Plastics degradation by microbes: A sustainable approach

1 Introduction

From different hydrocarbons and petroleum derivatives high molecular weight organic polymers are obtained. These polymers are known as plastic (Ahmed et al., 2018). The word “plastic” derived from the Greek word “Plastikos”, that means which can be molded into different shapes. Plastics stated as the polymers which start moving on heating so can be casted into moulds (Kale et al., 2015). Generally, plastic materials are derived from petrochemicals except biodegradable bioplastic (Akmal et al., 2015; Getachew and Woldesenbet, 2016). Plastic consists of chloride, oxygen, hydrogen, carbon, silicon and nitrogen. Polyethylene consists of 64% of total plastic and its general formula is CnH2n (Kale et al., 2015).

For packaging and many other purposes like agricultural films formation, diaper packaging and fishing nets plastics are used. Plastics play an important part in every sector of economy all over the world. In highly growing areas i.e. agriculture, building and construction, health and consumer goods, plastics use ensures that they are in high demand and without plastics no one can do work. Plastics, the backbone of many industries, are used in manufacturing of various products that are used in our daily life i.e. defense materials, sanitary wares, tiles, plastic bottles, artificial leather and different other household items. Plastics are also used in packaging of food items, pharmaceuticals, detergents and cosmetics (Thakur, 2012; Piergiovanni and Limbo, 2016).

One of the rapidly growing fields in global industry is the production of synthetic plastics. Plastics are more superior than other materials due to their unique properties. These properties have been led to increase the plastic production scale to 20 folds since 1964 (Ellen MacArthur Foundation 2016), and production scale exceeds 300 million tons/year (Plastics Europe 2015) in 2015 it reached to 335 million tons (Plastics Europe 2017) (Urbanek et al., 2018). There are advantages and disadvantages of plastics. Plastics are strong, durable, and light weight. On the other hand, they are harmful to the natural environment, resistant to degradation and leading to environmental pollution. On our planet, plastics pose a serious threat by accumulating in large quantities (Ahmed et al., 2018; Yang et al., 2020; Al-Thawadi, 2020).

Plastics can be differentiated into degradable and non-degradable polymers on the basis of their chemical properties (Ghosh et al., 2013). Plastics that are obtained from renewable resources are biodegradable plastics. These are naturally degradable, as a source of cellulose, starch and algal material, an important component in plants, animals and algae. These polymers are also produced by microorganisms. Non-degradable plastics, typically known as synthetic plastics, are derived from petrochemicals and are higher in molecular weight due to the repetitions of small monomer units (Imre and Pukánszky, 2013).

During plastic degradation the generation of plastic particles with a size of < 5 mm are known as microplastics (MPs) which lead to potential ecotoxicological effects (Zhang et al., 2017; Chen et al., 2020a; 2020b; Wong et al., 2020). Fibrous MPs may be inhaled, may persist in the lung, and along with associated contaminants including dyes and plasticizers could lead to health effects like carcinogenicity and mutagenicity (Gasperi et al., 2018; Wong et al., 2020). Generally, it is accepted that plastic waste can permanently be eliminated through incineration. However, unburned material still exists in the bottom ash in the form of a solid residue from incinerators that can produce 360 to 102,000 microplastic particles per metric ton after incineration. This bottom ash is a potential source of MPs released into the environment (Yang et al., 2021). It is reported that plastic fragments in the <100 nm size range, referred to as nanoplastics (NPs), may also be formed in the aquatic environment and may cause potential health effects (Nolte et al., 2017; Revel et al., 2018).

Suman et al. (2020) reported that the histopathology analysis indicated the deformation of epithelial cells in the midgut region after both chronic and acute exposures at 1 and 100 mg/L, respectively to polystyrene microplastics. In another study, Chen et al. (2020a; 2020b) reported that redclaw crayfish (Cherax quadricarinatus) were exposed to different concentrations (0, 0.5, and 5 mg/L) of 200 nm-sized polystyrene microspheres for 21 days and the microplastics were distributed in the intestines and hepatopancreas after ingestion and inhibited the growth of Cherax quadricarinatus. Xiao et al. (2020) reported that freshwater microalgae, Euglena gracilis, exposed to 1 mg/L of polystyrene microplastics (PS-MPs) for 24 h. The vacuoles of microalgae were induced and pigment contents were reduced significantly (p < 0.05).

Plastics can be degraded in the environment by 4 mechanisms i.e. hydrolytic degradation, photodegradation, thermo-oxidative degradation and biodegradation (Webb et al., 2013). Plastics posed serious threats to our environment and their removal from the environment is imperative. The plastics that are degraded by microorganisms are known as biodegradable plastics and microorganisms can degrade them into H₂O and CO₂ (Nakajima-Kambe et al., 2009). The rate of biodegradation of polymers can be increased by using thermo-oxidant and photo-degrading agents (Mahdiyah and Mukti, 2013).

Free radicals cause rupturing of the chains by oxidizing the polymeric molecules. Many physical and chemical changes occur due to photo oxidation including reduction in polymers molecular weight and production of carbonyl groups. In thermal oxidation high temperature more than melting point is given which decreases the fusion heat and increases level of carbonyl group production. As a result, polymers are more liable to be degraded by microorganisms (Manzur et al., 2004). Phase separation, erosion, discoloration treatment types, cracking and types of polymers are the various factors that are responsible for the biodegradation and source of pollution in the environment (Thomas et al., 2015).

As most of the reviews are on fates of plastics/microplastics including transportation, toxicity, and risk assessment to humans with reference to terrestrial and marine ecosystems (Nolte et al., 2017; Revel et al., 2018; Chen et al., 2020a; 2020b; Wong et al., 2020). The present review describes plastic classification, plastic types, degradation types, biodegradation and mechanism of biodegradation. This review focuses on microbial degradation of plastic/microplastics which has received less attention as compared to the toxicity of plastic/microplastics in terrestrial and marine environments to eradicate plastic pollution from the ecosystem Geyer et al. (2017).

2 Plastic classification on the basis of thermal properties

On the basis of thermal properties plastics are divided into two classes, i.e. thermoplastics and thermosetting polymers. By the polymerization of small molecules, plastics can be synthesized.

3 Types of degradable plastic

Plastics that are easily degradable can be divided into four types: Photodegradable bioplastics, bio-based bioplastics, compostable bioplastics and biodegradable bioplastics.

4 Types of degradation

5 Biodegradation

In a material, any physical and chemical change that is caused by the action of microorganisms is known as biodegradation. Natural and synthetic plastics are degraded by the action of microorganisms including bacteria, actinomycetes, and fungi (Ishigaki et al., 2004; Alshehrei, 2017).

5.1

5.1 Aerobic biodegradation (aerobic respiration)

In this type of degradation, microorganisms break down large organic compounds into smaller compounds by using oxygen as an electron acceptor (Fig. 1). By-products of this process are carbon dioxide and water (Müller, 2005; Priyanka and Archana, 2011). Carbon plastic + Oxygen → carbon dioxide + water + Carbon residual

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Fig. 1

General mechanism of plastic degradation under aerobic conditions (Müller, 2005).

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6 Mechanism of biodegradation

Biodegradation of polymers consists of three steps; (a) microorganism attachment on the surface of polymer, (b) utilization of polymer as a source of carbon, and (c) polymer degradation. Microorganisms attach to the surface of polymers and degrade these polymers by secreting enzymes in order to obtain energy for their growth (Danso et al., 2018). Large polymers degraded into monomers and oligomers that are low molecular weight molecules. Some oligomers may be assimilated in the internal environment of microorganisms after diffusing inside them (Fig. 2).

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Fig. 2

Mechanism of enzymatic biodegradation of polymers (Alshehrei, 2017).

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7 Analytical procedures for biodegradation

A wide variety of methods is currently available for measuring the biodegradability of polymeric materials (Yang et al., 2005). Several test methods to assess the potential biodegradability of plastics have been developed by International Standard Organization (ISO) and American Society for Testing and Materials (ASTM) (Piergiovanni and Limbo, 2016) including gas chromatography/mass spectrometry (GC–MS), stereomicroscopy and micro-Fourier transform infrared spectroscopy (µ-FTIR) (Lomonaco et al., 2020; Corami et al., 2020). Biodegradation can be characterized with loss of weight, change in tensile strength, change in dimensions, change in chemical and physical properties, carbon dioxide production, bacterial activity in soil and change in molecular weight distribution (Kathiresan, 2003; Sivan, 2011; Kumar and Maiti, 2016; Chen et al., 2020a; 2020b).

8 Polymers degradation by microorganisms

Microbial polymers degradation includes biodeterioration, bio-fragmentation, mineralization, and assimilation.

8.4

8.4 Assimilation

In the assimilation process, atoms are integrated in the microbial cells for complete degradation. Secondary metabolites are transported outside the cells or transfer to other microbes that further perform degradation and use these metabolites (Fig. 3). The oxidized products i.e. CO₂, N₂, H₂O and CH₄ are released during metabolites degradation (Krzan et al., 2006; Lucas et al., 2008).

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Fig. 3

Schematic representation of plastic degradation (Krzan et al., 2006).

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9 Enzymatic degradation of plastics

Due to the absence of hydrolysable groups in the carbon–carbon backbone, the degradation of plastic by microbial enzymes is a very difficult task. The reduction of molecular weight is the first step that is achieved by the action of both biotic and abiotic factors. By UV light exposure, the carbonyl group of polymer is easily attacked by microbial enzymes (Leja and Lewandowicz, 2010; Novotný et al., 2018). For polymers degradation different enzymes are used e.g. laccase, manganese-dependent enzymes (lignin degrading enzymes), urease, lipase, and protease. Thermostable laccase can degrade the polyethylene (PE) in 48 h of incubation at 37 °C (Jaiswal et al., 2019).

10 Polyethylene degradation

Plastic is the most used material for food wrapping and is basically made of PE material (Agustien et al., 2016). Shopping bags are PE bags. These bags are composed of PE and 10% of the municipal waste, all over the world, is due to the excessive use of plastic material which is mainly PE (Begum et al., 2015). Usage of PE bags all around the globe is about 500 billion to one trillion annually. The plastic accumulation in the terrestrial environment or in the sea coast is about 25 million tons every year (Madhu et al., 2014).

PE is chemically inert and hydrophobic in nature and microorganisms have no appropriate mechanism to digest these synthetic plastics (Yoon et al., 2012). PE polymers are used by microorganisms as a substrate for their growth. Erosion, discoloration, cracking and phase separation are the indicators of PE degradation (Trivedi et al., 2016; Agustien et al., 2016).

PE degradation is further classified into two classes: abiotic and biotic. In abiotic degradation all natural factors like temperature, ultraviolet rays cause degradation of PE while in case of biotic degradation microorganisms are involved that consume the plastics by changing their properties (Sen and Raut, 2015). As PE is safe, cheap, harmless and stable in the environment, and is easy to proceed, it is one of the polymers that are mostly seen all over the world. The two possible ways by which PE usefulness is maintained in nature are to use microbes in order to degrade polymers or PE. The second is to make polymers artificially that are prone to degradation by microorganisms (Okoh and Atuanya, 2014).

Polyolefins, low density PE, are unreactive in their chemical nature. For a shorter period 95 °C is used while for a longer time it may be used at 80 °C (Billmeyer, 1984). Due to incomplete crystallinity that ranges in 50–60%, there are several properties of low-density polyethylene (LDPE) such as rigidity, tensile strength, flexibility and tear strength (Ferreira et al., 2005). The carbonyl group, generated in polyethylene oxidation, is used by microorganisms for its degradation (Cornell et al., 1984; Awasthi et al., 2017).

The oxidative degradation mechanism, used for non-hydrolysable polymers e.g. polyethylene and polypropylene, leads to loss in molecular weight of polymers. Several oxidative enzymes are involved in oxidation of ethylenic groups; these enzymes are monooxygenase, peroxidase, manganese, peroxidase, dehydrogenase and oxidase. By the action of extracellular and intracellular enzymes, polymers convert into oligomers and monomers that are utilized by microorganisms for a source of energy (Arkatkar et al., 2009). β-oxidation of fatty acids that occurs in animals and humans shows similarities with β-oxidation of polyethylene (Albertsson et al., 1987).

Microorganisms that are capable of degrading polymers have been investigated and isolated from the natural environment. Polymer materials that are used for microbial degradation e.g., polyethylene and polypropylene (Park and Kim, 2019). Polymer degrading microbial species that are associated with degradation were identified as Streptococcus, Klebsiella, Micrococcus Staphylococcus, Pseudomonas (Das and Kumar, 2015). Biodegradability of polyethylene is enhanced by blending polyethylene with different additives, by adding these additives auto-oxidation of polyethylene enhances, by which molecular weight of polymer reduces and microorganisms then easily degrade these low molecular weight polymers (Fig. 4).

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Fig. 4

Biodegradation of polyethylene. (1) Everyday use of plastic bags generates huge amounts of polymeric waste material. Shopping bags are made up of polymers of ethylene i.e., PE. (2) Certain microorganisms such as bacteria (e.g., Micrococcus sp., Staphylococcus sp.) and fungi (e.g., Mucor sp., Rhizopus sp.), produce extracellular PE degrading enzymes. (3) Depolymerases are one type of the polyethylene degrading enzymes, that can split the PE chain into macromere fragments (i.e., oligomers, dimers) which subsequently get converted into monomers i.e., ethylene. (4) Microorganisms could metabolize theses monomers (ethylene) through aerobic or anaerobic pathways and utilize them as a carbon and energy source. (5) Microorganisms utilize this energy to reproduce which results in an increase in microbial biomass.

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Skariyachan et al. (2017) reported that Bacillus vallismortis bt-dsce01 was able to degrade LDPE up to 75% after 120 d of incubation. Similarly, Muhonja et al. (2018) described that both Aspergillus oryzae strain A5 and B. cereus strain A5 were able to degrade LDPE 36.4 and 35.72%, respectively after 112 d of incubation. Taghavi et al. (2021) reported that fungus, Aspergillus flavus, was capable of breakdown 5.5% HDPE within 100 days. Maroof et al. (2021) described a new bacterial strain, B. siamensis, which has the ability to degrade 8.46% LDPE after 90 d of incubation (Table 1).

Various products are produced when polyethylene is subjected to thermo-photo oxidation. These products are ketone, aldehydes, carboxylic acids, alkanes alcohols, lactones, dicarboxylic acids and esters. Despite all these attempts, the microbial degradation of PE is still slow (Tokiwa et al., 2009; Jaiswal et al., 2020). High molecular weight of PE limitized its use as a substrate for many enzymatic reactions. There are two important reactions in the biodegradation process of PE; the first one is the loss in molecular weight and the second is oxidation.

There are two reasons behind molecular weight loss. The first reason is to make possible the molecule transport from outside into the cell through cell membrane and the second reason is to provide opportunity to the microbial enzymes to attack on the certain molecules in the cell carrying molecular weight usually in the range of 10–50 carbons. The enzymatic activity up to 2000 carbons has been reported in such degradation processes (Yoon et al., 2012). By the loss of molecular weight the size of molecule is reduced and after this oxidation is required to convert hydrocarbons into carboxylic acid.

Carboxylic acid is metabolized through β-oxidation and Krebs cycle (Restrepo-Flórez et al., 2014). The first one is to observe the microbial growth on the sample in order to check the adverse effect of polymer on microorganisms. The second one is to monitor the organism activity on polymer that causes loss in polymer integrity. Loss of integrity includes mechanical strength loss or may be reduction in average weight of molecules. In the abiotic system, there is no effect on polymers so only one system by which degradation is possible is the microbial degradation (Sudhakar et al., 2007). Polymers degradation by microbes can be assessed by using different methods. The measurement of weight reduction, tensile strength, film surface analysis by scanning electron microscopy (SEM), and carbonyl index can be ascertained through these methods. Microorganisms produce biosurfactants that help microbes to adhere to the surface of polymers and also help in the degradation of different products that are formed during oxidation (Das and Mukherjee, 2005).

Raaman et al. (2012) reported that fungal strains including Aspergillus niger and Aspergillus japonicus were evaluated for their ability to degrade LDPE and both strains were found able to degrade 8–12% PE after one month incubation. Munir et al. (2018) reported that out of 9 fungal isolates, two strains i.e., Trichoderma viride and Aspergillus nomius were used for PE film degradation. Both fungal strains were able to reduce the weight of LDPE film by 5.13% and 6.63% after 45 days of cultivation. The tensile strength of treated film was reduced significantly up to 58% and 40% by T. viride and A. nomius, respectively.

11 Biodegradable plastics types based on the mode of degradation pathway

The degradable plastics are further classified into two types based on the mode of degradation pathway. (a) Oxo-biodegradable plastics and (b) Hydro-biodegradable plastics (Mukamto et al., 2015; Vázquez-Morillas et al., 2016). The hydro-biodegradable plastics are those that are degraded through hydrolytic mechanisms (Nampoothiri et al., 2010). The examples of these plastics are cellulose, most general polyesters like polyhydroxyalkanoate (PHA), and starch. Oxo-degradation consists of two stages: the abiotic oxidation and biotic degradation (Fig. S2). In the first stage, the carbon backbone of polyolefins is oxidized abiotically into small fragments. This oxidative degradation is accelerated by thermal degradation and UV radiations but the degradation rate of the entire process is not determined exactly. In the second stage, degradation of polyolefin is taken by microbes (Liu et al, 2014; Nikolić et al., 2017; Montazer et al., 2018).

The PE polymer is changed due to addition of a carbonyl group in the polymer backbone and this change is achieved by abiotic photooxidation. Polyethylene molecule carrying carbonyl group is transformed to an alcohol in the presence of monooxygenase. The alcohol is oxidized to an aldehyde through alcohol dehydrogenase. Subsequently, aldehyde is converted into fatty acid by the action of aldehyde dehydrogenase. Finally, the fatty acid is metabolized through β-oxidation pathway (Fig. S3) (Gautam et al., 2007).

Microbes, colonized on the surface of PE, cause change in mechanical properties by increasing the roughness of PE surface, by increasing its fragility and by reduction in its molecular weight (Palmisano and Pettigrew, 1992; Watanabe et al., 2009; Nowak et al., 2011; Park and Kim, 2019). The hydrophobic surface of PE is turned to hydrophilic by the attachment of microorganisms (Sudhakar et al., 2008). The change in carbonyl index was ascertained through FTIR and ketone and aldehyde groups were formed. The CO₂ and H₂O were produced as a result of β-oxidation (Novotný et al., 2018). Gram negative bacteria including Klebsiella pneumoniae play an important role in wastewater treatment (Maal et al., 2014). K. pneumoniae secretes lipase (Peil et al., 2016), tyrosinase, peroxidase, and laccase which can be involved in PE degradation (Dhanve et al., 2008). Surfactants, released by K. pneumoniae extracellularly, play their role in hydrophilic and hydrophobic phase exchange. These phase exchanges help microbes to penetrate easily into the PE and degrade it.

12 Conclusions

Plastics are petroleum-derived polymers and are used for various purposes. PE bags are used all over the world at large levels. The availability of micro- and nanoplastics in aquatic environment has been increased many folds due to biodegradation, thermo-oxidative degradation, photodegradation, thermal and hydrolysis processes in the ecosystem and poses serious threat to the aquatic life (fresh and marine) and human life through food web. There is a need to use adequate biodegradable methods to eradicate these polymers from the ecosystem. Due to the hydrophobic and inert nature, it is difficult to remove or degrade polymers. Besides physical and chemical methods, microbes have shown promising potential to degrade these polymers.

The potential use of microbes for polymers removal needs to be further evaluated using original polymers contaminated wastewater. The removal of microplastics/nanoplastics, their toxicity and the utilization of microbes remain to be addressed. The transfer of plastic polymers from the waste into the aquatic ecosystem including rivers and oceans through different processes and the strategy to shift these polymers from the wastewater to a suitable place for deposition/incineration should properly be advocated. Long-term coordinated cleanup operations are needed to evaluate the progressive ecosystem effects.

Funding

No funding was received for this work from any organization.