The Fungi That Degrade Plastic: History
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Subjects: Environmental Sciences
Contributor:
Anusha H. Ekanayaka
,
Saowaluck Tibpromma
,
Donqin Dai
,
Ruifang Xu
,
Nakarin Suwannarach
,
Steven L. Stephenson
,
Chengjiao Dao
,
Samantha C. Karunarathna

Plastic has become established over the world as an essential basic need for our daily life. Current global plastic production exceeds 300 million tons annually. Plastics have many characteristics such as low production costs, inertness, relatively low weight, and durability. The primary disadvantage of plastics is their extremely slow natural degradation. The latter results in an accumulation of plastic waste in nature. Many fungi can be used to degrade plastics.

  • fungi
  • global plastic production
  • plastic waste accumulation

As global plastic production and plastic waste accumulation increase rapidly, we need to look for a quick and efficient solution to save nature and, indeed, the entire planet [[1],[2],[3]]. The problem becomes even more acute as the natural degradation rate of all types of plastic is very slow [[4]]. Hence, it is essential to look at ways to accelerate plastic degradation methods. Several solutions that have been proposed are photo-degradation (degrade by light), chemical degradation, thermal degradation (degrade by heat), irradiation using gamma rays, and biodegradation (degrade by biological additives or microorganisms) [[5][6]]. Biodegradation has been suggested as the best solution as it is an eco-friendly approach. However, based on the results obtained in previous studies, people select biodegradation since the other options are not cost-effective [[6]]. In this study, we reviewed the literature on plastic-degrading fungi from different sources and summarized a list of records on plastic degraders in the fungi kingdom. Moreover, we analyzed phylogenetic relationships of plastic-degrading fungi based on a combined ITS, LSU, SSU, TEF, RPB1, and RPB2 dataset from 395 strains and provided brief taxonomy at the level of class.

 

1. Phylum Ascomycota

1.1. Class Dothideomycetes

The Dothideomycetes is the largest class within the phylum Ascomycota. Most of the taxa within this class are recorded as saprobes in various habitats and substrates [7]. Our investigations revealed that some members of Dothideomycetes are capable of plastic degradation. Most of the recorded species of the Dothideomycetes belong to the order Pleosporales, but a few taxa are recorded from the Dothideales and Botryosphaeriales (Table 2, Figure 1 and Figure 2). Plastic degraders in the Dothideomycetes have the ability to degrade LDPE, PUR, PS, PCL, PEA, PPA, PBA, HDPE, PVC, PE, PU, and Sky-Green plastics (Table 2). Recent studies on plastic-degrading members of the Dothideomycetes are those of Khruengsai et al. [8] and Brunner et al. [9]. In the phylogenetic tree, the Dothideomycetes formed a well-supported clade sister to the Arthoniomycetes. Most of the plastic-degrading Dothideomycetes were placed in the upper subclade of the main Dothideomycetes clade, and the rest were grouped in a basal subclade (Figure 1 and Figure 2).

1.2. Class Eurotiomycetes

The Eurotiomycetes are extremely common saprobes in diverse habitats and substrates [10]. Based on our results, most plastic-degrading fungal records belong to the Eurotiomycetes. Many plastic-degrading members of the Eurotiomycetes are taxonomically placed under the Eurotiales, and the most common plastic-degrading fungal genera are Aspergillus and Penicillium (Table 2, Figure 1 and Figure 2). The plastic types they are reported to degrade are HDPE, LDPE, PCL, PE, PVC, PS-PUR, PEA, PPA, PBA, PHB, Poly[3HB-co-(10 mol%) 3HV], Sky-Green, PHV, PBS, PLA and PVC (Table 2). Recent studies on plastic-degrading Eurotiomycetes are those of Rani & Singh [11], Ndahebwa Muhonja et al. [12], Bermúdez-García et al. [13], Laila [14], Khruengsai et al. [8], Munir et al. [15], Alshehrei [16], Sangale et al. [17], Duan et al. [18], El-Morsy et al. [19], Brunner et al. [9] and Ojha et al. [20]. The Eurotiomycetes is the uppermost clade within our phylogram (Figure 1 and Figure 2). The genera Aspergillus and Penicillium contain a large number of species with a worldwide distribution and a huge range of ecological habitats [21]. They are mostly widespread saprobes and can be found in both indoor and outdoor environments, including in both the air and soil. In addition, some species of Aspergillus and Penicillium have the ability to grow under extreme conditions [21]. Hence, further research on these genera would provide better solutions for the environmental accumulation of plastics.

1.3. Class Leotiomycetes

Most of the Leotiomycetes are saprobes on a wide variety of substrates. However, this class also includes many important plant pathogens [22]. Our results showed that the few records of plastic-degrading fungi are phylogenetically related to the Leotiomycetes (Table 2, Figure 1 and Figure 2). In the phylogenetic tree of this study, the Leotiomycetes formed a well-supported clade sister to the Laboulbeniomycetes (Figure 1 and Figure 2). However, there is a single record found that clearly belongs to the Leotiomycetes and possibly has the ability of plastic degradation [19]. The other records that grouped within Leotiomycetes in our phylogeny were Cephalosporium gramineum, which is currently placed under the Sordariomycetes. Therefore, studies with a wide range of taxon sampling are required to resolve the phylogenetic position of Cephalosporium gramineum. Furthermore, a recent study on the biodegradation of bio-based and biodegradable plastic, polybutylene succinate-co-adipate (PBSA), identified a species (Tetracladium furcatum) within the Leotiomycetes that has the ability to degrade PBSA [23]. However, recent studies on synthetic plastic-degrading members of the Leotiomycetes are very few. As a result, additional studies on the Leotiomycetes are required to assess their ability to degrade plastics.

1.4. Class Saccharomycetes

The Saccharomycetes is a small class of yeasts with a single order of about 1000 known species, which are classified under the Ascomycota [24]. Most of the Saccharomycetes are saprobes, and few are recorded as human and plant pathogens [24]. The present study discovered five records of five members of the Saccharomycetes capable of degrading plastics (Table 2, Figure 1 and Figure 2). The Saccharomycetes is the second basal clade within the phylum Ascomycota. All Saccharomycetes members that are plastic degraders are grouped in the upper subclade of the main Saccharomycetes clade (Figure 1 and Figure 2). Arxula, Candida, and Debaryomyces are the genera to which those plastic-degrading members of the Saccharomycetes belong [25][26]. Some members of the Saccharomycetes are widely used in industrial and biotechnological processes. Species such as Saccharomyces cerevisiae are model organisms in many types of research [24]. A recent study used Genetic engineering techniques on two strains of Saccharomyces cerevisiae to produce the heterologous protein Polyethylene Terephthalate (PET) hydrolase enzyme, which has been shown to have the capability of degrading PET into its subsequent monomers [27]. We believe future research on the Saccharomycetes would find a better solution for plastic accumulation in nature.

1.5. Class Sordariomycetes

The Sordariomycetes is the second largest class within the phylum Ascomycota. The majority of the Sordariomycetes are saprobes, but the group also includes some important plant pathogens [28]. They have a wide ecological distribution in both terrestrial and aquatic habitats [28]. Our research recorded many members of the Sordariomycetes with the ability to degrade plastics (Table 2, Figure 1 and Figure 2). The plastic types they are reported to degrade are PE, PS, PHB, Poly[3HB-co-(10 mol%) 3HV], PUR, PS-PUR, HDPE, LDPE, PVC, PCL, PEA, PPA, and PBA (Table 2). Recent studies of plastic-degrading Sordariomycetes are those of Munir et al. [15], (Yang et al. [29], Brunner et al. [9], and Khruengsai et al. [8]. The Sordariomycetes formed a middle clade within the main Ascomycota clade that is sister to the Laboulbeniomycetes (Figure 1 and Figure 2). Many plastic degraders in the Sordariomycetes are classified under the Hypocreales, while others belong to the Amphisphaeriales, Glomerellales, Phyllachorales, and Sordariales. Even though the Eurotiomycetes include the highest number of records of plastic-degrading fungi, the Sordariomycetes contain the highest number of genera with the capability to degrade plastics.

2. Phylum Basidiomycota

2.1. Class Agaricomycetes

The Agaricomycetes is a morphologically diverse class of macrofungi within the Basidiomycota, containing around 36,000 described species. They are ecologically diverse and include saprobes, mycorrhizal symbionts, and pathogens [30]. Moreover, the Agaricomycetes encompasses several important commercially growing edible mushrooms [31]. The present study found several records of Agaricomycetes with the ability to degrade plastics (Table 2, Figure 1 and Figure 2). They are reported to degrade Poly[3HB-co-(7 mol%) 3HV], LDPE, PVC, polyethylene, and PHB (Table 2). Additionally, da Luz et al. [32] performed a study on plastic-degrading Agaricomycetes. They investigated the degradation of oxo-biodegradable plastic bags and green polyethylene by Pleurotus ostreatus. The Agaricomycetes is the upper clade within phylum Basidiomycota, and it is highly statistically supported within the present phylogeny (Figure 1 and Figure 2). Further studies of edible mushrooms belonging to the Agaricomycetes and their ability to degrade plastics would increase world food production and reduce the plastic accumulation in nature.

2.2. Class Microbotryomycetes

The Microbotryomycetes include mainly mycoparasites, saprobic yeasts, and plant pathogens [33]. A single record of plastic-degrading fungi was found in the order Sporidiobolales of the Microbotryomycetes in the present study (Table 2, Figure 1 and Figure 2). In our phylogenetic tree, the Microbotryomycetes formed a well-supported clade sister to Tritirachiomycetes (Figure 1 and Figure 2).

2.3. Class Tremellomycetes

The Tremellomycetes are classified under the Basidiomycota and consist of saprobic yeasts, dimorphic taxa, and species that form hyphae and/or complex fruiting bodies [34]. The present study identified a few records from the Tremellomycetes that are capable of degrading plastics (Table 2, Figure 1 and Figure 2). All the records belong to the genera Cryptococcus and Papiliotrema (Tremellales), andthey are capable of degrading PCL, PBS, and PBSA (Table 2). The Tremellomycetes formed a well-supported clade sister to Agaricomycetes in the present phylogenetic tree (Figure 1 and Figure 2). A recent study on synthetic plastic-degrading Tremellomycetes was published by Hung et al. [35]. A recent study on biodegradable plastic mulch films (BDMs) and their associated soil microbial communities found that the Tremellomycetes are capable of degrading agriculturally-weathered BDMs [36].

2.4. Class Tritirachiomycetes

The Tritirachiomycetes is a small class within the Basidiomycota that is made up of filamentous fungi. They are mainly saprobes, but some have been recorded as human pathogens [37]. A single record of a fungus from this class that is capable of degrading plastics was found in the present study (Table 2, Figure 1 and Figure 2). The Tritirachiomycetes formed a well-supported clade sister to the Microbotryomycetes in our phylogenetic tree (Figure 1 and Figure 2).

2.5. Class Ustilaginomycetes

The majority of the Ustilaginomycetes are economically important plant pathogens. They are usually unicellular yeasts (sporidia), but some are simple multicellular forms, such as a pseudomycelium, multicellular cluster, or mycelium [38]. Moreover, the Ustilaginomycetes have a comparatively short life cycle, which makes them easy to handle under laboratory conditions. As a result, the Ustilaginomycetes can be considered model organisms for studying fungi [38]. The present study found a single record from the Ustilaginomycetes of a fungus capable of degrading plastics (Table 2, Figure 1 and Figure 2). The Ustilaginomycetes is the basal clade within the main Basidiomycota clade, and it is statistically highly supported (Figure 1 and Figure 2).

3. Phylum Mucoromycota

Class Mucoromycetes
The Mucoromycetes are a class within the phylum Mucoromycota and consist of mainly filamentous fungi with a saprobic lifestyle. Several species are also life-threatening human pathogens, plant parasites, and food spoilage organisms. Moreover, members of the Mucoromycetes are used as a traditional fermenting agent for Asian and African foods, such as soybean products and several varieties of European cheese. Fungi belonging to the Mucoromycetes are common in the environment and able to colonize all kinds of wet, organic substrates [39]. The present study found several Mucoromycetes fungi with the ability to degrade plastics. All the recorded plastic-degrading members of the Mucoromycetes belong to the genera Mucor and Rhizopus. These fungi are capable of degrading PHB, HDPE, LDPE, PVC, PCL, polyalkylene dicarboxylic acids, PPA, and PET copolymers with dicarboxylic acids (Table 2). A recent study of plastic-degrading Mucoromycetes was that of Pardo-Rodríguez & Zorro-Mateus [40]. The Mucoromycota formed the basal clade within our phylogenetic tree (Figure 1 and Figure 2). However, the phylum presented a polyphyletic nature in the present phylogenetic tree and was separated into two basal clades.
Even though plastic is currently an important material in the global environment, it is becoming a huge threat to nature. Because current global plastic production is increasing rapidly (300 million tons annually) and plastics have a very low natural degradation rate, they accumulate in natural environments and cause considerable damage to biodiversity and natural ecosystems. At present, scientists and researchers are assessing the usefulness of microorganisms in accelerating plastic degradation. In this study, we reviewed plastic degradation using fungi. Herein we list more than 200 records of fungi capable of degrading fungi based on the available literature. Their phylogenetic relationships were analyzed using a combined ITS, LSU, SSU, TEF, RPB1, and RPB2 dataset generated from 395 strains. Our results confirm that plastic-degrading fungi are taxonomically diverse and belong to three major fungal phyla—the Ascomycota, Basidiomycota, and Mucoromycota. The Ascomycota plastic degraders belong to five major classes: Dothideomycetes, Eurotiomycetes, Leotiomycetes, Saccharomycetes, and Sordariomycetes. Plastic-degrading Basidiomycota fall within the Agaricomycetes, Microbotryomycetes, Tremellomycetes, Tritirachiomycetes, and Ustilaginomycetes. Mucoromycota fungi capable of degrading plastics were found under the Mucoromycetes. The Eurotiomycetes include the highest number of recorded plastic degraders in the fungi kingdom. However, a wide range of plastic-degrading fungal genera was found within the class Sordariomycetes. Moreover, there is an acute need for future research on similar topics to resolve the global problem of plastic accumulation in nature.

This entry is adapted from the peer-reviewed paper 10.3390/jof8080772

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