Hazard Mater 2006;134:268-76. http://dx.doi.org/10.1016/jjhazmat.2005.11.021.         [ Links ]

69. Ullah H, Shah AA, Hasan F, Hameed A. Biodegradation of trinitrotoluene by immobilized Bacillus sp. YRE1. Pak J Bot 2010;42:3357-67. https://www.researchgate.net/publication/265571163.         [ Links ]

70. Pattanasupong A, Nagase H, Sugimoto E, Hori Y, Hirata K, Tani K, et al. Degradation of carbendazim and 2,4-dichlorophenoxyacetic acid by immobilized consortium on loofa sponge. J Biosci Bioeng 2004;98:28-33. http://dx.doi.org/10.1016/S1389-1723(04)70238-8.         [ Links ]

71. Paul D, Pandey G, Meier C, van der Meer JR, Jain RK. Bacterial community structure of a pesticide-contaminated site and assessment ofchanges induced in community structure during bioremediation. FEMS Microbiol Ecol 2006;57:116-27. http://dx.doi.org/10.1111/j.1574-6941.2006.00103.x.         [ Links ]

72. Mohammadi A, Nasernejad B. Enzymatic degradation of anthracene by the white rot fungus Phanerochaete chrysosporium immobilized on sugarcane bagasse. J Hazard Mater 2009;161:534-7. http://dx.doi.org/10.1016/jjhazmat.2008.03.132.         [ Links ]

73. Gouda MK, Omar SH, Chekroud ZA, Eldin HMN. Bioremediation of kerosene I: A case study in liquid media. Chemosphere 2007;69:1807-14. http: //dx.doi.org/10.1016/j.chemosphere.2007.05.079.         [ Links ]

74. Cubitto MA, Gentili AR. Bioremediation of crude oil - Contaminated soil by immobilized bacteria on an agroindustrial waste - Sunflower seed husks. Biorem J 2015;19:277-86. http://dx.doi.org/10.1080/10889868.2014.995376.         [ Links ]

75. Wang JY, De Belie N, Verstraete W. Diatomaceous earth as a protective vehicle for bacteria applied for self-healing concrete. J Ind Microbiol Biotechnol 2012;39: 567-77. http://dx.doi.org/10.1007/s10295-011-1037-1.         [ Links ]

76. Yang Y, Hu H, Wang G, Li Z, Wang B, Jia X, et al. Removal of malachite green from aqueous solution by immobilized Pseudomonas sp. DY1 with Aspergillus oryzae. Int Biodeter Biodegr 2011;65:429-34. http://dx.doi.org/10.1016/j.ibiod.2011.01.007.         [ Links ]

77. Paliwal R, Uniyal S, Rai JPN. Evaluating the potential ofimmobilized bacterial consortium for black liquor biodegradation. Environ Sci Pollut Res 2015;22:6842-53. http://dx.doi.org/10.1007/s11356-014-3872-x.         [ Links ]

78. tawniczak t, Kaczorek E, Olszanowski A. The influence of cell immobilization by biofilm forming on the biodegradation capabilities of bacterial consortia. World J Microbiol Biotechnol 2011;27:1183-8. http://dx.doi.org/10.1007/s11274-010-0566-5.         [ Links ]

79. Banerjee S, Khatoon H, Shariff M, Yusoff FM. Immobilized periphytic cyanobacteria for removal of nitrogenous compounds and phosphorus from shrimp farm waste- water. Turk J Biol 2015;39:388-95. http://dx.doi.org/10.3906/biy-1407-26.         [ Links ]

80. Li P, Wang X, Stagnitti F, Li L, Gong Z, Zhang H, et al. Degradation of phenanthrene and pyrene in soil slurry reactors with immobilized bacteria Zoogloea sp. Environ Eng Sci 2005;22:390-9. http://dx.doi.org/10.1089/ees.2005.22.390.         [ Links ]

81. Li Y, Gao F, Wei W, Qu JB, Ma GH, Zhou WQ. Pore size of macroporous polystyrene microspheres affects lipase immobilization. J Mol Catal B: Enzym 2010;66:182-9. http://dx.doi.org/10.1016/j.molcatb.2010.05.007.         [ Links ]

82. Lin J, Gan L, Chen Z, Naidu R. Biodegradation of tetradecane using Acinetobacter venetianus immobilized on bagasse. Biochem Eng J 2015;100:76-82. http://dx.doi.org/10.1016/j.bej.2015.04.014.         [ Links ]

83. Quek E, Ting YP, Tan HM. Rhodococcus sp. F92 immobilized on polyurethane foam shows ability to degrade various petroleum products. Bioresour Technol 2006;97: 32-8. http://dx.doi.org/10.1016/j.biortech.2005.02.031.         [ Links ]

84. Nicolucci C, Rossi S, Menale C, Godjevargova T, Ivanov Y, Bianco M, et al. Biodegradation ofbisphenols with immobilized laccase or tyrosinase on polyacrylonitrile beads. Biodegradation 2011;22:673-83. http://dx.doi.org/10.1007/s10532-010-9440-2.         [ Links ]

85. Siripattanakul S, Wirojanagud W, McEvoy JM, Casey FX, Khan E. Atrazine removal in agricultural infiltrate by bioaugmented polyvinyl alcohol immobilized and free Agrobacterium radiobacter J14a: A sand column study. Chemosphere 2009;74: 308-13. http://dxdoi.org/10.1016/j.chemosphere.2008.09.005.         [ Links ]

86. Siripattanakul S, Wirojanagud W, McEvoy J, Khan E. Effect of cell-to-matrix ratio in polyvinyl alcohol immobilized pure and mixed cultures on atrazine degradation. Water Air Soil Pollut Focus 2008;8:257-66. http://dx.doi.org/10.1007/s11267-007-9158-2.         [ Links ]

87. Yujian W, Xiaojuan Y, Hongyu L, Wei T. Immobilization of Acidithiobacillus ferrooxidans with complex of PVA and sodium alginate. Polym Degrad Stab 2006; 91:2408-14. http://dx.doi.org/10.1016/j.polymdegradstab.2006.03.015.         [ Links ]

88. Daumann LJ, Larrabee JA, Ollis D, Schenk G, Gahan LR. Immobilization of the enzyme GpdQ on magnetite nanoparticles for organophosphate pesticide bioreme- diation. J Inorg Biochem 2014;131:1-7. http://dx.doi.org/10.1016/jjinorgbio.2013.10.007.         [ Links ]

89. Lyew D, Guiot SR, Monot F, Fayolle-Guichard F Comparison of different support materials for their capacity to immobilize Mycobacterium austroafricanum IFP 2012 and to adsorb MtBE. Enzyme Microb Technol 2007;40:1524-30. http://dx.doi.org/10.1016/j.enzmictec.2006.10.040.         [ Links ]

90. Su D, Li PJ, Frank S, Xiong XZ. Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite. J Environ Sci 2006;18: 1204-9. http://dxdoi.org/10.1016/S1001-0742(06)60063-6.         [ Links ]

91. Salis A, Pisano M, Monduzzi M, Solinas V, Sanjust E. Laccase from Pleurotus sajor-caju on functionalised SBA-15 mesoporous silica: Immobilisation and use for the oxidation ofphenolic compounds. J Mol Catal B: Enzym 2009;58:175-80. http://dx.doi.org/10.1016/j.molcatb.2008.12.008.         [ Links ]

92. Compart LCA, Machado KMG, Matheus DR Cardoso AV. Immobilization of Psilocybe castanella on ceramic (slate) supports and its potential for soil bioremediation. World J Microbiol Biotechnol 2007;23:1479-83. http://dx.doi.org/10.1007/s11274-007-9393-8.         [ Links ]

93. Yunoki A, Tsuchiya E, Fukui Y, Fujii A, Maruyama T. Preparation of inorganic/ organic polymer hybrid microcapsules with high encapsulation efficiency by 36 A. Dzionek et al. / Electronic Jouran electrospray technique. ACS Appl Mater Interfaces 2014;6:11973-9. http://dx.doi.org/10.1021/am503030c.         [ Links ]

94. Bhatnagar Y, Singh GB, Mathur A, Srivastava S, Gupta S, Gupta N. Biodegradation of carbazole by Pseudomonas sp. GBS. 5 immobilized in polyvinyl alcohol beads. J Biochem Technol 2015;6:1003-7. http://www.jbiochemtech.com/index.php/jbt/article/viewFile/JBT638/pdf.         [ Links ]

95. Angelim AL, Costa SP, Farias BCS, Aquino LF, Melo VMM. An innovative bioremediation strategy using a bacterial consortium entrapped in chitosan beads. J Environ Manage 2013;127:10-7. http://dx.doi.org/10.1016/j.jenvman.2013.04.014.         [ Links ]

96. Carabajal M, Perullini M, Jobbágy M, Ullrich R, Hofrichter M, Levin L. Removal of phenol by immobilization of Trametes versicolor in silica-alginate-fungus biocomposites and loofa sponge. Clean Soil Air Water 2015;44:180-8.http://dx.doi.org/10.1002/clen.201400366.         [ Links ]

97. Leilei Z, Mingxin H, Suiyi Z. Biodegradation of p-nitrophenol by immobilized Rhodococcus sp. strain Y-1. Chem Biochem Eng Q 2012;26:137-44. http://hrcak.srce.hr/83969.         [ Links ]

98. Labana S, Pandey G, Paul D, Sharma NK, Basu A, Jain RK. Pot and field studies on bioremediation of p-nitrophenol contaminated soil using Arthrobacter protophormiae RKJ100. Environ Sci Technol 2005;39:3330-7.http://dx.doi.org/10.1021/es0489801.         [ Links ]

99. Liu J, Chen S, Ding J, Xiao Y, Han H, Zhong G. Sugarcane bagasse as support for immobilization of Bacillus pumilus HZ-2 and its use in bioremediation of mesotrione-contaminated soils. Appl Microbiol Biotechnol 2015;99:10839-51.http://dx.doi.org/m1007/s00253-015-6935-0.         [ Links ]

100. Basak B, Bhunia B, Dey A. Studies on the potential use of sugarcane bagasse as carrier matrix for immobilization of Candida tropicalis PHB5 for phenol biodegradation. Int Biodeter Biodegr 2014;93:107-17.http://dxdoi.org/10.1016/jjbiod.2014.05.012.         [ Links ]

101. Hazaimeh M, Mutalib SA, Abdullah PS, Kee WK, Surif S. Enhanced crude oil hydrocarbon degradation by self-immobilized bacterial consortium culture on sawdust and oil palm empty fruit bunch. Ann Microbiol 2014;64:1769-77. http://dx.doi.org/10.1007/s13213-014-0821-3.         [ Links ]

102. Yáñez-Ocampo G, Sánchez-Salinas E, Ortiz-Hernández ML. Removal of methyl parathion and tetrachlorvinphos by a bacterial consortium immobilized on tezontle-packed up-flow reactor. Biodegradation 2011;22:1203-13. http://dx.doi.org/m1007/s10532-011-9475-z.         [ Links ]

103. Yáñez-Ocampo G, Sanchez-Salinas E, Jimenez-Tobon GA, Penninckx M, Ortiz- Hernández ML. Removal of two organophosphate pesticides by a bacterial consortium immobilized in alginate or tezontle. J Hazard Mater 2009;168: 1554-61. http://dx.doi.org/10.1016/jjhazmat.2009.03.047.         [ Links ]

104. Iqbal M, Saeed A, Edyvean RGJ, O'Sullivan B, Styring P. Production of fungal biomass immobilized loofa sponge (FBILS)-discs for the removal of heavy metal ions and chlorinated compounds from aqueous solution. Biotechnol Lett 2005;27:1319-23. http://dx.doi.org/m1007/s10529-005-0477-y.         [ Links ]

105. Mazmanci MA, Onyayar A. Decolonisation of reactive black 5 by Funalia trogiiimmobilised on Luffa cylindrica sponge. Process Biochem 2005;40:337-42. http://dx.doi.org/10.1016/j.procbio.2004.01.007.         [ Links ]

106. Lin M, Liu Y, Chen W, Wang H, Hu X. Use of bacteria-immobilized cotton fibers to absorb and degrade crude oil. Int Biodeter Biodegr 2014;88:8-12.http://dx.doi.org/m1016/j.ibiod.2013.11.015.         [ Links ]

107. Podorozhko EA, Lozinsky VI, Ivshina IB, Kuyukina MS, Krivorutchko AB, Philp JC, et al. Hydrophobised sawdust as a carrier for immobilisation of the hydrocarbon-oxidizing bacterium Rhodococcus ruber. Bioresour Technol 2008;99:2001-8. http://dx.doi.org/10.1016/j.biortech.2007.03.024.         [ Links ]

108. Mishra S, Jyot J, Kuhad RC, Lal B. Evaluation ofinoculum addition to stimulate in situ bioremediation of oily-sludge-contaminated soil. Appl Environ Microbiol 2001;67:1675-81. http://dx.doi.org/m1128/AEM.67A1675-1681.2001.         [ Links ]

109. Plangklang P, Reungsang A. Biodegradation of carbofuran in sequencing batch reactor augmented with immobilised Burkholderia cepacia PCL3 on corncob. Chem Ecol 2013;29:44-57. http://dx.doi.org/10.1080/02757540.2012.686609.         [ Links ]

110. Liu SJ, Jiang B, Huang GQ, Li XG. Laboratory column study for remediation of MTBE- contaminated groundwater using a biological two-layer permeable barrier. Water Res 2006;40:3401-8. http://dx.doi.org/10.1016/jwatres.2006.07.015.         [ Links ]

111. Paca J, Koutsky B, Maryska M, Halecky M. Styrene degradation along the bed height of perlite biofilter. J Chem Technol Biotechnol 2001; 76:873-8. http://dx.doi.org/10.1002/jctb.461.         [ Links ]

112. Emtiazi G, Shakarami H, Nahvi I, Mirdamadian SH. Utilization of petroleum hydrocarbons by Pseudomonas sp. and transformed Escherichia coli. Afr J Biotechnol 2005; 4:172-6. https://tspace.library.utoronto.ca/bitstream/1807/6609/1/jb05032.pdf.         [ Links ]

113. Santacruz G, Bandala ER Torres LG. Chlorinated pesticides (2,4-D and DDT) biodegradation at high concentrations using immobilized Pseudomonas fluorescens. J Environ Sci Health Part B 2005;40:571-83. http://dx.doi.org/10.1081 /PFC-200061545.         [ Links ]

114. Abdel-Razek MARS, Folch-Mallol JL, Perezgasga-Ciscomani L, Sánchez-Salinas E, Castrejón-Godínez ML, Ortiz-Hernández ML. Optimization of methyl parathion biodegradation and detoxification by cells in suspension or immobilized on tezontle expressing the opd gene. J Environ Sci Health Part B 2013;48:449-61. http://dx.doi.org/10.1080/03601234.2013.761863.         [ Links ]

115. Nunal SN, Santander-De Leon SMS, Bacolod E, Koyama J, Uno S, Hidaka M, et al. Bioremediation of heavily oil-polluted seawater by a bacterial consortium immobilized in cocopeat and rice hull powder. Biocontrol Sci 2014;19:11-22. http://dx.doi.org/10.4265/bio.19.11.         [ Links ]

116. Partovinia A, Naeimpoor F. Phenanthrene biodegradation by immobilized microbial consortium in polyvinyl alcohol cryogel beads. Int Biodeter Biodegr 2013;85: 337-44. http://dx.doi.org/10.1016/j.ibiod.2013.08.017.         [ Links ]

117. Kuyukina MS, Ivshina IB, Serebrennikova MK, Krivorutchko AB, Podorozhko EA, Ivanov RV, et al. Petroleum-contaminated water treatment in a fluidized-bed bio-reactor with immobilized Rhodococcus cells. Int Biodeter Biodegr 2009;63:427-32.http://dx.doi.org/10.1016/jjbiod.2008.12.001.         [ Links ]

118. Mulla SI, Bangeppagari M, Mahadevan GD, Eqani SAMAS, Sajjan DB, Tallur PN, et al. Biodegradation of 3-chlorobenzoate and 3-hydroxybenzoate by polyurethane foam immobilized cells of Bacillus sp. OS13. J Environ Chem Eng 2016;4:1423-31. http://dx.doi.org/10.1016/jjece.2016.02.027.         [ Links ]

119. Usha MS, Sanjay MK, Gaddad SM, Shivannavar CT. Degradation of h-acid by free and immobilized cells ofAlcaligenes latus.Braz J Microbiol 2010;41:931-45. http://dx.doi.org/10.1590/S1517-83822010000400012.         [ Links ]

120. Phisalaphong M, Budiraharjo R Bangrak P, Mongkolkajit J, Limtong S. Alginate-loofa as carrier matrix for ethanol production. J Biosci Bioeng 2007;104:214-7. http://dx.doi.org/10.1263/jbb.104.214.         [ Links ]

121. Abdeen Z, El-Sheshtawy Hk, Moustafa YMM. Enhancement of crude oil biodegra-dation by immobilizing of different bacterial strains on porous PVA hydrogels or combining of them with their produced biosurfactants. J Pet Environ Biotechnol 2014;5:1 -10. http://dx.doi.org/10.4172/2157-7463.1000192.         [ Links ]

122. Maliji D, Olama Z, Holail H. Environmental studies on the microbial degradation of oil hydrocarbons and its application in Lebanese oil polluted coastal and marine ecosystem. Int J Curr Microbiol App Sci 2013;2:1-18. http://www.ijcmas.com/vol-2-6/Darin%20Maliji,%20Zakia%20Olama%20and%20Hanafy%20HolaiLpdf.         [ Links ]

123. Ahmad WHW, Chyan JB, Zakaria ZA, Ahmad WA Sugarcane bagasse as nutrient and support material for Cr (VI)-reducing biofilm. Int Biodeter Biodegr 2015;102: 3-10. http://dx.doi.org/10.1016/j.ibiod.2015.03.007.         [ Links ]

124. Ahmad WA, Zakaria ZA, Razali F, Samin J. Evaluation of the combined Cr(VI) removal capacity of sawdust and sawdust-immobilized Acinetobacter haemolyticus supplied with brown sugar. Water Air Soil Pollut 2009;204:195-203.http://dx.doi.org/m1007/s11270-009-0037-5.         [ Links ]

125. Plangklang P, Reungsang A. Bioaugmentation of carbofuran by Burkholderia cepacia PCL3 in a bioslurry phase sequencing batch reactor. Process Biochem 2010;45: 230-8. http://dx.doi.org/10.1016/j.procbio.2009.09.013.         [ Links ]

126. Velasco-Alvarez N, González I, Damian-Matsumura P, Gutiérrez-Rojas M. Enhanced hexadecane degradation and low biomass production by Aspergillus niger exposed to an electric current in a model system. Bioresour Technol 2011;102:1509-15.http://dx.doi.org/10.1016/j.biortech.2010.07.111.         [ Links ]

127. Cobos-Vasconcelos D, Ruiz-Ordaz N, Galíndez-Mayer J, Poggi-Varaldo H, Juàrez-Ramírez C, Aarón LM. Aerobic biodegradation of a mixture of sulfonated azo dyes by a bacterial consortium immobilized in a two-stage sparged packed-bed biofilm reactor. Eng Life Sci 2012;12:39-48. http://dx.doi.org/10.1002/elsc.201000227.         [ Links ]

128. Herrera-González VE, Ruiz-Ordaz N, Galíndez-Mayer J, Juárez-Ramírez C, Santoyo-Tepole F, Montiel EM. Biodegradation of the herbicide propanil, and its 3,4-dichloroaniline by-product in a continuously operated biofilm reactor. World J Microbiol Biotechnol 2013;29:467-74. http://dx.doi.org/10.1007/s11274-012-1200-5.         [ Links ]

129. Deng F, Liao C, Yang C, Guo C, Ma L, Dang Z. A new approach for pyrene bioreme-diation using bacteria immobilized in layer-by-layer assembled microcapsules: Dynamics ofsoil bacterial community. RSC Adv 2016;6:20654-63.http://dx.doi.org/10.1039/C5RA23273B.         [ Links ]

130. Eroglu E, Agarwal V, Bradshaw M, Chen X, Smith SM, Raston CL, et al. Nitrate removal from liquid effluents using microalgae immobilized on chitosan nanofiber mats. Green Chem 2012;14:2682-5. http://dx.doi.org/10.1039/C2GC35970G.         [ Links ]

131. Wang ZY, Xu Y, Wang HY, Zhao J, Gao DM, Li FM, et al. Biodegradation of crude oil in contaminated soils by free and immobilized microorganisms. Pedosphere 2012; 22:717-25. http://dx.doi.org/10.1016/S1002-0160(12)60057-5.         [ Links ]

132. Mehta PK, Ghose TK, Mishra S. Methanol biosynthesis by covalently immobilized cells of Methylosinus trichosporium: Batch and continuous studies. Biotechnol Bioeng 1991;37:551-6. http://dx.doi.org/10.1002/bit.260370609.         [ Links ]

 


Article history: Received 5 April 2016 Accepted 27 July 2016 Available online 12 August 2016

* Corresponding author. E-mail address: urszula.guzik@us.edu.pl (U. Guzik).

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