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Chapter 3
Biological Degradation of Plastics: Polyethylene Biodegradation by Aspergillus and Streptomyces Species—A Review Antony Rojas-Parrales,1 Tatiana Orantes-Sibaja,1 Carlos Redondo-Gómez,2 and José Vega-Baudrit*,1,2 1Facultad
de Ciencias Exactas y Naturales, Escuela de Química, Universidad Nacional, Heredia, 86-3000 Costa Rica 2Laboratorio Nacional de Nanotecnología LANOTEC-CeNAT, Centro Nacional de Alta Tecnología (CeNAT), San José, 1174-1200 Costa Rica *E-mail:
[email protected].
Plastic contamination threatens a wide variety of ecosystems, and presents damaging repercussions and negative consequences to many wildlife species. The problem of plastic contamination requires an innovative solution, one that avoids creating further adverse environmental impacts. Thus, the production of biodegradable plastic, in combination with the use of microorganisms for its consequent degradation, could be an alternative way to treat this problem. This chapter comprehensively reviews the biological degradation of synthetic plastics, such as polyethylene, and the use of the Aspergillus and Streptomyces species to degrade this polymer and its various structures, which represent some of the most typical residuals in the environment.
Introduction Plastic contamination treatment has become a priority due to its adverse impact on the environment. It is estimated that approximately 140 million tons of synthetic polymers are produced each year; and several studies have investigated the global impact of plastic contamination and its interactions with organisms at
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several trophic levels (1). In fact, 34 million tons of plastic waste are generated globally each year, 93% of which is disposed of in landfills and oceans (2). This excessive production of petroleum-based plastics demands sustainable alternatives from renewable resources. Moreover, the adverse environmental impacts—including carbon dioxide (CO2) emissions and their long-period accumulation in the environment due to their non-biodegradability—are significant drawbacks of non-biodegradable plastics (3). All these materials have contributred to a growing concern because of their persistence in the environment, which adversely affects wildlife and changes the appearance of forests, cities, and even protected areas. Plastics are man-made long chain polymer molecules (4), and polyethylene (PE) is one of the most abundant commercially produced synthetic polymers (5). PE represents 64% of the synthetic plastics produced, and is mainly used for manufacturing plastic bags, bottles, and disposable containers, which are discarded within a short time (6). Over time, the stability and durability of plastics have been continuously improved, mainly in the area of resistance to different environmental influences, strength, and lightness, among other mechanical and thermal properties. The plastics we use today are made from organic and inorganic raw materials, such as carbon silicon, hydrogen, nitrogen, oxygen, and chloride. These materials are extracted from oil, coal, and natural gas (7). The most commonly used plastics are the aforementioned low-density polyethylene (LDPE), medium-density polyethylene (MDPE), high-density polyethylene (HDPE) and linear low-density polyethylene (LLDPE), polypropylene (PP), polystyrene (PS), polyvinyl chloride (PVC), polyurethane (PUR), polyethylene terephthalate (PET),polybutylene terephthalate (PBT), and nylon (8), as shown in Table 1. However, everyday plastics are resistant against microbial attack; as owing to their only recent presence in nature, evolution has yet to yield new enzyme structures capable of degrading these types of polymers (9). Scientists are trying to find mechanisms to make these plastics decompose more easily and to decrease their degradation time (from centuries to decades or even years). Toward this goal, plastics have been modified so they become more susceptible to microbial attack, creating bioplastics. There is an urgent need to develop efficient microorganisms and their products to solve this global issue (10). Although there are other ways to degrade plastics, such as photodegradation, thermal degradation, and oxodegradation, the use of microorganisms provides an ecological and effortless alternative to reduce the accumulation of plastic materials in the natural environment. A certain strain of microorganisms, such as bacteria and fungi, has shown the ability to degrade polymers through the use of enzymes; however, the activity of these microorganisms depends on the chemical structure of the polymers. Degradable plastics allow some species of Streptomyces the development of lignocellulose-degrading enzymes; the potential of these microorganisms can be used to reduce the contamination of these synthetic products.
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Table 1. Different Uses of Common Synthetic Plasticsa
a
Plastic
Use
Polyethylene (PE)
Plastic bags, milk and water bottles, food packaging film, toys, irrigation and drainage pipes, motor oil bottles
Polystyrene
Disposable cups, packaging materials, laboratory ware, certain electronic uses
Polyurethane
Tires, gaskets, bumpers, in refrigerator insulation, sponges, furniture cushioning, and life jackets
Polyvinyl chloride
Automobile seat covers, shower curtains, raincoats, bottles, visors, shoe soles, garden hoses, and electrical pipes
Polypropylene
Bottle caps, drinking straws, medicine bottles, car seats, car batteries, bumpers, disposable syringes, carpet backings
Polyethylene terephthalate (PET)
Carbonated soft drink bottles, processed meat packages, peanut butter jars, pillow and sleeping bag filling, textile fibers
Nylon
Small bearings, speedometer gears, windshield wipers, water hose nozzles, football helmets, racehorse shoes, inks, clothing, parachute fabrics, rainwear, and cellophane
Polycarbonate
Lenses in eyeglasses, making nozzles on paper-making machinery, street lighting, safety visors, rear lights of cars, baby bottles, and houseware. It is also used in skylights and the roofs of greenhouses, sunrooms, and verandahs
Polytetrafluoro- ethylene (PTFE)
Industrial applications such as specialized chemical plants, electronics, and bearings. Household uses include as a coating on non-stick kitchen utensils, in saucepans, and frying pans
Modified from (8).
Bioplastics We can refer to the word bioplastic as a bio-based polymer synthesized from biomass and renewable resources, such as polylactic acid (PLA) and polyhydroxyalkanoate (PHA) or plastics produced from fossil fuel, including aliphatic plastics, such as polybutylene succinate (PBS), which can also be utilized as a substrate by microorganisms (11, 12). Bioplastics will decompose in the natural environment. These biopolymers are considered to be friendly materials or “green” plastics, but high production cost and poor mechanical and thermal properties represent inconvenient factors for their creation. Nonetheless, renewable resources, such as agricultural and some industrial wastes, can be used to reduce monetary expense. Bioplastics based on starch use the benefits of natural polymerization and the availability of raw material and process technology (13). The use of these materials has resulted in a lower consumption of non-renewable energy sources (-50%) and, therefore, lower greenhouse gas emissions (-60%) (14). 71
Scientists have developed sustainable and green engineering to reduce energy and natural resource consumption. The goal of green engineering is to minimize adverse impact while simultaneously maximizing benefits to the economy, society, and the environment (15).
Biodegradation of Plastics The term biodegradation involves, above all, biological activity (16), and can be defined as an irreversible change in the chemical structure of a plastic involving a deleterious change in properties (17). Degradation is strongly related to changes in mechanical, optical, or electrical characteristics, as well as crazing, cracking, erosion, discoloration, phase separation, or delamination (14). Any of these will provide bond scission, chemical transformation, and a generation of new functional groups in the structure of the polymer. Microorganisms, such as bacteria and fungi, are involved in the biodegradation of both natural and synthetic plastics (18), in the same way as many aerobes, anaerobes, photosynthetic bacteria, archaebacteria, and lower eukaryotes. All of these microorganisms can be found widely spread in compost and soil materials, and some are present in aquatic environments. The process of degradation is affected by many factors. For example, plastics present in surface waters are more prone to degradation compared to those on the seafloor, for which decomposition takes longer due to the cold water temperature and reduced sunlight penetration (19). Location of plastic waste, temperature, pH, light (UV), moisture content, polymer characteristics (such as chemical structure, polymer chains, crystallinity, mobility, tacticity, molecular weight, and functional groups), type of organism, and the environment status are essential factors for successful microorganisms’ growth and need to be considered. Biodegradation consists of three important steps (20): biodeterioration, biofragmentation, and assimilation, which are explained as follows:
1.
2.
3.
Biodeterioration: This phase consists of modifying mechanical, chemical, and physical properties of the plastic due to the growth of microorganisms on or inside the surface of the material. Biofragmentation: Microbial activity on the polymer surface starts to turn the large chain molecules into smaller ones (oligomers and monomers), as these structures cannot pass through cellular membranes. Assimilation: Via microorganism metabolism, polymer pieces are absorbed within microbial cells, so the carbon from the plastic is transformed into carbon dioxide or methane, water, and biomass, in exchange of energy and nutrient sources due to the previous fragmentation of the polymer. This is also called mineralization. 72
To increase the rate of degradation, plastics must be degraded more rapidly than conventional disposable plastics; this can be done through the use of compounds, such as starch, used in some microorganism metabolism. Starch guarantees at least partial biodegradation due to changes in the mechanical and rheological behavior of the polymer. It is important to remember that biodegradation serves as an innovative and effective approach to waste management as compared to land-filling and burning processes (20), because microorganisms use intracellular and extracellular enzymes, which are the ones responsible for enzymatic degradation of bioplastics. Many enzymes are involved in plastic degradation, and plastics components are important in order to choose which strain and their enzymes are adequate for each degrading process.
PE and Its Biodegradation In its simplest form, a PE molecule consists of a long backbone of an even number of covalently linked carbon atoms with a pair of hydrogen atoms attached to each carbon, and methyl groups as chain ends (21). This structure is shown in Figure 1. Usually, the degree of polymerization for being a plastic is well in excess of 100 and can be as high as 250,000 or more carbon atoms, which indicates a varying molecular weight between 1400 and 3,500,000 (or more).
Figure 1. Chemical structure of pure polyethylene. The type of PE depends on the different branches that change the nature of the compound. Generally, the higher the concentration of branches, the lower the density of the solid. This leads to having the following classes of PE: HDPE, LDPE, linear low density polyethylene (LLDPE), very low density polyethylene (VLDPE or ULDPE), cross-linked polyethylene (XLPE), and others. Nowadays, we can unquestionably consider PE as the most utilized synthetic polymerin human applications. PE biodegradation is not a trivial process, since the polymer is extremely resistant to microbial attack (22, 23). Its high level of hydrophobicity and molecular weight leads to a non-biodegradable plastic that causes many dangerous environmental problems (24). Several studies have reported that PE biodegradation is possible after abiotic pretreatment (chemical, thermal, and/or photooxidation), which decreases its hydrophobicity and molecular weight to facilitate biotic degradation (25). Therefore, a reduction in the molecular weight, crystallinity, and certain mechanical properties of plastics can improve the polymer biodegradability, because low molecular weights make them more soluble in water and increase the wettability of the film surface, which favors the attack by hydrolytic enzymes, and the formation of the enzyme-substrate complex. Although microorganisms 73
are only able to attack molecules between 10 to 50 carbons, reports have shown enzymatic activity up to 2000 carbons (26). LDPE is more commonly used for packaging, as it possesses most of the characteristics of an ideal packaging material (foods, milk, agricultural products, shrink-wrapping, electronic goods, vehicles, and so on) (27). It is known that microorganisms decompose LDPE easily because its level of crystallinity is lower compared to HDPE, making it more susceptible to microorganisms. Seven different characteristics are usually monitored for change in order to establish the extent of biodegradation of the polymer: functional groups on the surface, hydrophobicity/hydrophilicity, crystallinity, surface topography, mechanical properties, molecular weight distribution, and mass balance (28). All of these show evidence of interactions by microorganisms with the material surface. Over the past 50 years, some strains have been identified as having abilities on PE biodegradation, causing some kind of deterioration. The richness of microorganisms able to degrade PE is so far limited to 17 genera of bacteria and nine genera of fungi; however, these numbers are likely to increase based on the more sensitive isolation and characterization techniques based on sequencing of rDNA (29). The number of organisms that can utilize PE is not that low. In fact, among the reported microorganisms capable of degrading PE are the following fungi: Aspergillus niger, Aspergillus flavus, Aspergillus oryzae, Chaetomium globusum, Penicillium funiculosum, and Pullularia pullulan. As for bacteria, the list includes Pseudomonas aeruginosa, Bacillus cereus, Coryneformes bacterium, Bacillus sp., Mycobacterium, Nocardia, Corynebacterium, Candida, Pseudomonas, and Actinomycetales (Streptomycetaceae) (30). In a later section, this review will focus on some advances made with Aspergillus and Streptomyces species. Biodegradation of PE is known to occur by two mechanisms: hydrobiodegradation and oxobiodegradation (31). Both mechanisms work with additives. Hydrophilic supplements, such as starch, cellulose, or proteins, significantly reduce the level of some mechanical properties, making PE more hydrophilic; therefore, degradation is catalyzed by different enzymes secreted by fungi or bacteria. The application of these additives will increase the surface area of the synthetic bulk material, rendering it more susceptible to abiotic oxidation (32). On the other hand, oxidizing agents allow chemical- and photodegradation, increasing the probability of obtaining more oligomers and monomers useful for these microorganisms. These agents are called prooxidants, which can be various complexes of transition metals, particularly Fe, Co, and Mn, which increase the rate of oxidation by air oxygen and cleavage of PE chains under the influence of light and/or heat (33) as they are a source for reaction initiation radicals, rendering the polymer apparently more susceptible to biodegradation. Microorganisms, such as Bacillus subtilis, tend to produce biosurfactants that enhance the degradation process of PE. Biosurfactants are surface-active compounds synthesized by a wide variety of microorganisms. They are molecules that have both hydrophobic and hydrophilic domains, comprising an acid, peptide cations, or anions, mono-, di-, or polysaccharides, and a hydrophobic moiety of 74
unsaturated or saturated hydrocarbon chains or fatty acids (34). These compounds have been demonstrated to increase surface area and water availability, and to change properties of the bacterial cell membrane, which strengthens the attachment of bacteria on hydrophobic surfaces, such as PE plastics. Another possible factor in the mechanism of PE biodegradation has been reported for microorganisms such as Pseudomonas, Candida, and Norcardia; as PE is considered as one of n-alkanes, it should be subjected to carboxylation via one of these oxidative pathways. PE molecules carboxylated via these metabolic processes become structurally analogous to fatty acid, and are subject to β-oxidation (35). In this way, PE long chains will decompose piece by piece (of two carbons) in every cycle due to enzymes in their cell machinery, while smaller molecules are directly consumed.
Aspergillus Species Degrading Activity Aspergillus species are greatly aerobic and are found in almost all oxygen-rich environments, where they commonly grow as mold on the surface of a substrate, due to high oxygen tension (36). Many species of this genus have been qualified to degrade plastics due to their enzymes, and PE is not an exception. Aspergillus niger is a well-known cosmopolitan fungus and has been detected in a broad range of habitats because it can colonize a wide variety of substrates, as it has a wide array of hydrolytic and oxidative enzymes involved in the breakdown of plant lignocelluloses (37), for example, catalases and proteases (38). Also, A. niger is a producer of cellulolytic and hemicellulolytic enzymes (39). LDPE degradation by Aspergillus niger and Aspergillus fumigatus has been shown by Esmaeli et al. (40). Some studies have confirmed that formation of biofilms of A. terreus and A. fumigatus was observed on the surface of LDPE (without additives) and was considered to be a result of the surface moistness (41). Similarly, A. terreus has participated in the degradation of modified and unmodified PE (42). Other Aspergillus species, such as A. tubingensis and A. flavus, have shown the highest degradation rate of HDPE without any pretreatment and pro-oxidant additives (43). This demonstrated that the higher cell surface hydrophobicity of these fungal strains means an improvement in microbial adherence. Enzyme production by A. tubingensis is based on esterases and lipases (44), which are useful in plastic biodegradation. A. flavus instead secretes enzymes as glucosidases (38). In addition, Maeda et al. conducted some research to develop a cost-effective biodegradable plastic recycling system using the filamentous fungus Aspergillus oryzae to recover hydrolysates (45). There are more Aspergillus species than can possibly participate in PE breakdown. Identified fungal strains, such as A. nidulans, A. candidus, A. versicolor, and A. glaucus, have exhibited colonization of PE bags (38), while A. awamori has been able to colonize LDPE films (46). However, no further studies have shown their actual ability in PE degradation. Several findings have corroborated the fact that fungi have better biodegradation efficiency than bacteria. 75
Streptomyces Species Degrading Activity The Streptomyces species is known for its ability as a lignocellulose degrader (47). Some studies have shown that Streptomyces sp. can carry through the production of extracellular enzymes to degrade PE (48). There is a lignin-induced extracellular peroxidase produced during lignocellulose degradation by S. viridosporus (49); these strains degrade both lignin and carbohydrate portions of lignocellulose (50). Due to these activities, plastics with lignin can be degraded, aiding in plastic removal. Also, genetically manipulated strains have been created with enhanced abilities to produce a water-soluble lignin degradation intermediate (49). There is currently great interest in lignin-degrading because of its industrial potential; some are recognized in biomechanical pulping (51). As previously mentioned, microbial activity on plastics takes place by an enzymatic action. Several authors propose that alkane monooxygenase is also responsible for the microbial attack on the surface of synthetic polymers (52). Many microorganisms can degrade n-alkanes, using them as a source of carbon and energy (53, 54). Among these, several Streptomyces n-alkane-degrader strains, belonging to the species S. griseoflavus, S. parvus, or S. plicatus, have been isolated from oil-polluted soils (55–57). Because of that, Streptomyces species are able to degrade plastics.
Determination of Plastics Degradation To determine the biodegradability of plastic materials after exposure with fungi or bacteria, the evaluation of weight, tensile strength, changes in percent elongation, and changes in molecular weight distribution are needed. Transmission electron microscopy (TEM) is a useful technique to determine the surface characteristics of degradable plastics, as is scanning electron microscopy (SEM), which is generally used to monitor changes in the surface of PE samples during the biodegradation process (41). Fourier transform infrared spectroscopy (FTIR) analysis of the products of degradation are, in many cases, contradictory, especially with regard to the relative intensities of different signals, suggesting that pathways are complex and may differ among organisms (58). Yamada-Onodera et al. observed that the distribution of molecular weights of the PE by HT-GPC and FTIR analysis was used for detection of functional groups in the PE (59). In investigations of environmental degradation of PE, FTIR analysis showed that the amount of carbonyl groups in PE increased with time in the abiotic environment, while the amount of carbonyl groups decreased in the biotic environment (60).
Conclusions Microbial use for plastic waste treatments is a potential tool to reduce the impact of these materials on the environment with no adverse results. Together with thermal- and photo-degradation, this process can be much more effective because microorganisms can only absorb PE molecules with a low molecular weight, making HDPE more susceptible. Biodegradable plastics accelerate 76
the process of degradation made by microorganisms compared with common plastics. Also, the use of hydrophilic additives and prooxidants in combination with microorganisms, such as fungi and bacteria, can dramatically reduce the molecular weight of PE from several hundred thousand to thousands or even hundreds. It has been shown that many strains of Aspergillus sp. can degrade PE due to their wide range of hydrolytic and oxidative enzymes. Moreover, fungi tend to result in better biodegradation efficiencies compared to those produced by bacteria. Nonetheless, Streptomyces strains can be used for plastic biodegradation because of their enzymes, being an option to reduce or treat plastic contamination. Techniques such as TEM, SEM, and FTIR have been successful to determine how much PE has biodegraded by studying surface characteristics and different functional groups that appear on plastic material after exposure to these microorganisms.
Acknowledgments The authors wish to thank Sergio A. Paniagua for proofreading the paper.
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