Microbial colonization and degradation of marine microplastics in the plastisphere: A review

1Plastics have the advantages of low density, good ductility, durability and low cost, and have become widely used, worldwide. The current use of plastics is ~20 times that of half a century ago, and it is expected that the production and use will double in the next 20 years. Most of the plastic wastes discharged into the environment are chemically stable, corrosion-resistant, and difficult to be degraded by microorganisms. This has resulted in a severe environmental issue. It is predicted that 4.8–12.7 million tonnes of plastics enter the oceans annually. This amount is likely to increase by an order of magnitude within the next decade. Recently, the COVID-19 pandemic has driven explosive growth in the use of face masks resulting in many issues related to their disposal. Indeed, it is estimated that over 129 billion face masks are used globally each month, and over 16 million plastic particles are released from just one weathered mask by the effect of sand. Plastics could be classified by physical and chemical properties, such as density, molecular weight, crystallinity and functional groups as well as the additives used, such as plasticizers, antioxidants and flame retardants. The main types of “nonbiodegradable” plastics include polyethylene (PE), polypropylene (PP), polystyrene (PS), polyethylene terephthalate (PET) and polyvinylchloride (PVC).

2Microplastics (MPs) refer to the plastic fragments of <5 mm in diameter, and may be divided into primary and secondary MPs. Primary MPs are directly produced and used in personal care products, such as toothpaste and certain cosmetics, and cause direct microplastic pollution after discarded to the environment. Secondary MPs refer to the plastic fragments that are broken up by photodegradation, mechanical breakup, erosion and aquatic immersion, which are main form of MPs present in the ocean. It is estimated that there are more than 5.25 × 1012 plastics in the surface waters of the world’s ocean, of which the weight of MPs is ~0.35 × 105 tonnes. MPs could be transported horizontally for long distances through the ocean currents and wind, and vertically depending on the density of the particles. At present, MPs have been found to be widely distributed in the oceans, from polar regions to the equator, from densely populated areas to remote islands, and from beaches to large ocean gyres and deep seas. In addition, MPs has been detected in the deepest trenches, i.e., the Mariana Trench. For example, the MPs isolated from the coast of Qingdao, China are detailed in Figure 1.

3MPs have serious toxic effects on marine organisms and human beings, as well as negative effects on the ecological environment. Firstly, plasticizers with ecological toxic effects are released into the marine environment. Secondly, MPs can combine with persistent organic matter to form composite pollutants that cause enhanced toxicological effects. Thirdly, MPs’ surface structure may be changed, and become charged in the seawater thereby increasing toxicity that may be caused by interaction with heavy metals. The toxic substances may be accumulated in marine animals after they ingest MPs, which lead to damage to the biodiversity in marine environments. Moreover, MPs may be enriched by passage through the human body leading to adverse effects on health. Recently, increasing concern has been raised regarding the hazard potential of microplastic-associated microbial communities. In particular, certain MP surfaces have been shown to exhibit selective enrichment of bacterial pathogens—so called “dangerous hitchhikers”—that disperse over long distances. For example, Vibrio species are enriched particularly on MPs. The ability of MPs to serve as carriers for dangerous hitchhikers poses threats to both aquatic ecosystems and human health. Besides colonization with pathogens, MPs could act as a long-term reservoir for antibiotic resistance.

4The damage of MPs to biodiversity and ecosystem health is increasing in significance, especially with regards to microorganisms. Elucidating the role of MPs in the microbial loop and the role of microorganisms in the degradation of MPs is of great value. This may provide insights for the design of efficient degradation enzymes, and thereby reduce damage to human beings and the environment. This article reviews the current knowledge of the bacterial composition of the MP biofilms, the biodegradation of MP, and the relationship between plastisphere and quorum sensing (QS).

5MPs can provide advantages to the colonizing microbial communities, including physical support, nutrient supply and habitats that help microorganisms to resist harsh environmental conditions. As with any kind of surface, microorganisms attach to and colonize MP surfaces immediately after the material enter the aquatic ecosystem, forming MP biofilms that have been termed the “plastisphere”. The plastisphere may be regarded as a new micro-ecosystem in pelagic waters, and include primary producers, predators, symbionts, and decomposers. The microbial communities in the plastisphere are composed of a diverse range of bacteria, fungi, viruses, archaea, algae, and protozoans.

6The growth of the microbial community on MP biofilms represents a temporal succession process that may be divided into different stages. In the initial colonization stage, the pioneer microorganisms are able to form microbial assemblages, and cover the maximum possible surface area of plastic. These generalist organisms proliferate without competition other than to grow faster than the rest to cover the surface, and pave the way for the enhanced attachment of other microorganisms, and recycling of resources. As the biofilm grows, within days microorganisms attach to the plastic surface irreversibly, followed by a succession of other bacteria, viruses and eukaryotic microorganisms. This is achieved by pili, adhesion of proteins, and production of complex extracellular polymeric substances (EPS), which facilitate adhesion to surfaces and stablish cell–cell interactions. The secondary metabolites may improve quorum sensing and the antimicrobial effect to resist competing microorganisms. Processes involve catalyzing metabolic reactions, including adsorption, desorption, and fragmentation of microplastic-associated compounds. Finally, the continuous recruitment, loss, and replacement of species transform the structure into a hotspot for diverse interacting communities, resulting in a mature plastisphere. For example, maturation phase of the PE plastisphere appeared after 30 days immerging in seawater, and a stabilization of bacterial abundance and heterotrophic bacterial production without significant increase was reached. However, there was a drastic shift in bacterial community structure in maturation phase. The formation of and succession in the plastisphere is described in Figure 2.

7Early dominant pioneer communities in marine and estuarine plastispheres belong to primary producers including diatoms, cyanobacteria, green algae and bacterial members of Gammaproteobacteria and Alphaproteobacteria. As for Gammaproteobacteria, Oceanospirillaceae and Alteromonadaceae representatives were present, and which could occur up to 59.1% of the total microbial community after 1 day of immersion of the MPs in the marine habitat. Their presence decreased significantly later. Also, Vibrio spp. were early colonizers of PE and PS in marine environments. Alcanivorax, Aestuariicella, and Marinobacter were the dominant early colonizers on different plastic substrates. In addition, the families Saprospiraceae and Oscillatoriaceae were found on early stages of the plastisphere. With the plastisphere becoming mature, the abundance of distinct microbial communities, including Bacteroidetes and Alphaproteobacteria, increased quickly on the plastisphere. For example, Bacteroidetes were always significantly more abundant at later stages. In contrast, Rhodobacteraceae came early to MPs, and they were persistent and became dominant as time passed. Rhodospirillaceae, including purple sulfur bacteria, may fix N2 and thus provide “fertilizer” to other community members. In addition, flavobacteria, Planctomycetaceae and Phyllobacteriaceae were abundant at the later stages of the MPs colonization.

8The microbial community composition of the plastisphere represents the main research target, and many studies revealed significant differences from microhabitats in the same environment. Proteobacteria, Bacteroidetes, Firmicutes and Cyanobacteria are usually the main bacteria enriched in the plastisphere. This differs from a range of other substrates, such as metal, rubber, glass, fabric, and seawater. Moreover, there was a different abundance and distribution pattern of photosynthetic and heterotrophic bacteria in plastic samples compared with those in seawater. These data indicate that the plastisphere is a specific ecological niche where microorganisms with potential metabolic adaptations, specific metabolic pathways (including attachment, chemotaxis, additive resistance, degradation, secretion, nitrogen fixation and motility) were enriched. Studies on microbial community composition of the plastisphere based on research methods of field sampling and in situ incubation are summarized in Table 1.

9Diatoms (phototrophic organisms) are common residents of the plastisphere, and are often reported as early and even dominant colonizers on plastic debris (notably the plastics exposed to sunlight; Table 1). For example, diatoms dominated in the microbial community on the abundant MPs in the Eastern North Pacific Gyre. Although the dominate role of diatoms declines with plastisphere maturing, they remain consistent members in the plastisphere.

10As another photosynthetic organism, Cyanobacteria join with diatoms to typically contribute net primary production on MPs, providing nutrients for heterotrophs in the plastisphere. Many studies have shown that Cyanobacteria are dominate candidates of the plastisphere, especially in the early stages (Table 1). For example, the genera Stanieria and Pseudomorphium were found abundant on PET across stations. In particular, the genus Phormidium was found commonly in microbial mat on various substrates, and has been found to be present on PE, PET, and PP samples (Table 1). This genus was identified as an important member of a plastic-colonizing community in the North Atlantic, and also determined to degrade hydrocarbons. In addition, filamentous cyanobacteria, Phormidium, occurred on plastics, but was absent from seawater samples. Sunlight exposure on floating MPs may well be beneficial to the enrichment of this photosynthetic organism on plastic debris.

11As the most abundant phylum globally, Proteobacteria comprise the most enriched phylum on the plastisphere in comparison with populations in seawater. As is shown in Table 1, within the phylum Proteobacteria, the classes Alphaproteobacteria, Gammaproteobacteria, Betaproteobacteria, and Deltaproteobacteria are enriched on plastic samples.

12Many studies showed that the family Rhodobacteraceae, within class Alphaproteobacteria, occupied the core population of the plastisphere (Table 1). Rhodobacteraceae, especially Roseobacter, was recognized as a primary colonizer of various substrates in marine environments. However, these organisms were found to be enriched significantly on marine plastic debris as compared with organic particles and seawater. In fact, Rhodobacteraceae is not only the primary colonizer, but is also abundant at all colonization periods, and exerts an important role in biofilm formation. This reflects the extracellular polymeric substance (EPS) produced by Rhodobacteraceae after colonizing new surfaces, leading to enhancing the settlement of other microorganisms. Apart from Rhodobacteraceae, bacteria belonging to the family Erythrobacteraceae have been found on various macro−/micro-plastics (Table 1). Moreover, hydrocarbonoclastic bacteria were overrepresented in the plastic fraction.

13Within Gammaproteobacteria, the order Pseudomonadales has been highlighted. Pseudomonas was found to have biodegradation potential on MPs (as discussed later) leading to interest for MP-degradation research. As is shown in Table 1, Vibrio is another member of the Gammaproteobacteria detected widely on MPs in marine environments. Many Vibrio spp. are pathogenic and regarded as dangerous hitchhikers on MPs facilitating their spread widely throughout the marine environment. Vibrio spp. are usually primary colonizers, and grow rapidly with the ability to dominate on the plastisphere in comparison with natural seston. Moreover, the order Oceanospirillales and the family Alcanivoraceae have been found in the plastisphere (;; Table 1).

14Bacteriodetes is the second most represented bacterial phylum on plastic surfaces (Table 1). Here, the distribution of Bacteroidetes do not reveal clear temporal patterns, and is dominated constantly by Flavobacteria. These may well be essential members, and key players in the formation of biofilms. The class Flavobacteria has been recognized as colonizers on various MPs, including PS, PE, PP, and PET (Table 1). For example, the family Flavobacteriaceae occurred more frequently on PET particles compared with glass beads, and PE and PS compared with wooden pellets. Flavobacteriaceae has been described as a keystone taxon in biofilms that feed off exudates from dinoflagellates and diatoms.

15The order Sphingobacteriales and genus Lewinella have been reported frequently as colonizers of the plastisphere. Sphingobacteriales was shown capable of metabolizing polycyclic aromatic hydrocarbons (PAHs; ) and abundant in both short-term (60 days) and long-term (5 months) MP samples after outside incubation in North Seawater.

16Firmicutes was found among the most abundant populations enriched on marine PS samples. In particular, the genus Bacillus has revealed a wide-spread and powerful biodegradation potential on various kinds of MPs, namely PE, PP, PS, PVC, and PET.

17Factors driving the microbial composition in the plastisphere are complex, and may be divided into environmental and polymer characteristic factors. Environmental aspects include physicochemical factors (namely temperature, salinity, depth, pH, dissolved oxygen and light), nutrient availability (e.g., organic/inorganic carbon, ammonium, nitrate, nitrite and phosphorus) for microbial growth, pollutants (e.g., toxic metals, antibiotics and persistent organic pollutants), and biotic factors (principally algae and animals; ). Also, polymer characteristic factors include the type, surface property and size of the plastics.

18Environmental factors related to geography have a larger influence on the plastisphere community than the plastic type. Studies on microbial communities on different polymer types floating in the North Pacific and North Atlantic demonstrated that plastisphere communities were well-defined biogeographically, displaying latitudinal gradients in species richness, and to a lesser extent between polymer types. As is shown in Table 1, core microbial communities in marine environments show clear geographical distribution patterns, which may influence the formation of specific plastispheres. So far, studies investigating the plastisphere in various marine environments are mainly focused in Europe (Mediterranean Sea, North Sea and Baltic Sea) and China, and to a lesser extent the Atlantic, Pacific and Southern Ocean (Table 1).

19Apart from geography, there are other environmental factors influencing the plastisphere community. Microbial diversity and function show strong dependency on environmental conditions, in turn influencing MP biofilm formation and structure. And the early attachment and succession of plastisphere are affected by the growth rate of the biofilm, determined by factors including temperature, light, and nutrient availability. For instance, the light availability was shown to play a key role in shaping plastisphere communities, and revealed that environmental variables, not plastic type, had the largest impact on microbial composition. In addition, microbial communities in the plastisphere along an environmental gradient were shaped more by salinity than by plastic type. Indeed, salinity gradients influenced microbial communities in the plastisphere significantly, particularly enhancing the abundance of Gammaproteobacteria. Moreover, ocean acidification altered bacterial communities on marine plastic debris. It was noteworthy that the light intensity was negatively correlated with depth, which could cause the depth-dependent distribution of photosynthetic bacteria. Photoautotrophic bacteria, such as cyanobacteria, i.e., the genera Phormidium and Rivularia, dominated the plastisphere communities living in surface seawater, whereas the core microbiome of the plastisphere living on the seafloor and sub-surface seawater appeared to comprise Bacteroidetes (Flavobacteriaceae) and Proteobacteria (Rhodobacteraceae and Alcanivoracaceae; ).

20In addition, the abundance of the microbial community of the plastisphere is influenced by the size and especially the type of plastic. This may be attributed to the chemotactic selectivity colonization on MPs with different polymer chemical properties. The results in a situ exposure experiments for nine different types of MPs, including low density polyethylene (LDPE), PS, expanded polystyrene (EPS), PP, polycarbonate (PC), polyamide 6 (PA6), PVC, PET, and acrylonitrile butadiene styrene (ABS) in mangrove, revealed that MPs with different chemical structures would attract different microbial colonizers. quantified the biofilm on PE, PP, and PS by six marine bacterial strains (Vibrio, Pseudoalteromonas and Phaeobacter), demonstrating that each one had a unique colonization behavior with either a preference for PS or PP over the other polymer types, or no preference at all. re-analyzed all plastisphere studies that utilize 16S rRNA gene amplicon sequencing, and found that Oceanospirillales and Alteromonadales were more abundant in plastic samples than control biofilms, with Oceanospirillales generally being more abundant in aliphatic plastic samples, and Alteromonadales in other plastics. In addition, the roughness, hydrophobicity and age of MPs could clearly influence microbial community structure of plastisphere. Interestingly, differences in microbial composition between polymers are usually caused by rare taxa whereas the abundant microbial groups remain largely unchanged.

21Plastisphere development does rely largely on the surrounding microbial communities although there are significant differences between them. In fact, consistent conclusions have not been made when studying the microbial community compositions of the plastisphere in marine environments because of the variety of plastic substrate types, season and geographical location. For example, early attachment and succession of the plastisphere depend on the growth rate of the biofilm, determined by physicochemical factors and nutrient availability. There may well be some polymer-specific communities in the initial colonization, which are largely influenced by the differences between materials, such as additives or preweathering, and will eventually converge over time.

22The plastisphere has multiple effects on the fate of plastics and the marine environment. Firstly, the plastisphere may change the density of MP particles, making them susceptible to vertical transport by sinking and floating. Secondly, the plastisphere may change the adsorption state of the MP surface, and affect the decomposition rate of the MPs in seawater. In the biofilm, autotrophic microorganisms may accelerate the oxidative decomposition of MPs by producing oxygen during photosynthesis. Heterotrophic microorganisms may degrade MPs by a series of processes, including biodeterioration, bio-fragmentation, bio-assimilation and biomineralization. Conversely, the plastisphere may slow down the photochemical decomposition process of MPs by ultraviolet light. Moreover, microorganisms colonizing MPs may be transported vertically and for long-distances horizontally in the ocean, which may promote the diffusion of invasive species to fragile ecosystems. Pathogens, such as Vibrio, Tenacibaculum, Pirellulaceae and spirochetes, were usually found on MPs. When algal blooms and infectious diseases caused by pathogens occur, the negative influence on marine ecosystems is significant. Therefore, the risk of MPs carrying pathogens to infect humans and cause long-distance transmission should be determined.

23The biodegradation of plastics may be defined as the process that microorganisms digest and decompose plastic fragments into available carbon sources by changing the plastics functional group structure, molecular weight, tensile property and other features associated with the polymers. The microbial degradation of MPs is affected by microorganisms, MPs properties, and environmental factors.

24Up to now, information regarding the microorganisms involved in plastic degradation is rudimentary. Currently, the microorganisms capable of degrading MPs are mainly associated with the terrestrial environment, and more so for PE degradation, and include Achromobacter, Acinetobacter, Arthrobacter, Aspergillus (fungus), Bacillus, Comamonas, Delftia, Micrococcus, Nesiotobacter, Paenibacillus, Pseudomonas, Rahnella, Staphylococcus, and Stenotrophomonas. These have been isolated from various soil environments, saltpan water and landfills (Table 2). Bacteria capable of degrading PET include Ideonella and Saccharomonospora, which were isolated from a PET bottle recycling site and recovered from compost, respectively. Pseudomonas, Bacillus and Achromobacter were demonstrated to degrade PVC. Aspergillus showed the ability to degrade PU. Moreover, Thermus, Bacillus and Geobacillus, which were isolated from a sludge composting pool, degraded PS, suggesting that hyperthermophilic composting was a promising strategy for MPs removal from organic wastes. Bacillus and Pseudomonas, capable of degrading high impact polystyrene (HIPS), were obtained from landfills. Aspergillus, Bacillus, Pseudomonas, Staphylococcus, and Streptococcus were isolated from different soil samples, and were capable of degrading PET and PS. In addition, a Rhodococcus strain isolated from soil burying PE mulch was capable of degrading both PS and PE.

25It is noteworthy that Bacillus and Enterobacter in waxworm gut could “eat” PE, whereas Exiguobacterium, Bacillus anthracis, Enterobacter hormaechei, and Aspergillus niger in mealworm gut could attack PS. In addition, the marine polychaete Marphysa sanguinea inhabiting PS debris was able to degrade PS particles. Certainly, studying the microfauna and gut microorganisms may be an innovative way for the treatment of plastic waste.

26At present, studies on the microbial degradation of marine plastics are limited, and mainly involve the enrichment and isolation of plastic degrading microorganisms in the offshore environment. Thus, Arthrobacter, Aspergillus, Bacillus, Kocuria, Pseudomonas and Zalerion maritimum (fungus) demonstrated the capability of degrading PE, and Bacillus could degrade PVC (Table 2). Pseudomonas, isolated from plastics immersed for several days in Bay of Bengal, was found have a great ability to degrade PP, LDPE and HDPE. Furthermore, Pseudomonas aeruginosa E7, which was isolated from beach soil contaminated by an oil spill, displayed high degradative activity to low-molecular-weight polyethylene (LMWPE), and metabolized 40.8% of the carbons of LMWPE into CO2 after 80 days of composting. Pseudomonas and Lysinibacillus, which were isolated from deep-sea sediment, used an increased extracellular matrix to improve cell adhesion to weathered HDPE. Other examples include Rhodococcus and Bacillus, which were isolated from mangrove, and were capable of degrading several kinds of MPs. Moreover, after 40 days of incubation, weight losses of PE, PET, PP, and PS particles were found and it was resulted from the action of Bacillus cereus and Bacillus gottheilii. Bacillus sp. strain 27 and Rhodococcus sp. strain 36 could also degrade PP and cause weight losses. Apart from aerobic bacteria, anaerobic marine consortia were found degrade PVC.

27As is shown in Table 2, Bacillus and Pseudomonas were very important bacteria in the degradation of MPs. Among the 15 strains of bacteria capable of degrading HDPE isolated from the coast, Pseudomonas was the most efficacious. Pseudomonas spp. achieved a percentage weight reduction of PE of up to 20% within 120 days. The metabolites of PS decomposed by Pseudomonas were styrene, toluene and benzene, which could be easily used by other bacteria. A novel carboxylic ester hydrolase was identified in the genome of the marine bacterium Pseudomonas aestusnigri, indicating its significant potential for PET degradation. It seems that the degradation ability of Pseudomonas is partly due to the high hydrophobicity of the cell surface, which is conducive to its adhesion to the polymer, and the formation of biofilm to promote degradation. In addition, the secretion of extracellular polysaccharide is important to promote the degradation of LDPE. However, the degradation effects vary with types of plastics.

28Biofilm has an important effect on biodegradation, which relies on the influence of nutritional conditions for its formation. An alteration of Pseudomonas surface hydrophobicity was detected by the change of glucose and ammonium sulfate concentrations. Thus, the increased cell surface hydrophobicity promoted the efficient formation of biofilm in a polyethylene succinate film, which was positively correlated to degradation. Conversely, in the presence of marine sediments, which were organic carbon-rich, biofilm formation was diminished, and the degradation of PE was minimal. Therefore, environmental and nutritional conditions that favor the genesis of biofilms on plastic polymers are important stimuli for the degradation of synthetic plastics by Pseudomonas.

29A toxic metabolite produced by one microorganism may be a substrate for the growth of another, thus eliminating the toxic effects to the former. Conversely, symbiotic interactions in consortia increased the activity and tolerance for the treatment of pollutants. For example, Bacillus and Paenibacillus reduced the dry weight of MP particles (14.7% after 60 d) and the mean particle diameter (22.8% after 60 d) when in a bacterial consortium. Moreover, a marine bacterial community composed of Idiomarina, Marinobacter, Exiguobacterium, Halomonas, and Ochrobactrum was capable of colonizing and degrading PET and PE efficiently.

30The mechanisms and enzymes of MP biodegradation have not been fully elucidated. Overall, the process of microbial degradation of MPs may be divided into colonization, depolymerization, assimilation and mineralization, which involve multiple biochemical reactions. After colonization on the surface of MPs, microorganisms release extracellular enzymes to combine with polymers and cleave them. This leads to depolymerization into low molecular weight oligomers, dimers and even monomers. The processes involve hydrolysis (for hydrolyzable plastics) and oxidative degradation (for hydrolyzable and non hydrolyzable plastics). After depolymerization, the oligomers enter the cells, and serve as the carbon source for microbial growth, which is assimilation. The mineralization refers to the decomposition of different types of MPs into small molecules, such as CO2, CH4 and H2O, through the TCA cycle (Figure 3). Up to now, the plastic degrading enzymes have been reported to include hydrolases (such as esterase, lipase, keratinase, and cutinase) and oxidoreductases (such as laccase, manganese peroxidase, hydroxylase and lignin peroxidases).

31PE degrading biocatalysts include hydroxylase, laccase, peroxidase and reductase. A manganese peroxidase was identified in two types of fungi leading to degradation of PE. Laccase, which is produced by Actinomycetes, Rhodococcus, Aspergillus flavus and Pleurotus ostreatus, degraded PE significantly. With Pseudomonas aeruginosa, alkane hydroxylase was involved directly in the biodegradation of LMWPE. Also, rubredoxin and rubredoxin reductase exerted an indirect role through the transfer of related electrons. In addition, alkane hydroxylase, which was produced by Pseudomonas sp. E4, played an important role in the degradation of PE through the oxidation of the PE main chain.

32Although the microbial degradation of PS by various bacteria and fungi has been demonstrated, the major enzymes involved in the initial depolymerization have not been clearly identified. An extracellular esterase from Lentinus tigrinus and certain polymerases from Bacillus and Pseudomonas have been shown to degrade PS. It was determined that styrene monooxygenases (SMO), styrene oxide isomerase (SOI), phenylacetaldehyde dehydrogenase (PAD) and multiple enzymes of phenylacetate degradation (PAA#) could degrade PS into styrene oxide, phenylacetaldehyde, phenylacetate and phenylacetic acid (an intermediate product of TCA cycle; ).

33Many hydrolases, including lipase, esterase and keratinase, showed PET degrading ability. Ideonella sakaiensis produced two enzymes, PETase and MHETase (encoded by ISF6_4831 and ISF6_0224), hydrolyzing PET efficiently into two environmentally benign monomers, i.e., terephthalic acid (TPA) and ethylene glycol (EG; ). PETase contained a Ser-His-Asp catalytic triad at the active site, and its catalytic mechanism was revealed. Then, PETase was found have structural characteristics of lipase and cutinase, and a method for degradation of high crystallinity PET catalyzed by this enzyme was established. IsPETase variants with improved thermal stability and much higher PET degradation activities were developed. In addition, a suberinase with remarkable stability and capability to hydrolyse PET to terephthalic acid and other polymers was sourced from Streptomyces scabies. Furthermore, a dual enzyme system composed of polyester hydrolase and carboxylesterase enhanced the biocatalytic degradation of PET films. Moreover, 504 possible PET hydrolase candidate genes from databases were identified, and 349 putative PET hydrolases were detected by analyzing 108 marine and 25 terrestrial metagenomes. PET hydrolase genes were found mainly in the phylum Bacteroidetes in marine metagenomes, and in Actinobacteria and Proteobacteria in terrestrial metagenomes. Four novel PET hydrolase genes were cloned, expressed heterologously and their biochemical traits were described, moreover, two displayed thermal stability and potential application value.

34Quorum sensing (QS) refers to the cell-to-cell communication process that is mediated by the production, release, accumulation and group-wide detection of extracellular signaling molecules. These regulate biological behaviors, such as bioluminescence, secondary metabolite production and biofilm formation. Gram negative bacteria mainly rely on N-acylhomoserine lactones (AHLs) as their autoinducers, whereas Gram positive bacteria mostly use autoinduced peptides.

35QS plays an important role in the formation of bacterial biofilms. QS will be induced when planktonic microorganisms proliferate to a certain cell density on a medium, promoting more bacteria to attach, leading to a mature biofilm. It was demonstrated that the stages of bacterial biofilm formation, attachment, maturation, aggregation and dispersal, are always regulated by QS, which affects the structure of biofilms. For example, rhlI/R and lasI/R are AHL-dependent QS systems in Pseudomonas aeruginosa. Rhl system influences greatly the formation of biofilm. The las system determines the structural differences of bacterial biofilms, and exerts an important role in the irreversible adhesion phase of the film-forming process. Studies on Burkholderia cepacia, Aeromonas hydrophila, Yersinia pseudotuberculosis, Vibrio cholerae and Staphylococcus showed that QS could regulate bacterial aggregation and surface adhesion. Furthermore, QS was found to play an important role in the degradation of marine organic particles by Pantoea ananatis and Ruegeria mobilis. Also, quorum sensing is involved in marine snow, and its possible influence on production of extracellular hydrolytic enzymes in Pantoea ananatis B9.

36Although the relevant research has not yet occurred, it is reasonable to believe that QS has the potential to affect the formation and composition of the plastisphere. Studies have showed that Rhodobacteraceae occupied core populations in the plastisphere and accounted for 16.4% in bacterial biofilms of MPs in the Yangtze River Estuary, China. A high proportion of Rhodobacteraceae in the plastisphere was attributed to the conserved and widespread QS signaling molecules participating in various metabolic regulations, especially flagellum movement and biofilm formation on plastic particles. QS may help Rhodobacteraceae attach and aggregate on the surface of MPs, and inhibit other bacteria, including Gammaproteobacteria. The primary model of QS regulation to the plastisphere is shown in Figure 4. In addition, QS bacteria, which were isolated from MPs, exhibited strong biofilm-forming ability and favorable conditions for epiphytic growth. Thus, Oceanicola sp. strain D3 with QS ability was isolated from a PVC biofilm. Interestingly, bacteriostasis, algae inhibition and the dimethylsulphoniopropionate (DMSP) degradation function of QS bacteria may impact the pollution of MPs in the marine environment.

37QS has the potential to be a new way to study marine MP biofilms and their degradation. On the one hand, QS has a profound impact on the microbial communities and the succession of biofilms, and the bacteria may have an important role in regulating the process of plastisphere formation. This may not only increase QS bacterial colonization on MPs by producing extracellular polysaccharides, but also inhibit the adhesion of other bacteria by producing antibacterial materials. Conversely, QS regulates many metabolic functions of dominant bacteria and enlarges their ecological function. For example, AHLs may change the activity of extracellular hydrolases. Thus, a QS system based on AHLs may have a key role in the degradation of MPs. Moreover, bacterial interaction based on the QS network may provide a new perspective for the degradation of marine MPs. The dominant colonization and rapid sensitivity to organic substances may allow QS bacteria to be effective indicators for monitoring MP pollution in the marine environment. Consequently, understanding the plastisphere and promoting MPs degradation by QS is expected to become a new research perspective.

38Plastic pollution is a problem that needs to be solved urgently, and has gained growing public and scientific attention in recent years. In this review, the formation process and microbial community composition of plastisphere – the biofilm colonizing on plastic, the bacteria and the enzymes as well as their degrading mechanism of MPs are discussed. In particular, we clarified the potential role of QS in plastic research for the first time. This may well offer novel ideas to the study of plastic pollution control.

39Microorganisms provide a new perspective for the exploration of plastic treatment, however, research on the plastisphere still needs to be advanced. The understanding of the distribution of MPs, the microbial community structure and formation process of the plastisphere and potential degrading bacteria of MPs need to be fully explored. Future studies could be categorized mainly into three themes. Firstly, more geographical distributions of MPs and biofilms and comparisons of different materials, types of plastics and plastic area/color are needed. These studies will help form the global distribution pattern of MPs, and composition of biofilms (similarities and differences), as well as promote regional targeted MP pollution control. Studying the heterogeneity of microbial community structure in the plastisphere and biofilms will lay the foundation for exploring the metabolism and MPs degradation ability of bacteria. Secondly, more investigations are needed on the effects of single bacterial strains and communities on degradation. Methods of exploring the characteristics of materials as the basal point, optimizing degradation conditions, using bioinformatics to analyze the environmental response of relevant metabolic genes in the habitat, as well as creating high-efficiency MP degrading bacterial consortia should be undertaken. Thirdly, new molecular techniques and in-situ characterization of isolated strains are needed. Specific degradation pathways and degradation enzymes need to be found to fully develop the known non-specific pathways to metabolize plastics. In addition, the study of QS could focus on the distribution, proportion and metabolism of QS bacteria in the plastisphere, which will help deepen the understanding of plastisphere and potential degrading bacteria of MP.

40MY and X-HZ: conceptualization. XZ: writing—original draft. XZ, MY, and X-HZ: writing—review and editing. X-HZ: resources and funding acquisition. All authors contributed to the article and approved the submitted version.

41This work was funded by the Scientific and Technological Innovation Project of Laoshan Laboratory (nos. LSKJ202203200 and 2022QNLM030004-3), the National Natural Science Foundation of China (nos. 41730530 and 92251303), and the Fundamental Research Funds for the Central Universities (no. 202172002).

42The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

43All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.