EFSA (2016) and FAO (2017) both recognize that plastic debris can act as a substrate for diverse microbial communities, including pathogens, but conclude that the relevance to human health still remains unknown.
SAPEA (2019) basically does not cover microbial contamination of microplastic.
The main concern about biofilms on plastic debris is that pathogenic microorganisms and antibiotic resistance genes (ARG) can be spread long distances and to new ecological niches with potencial high impact for both the environment and human health. Another interesting health related effect of microplastics on microbial diversity is reported by Lu et al. (Lu et al., 2018a). They found significant changes in the richness and diversity of the gut microbiota in the cecums of polystyrene microplastic-treated mice, resulting in dysbiosis (Lu et al.,
2018a). These results may indicate that polystyrene microplastics could modify the gut microbiota composition in mice. The relevance of this finding may be low in the context of the levels and types of microplastics present in the environment, and overall the possible health risks of microplastics to mammalian gut microbiota is not known.
6.1 The plastisphere
Microplastics can be colonized by different types of microbial communities (Kettner et al., 2017; Oberbeckmann et al., 2018) and can thus be considered as specific niches for microbial life, commonly termed plastisphere (Keswani et al., 2016). A high diversity of microorganisms have been detected on microplastics, raising questions about the role of microplastics as a novel ecological niche for potentially pathogenic (Arias-Andres et al., 2018b; Kirstein et al., 2016) or invasive (Maso et al., 2016) microorganisms. As microplastics can be transported horizontally and vertically over long distances in aquatic systems, they might be vectors for spreading of attached pathogenic bacteria and fungi, harmful algae and invasive species (Arias-Andres et al., 2018b; Keswani et al., 2016; Kirstein et al., 2016; Maso et al., 2016).
However, the potential role of microplastics as a vector for distinct microbial assemblages or even pathogenic bacteria is hardly understood (Oberbeckmann et al., 2018). The main question is if microbial biofilms remains stable on microplastics over a prolonged period of time and various environmental conditions and whether microplastics thus could serve as a vector for potential pathogenic microorganisms. Microorganisms attached to the
microplastics can potentially also play a significant role in their degradation.
6.2 Microbial diversity
Several studies on microbial attachment to various types of microplastics have been performed. Microplastic bacterial assemblages are reported to have lower taxon richness, diversity, and evenness than those on other substrates (McCormick et al., 2016). Wu et al.
93 (Wu et al., 2019) revealed through high-througput sequencing of 16sRNA that biofilm on microplastic had an unique community structure, and suggested that microplastic is a novel microbial niche. Functional potential and taxonomic composition of plastic-associated microbes versus planktonic microbes found in the open ocean are reported (Bryant et al., 2016), and the bacteria inhabiting plastics harboured distinct metabolisms from those present in the surrounding water (Debroas et al., 2017). Furthermore, there are indications that microplastic selects for taxa that may degrade plastic polymers (e.g., Pseudomonas) and common human intestinal pathogens (e.g., Arcobacter) (McCormick et al., 2016).
Oberbeckmanet al. investigated how different in situ conditions contribute to the
composition and specificity of bacterial communities on microplastics (PS and PE vs. wooden pellets) (Oberbeckmann et al., 2018). They concluded that the surrounding environment prevailingly shapes the biofilm communities, but that some microplastic-specific assemblage factors exist.
Kesy et al. compared the taxonomic composition of the biofilms on PA and chitin and found that they did not differ (Kesy et al., 2017). No potential pathogens was detected exclusively on polyamide. However, after 7 days of incubation of the biofilms in seawater, the species richness of the PA assemblage was lower than that of the chitin assemblage (Kesy et al., 2017).
Potentially pathogenic microorganisms can actually be considered hitchhikers in plastic-associated microbial communities (Kirstein et al., 2016; Shen et al., 2019). Several studies confirms the indicated occurrence of potentially pathogenic bacteria on marine microplastics (Foulon et al., 2016; Kirstein et al., 2016), among them Vibrio spp. and Aeromonas
salmonicida (Imran et al., 2019). Wu et al. (Wu et al., 2019) detected two opportunisitic human pathogens (Pseudomonas monteilii and Ps. mendocina) and one plant pathogen (Ps.
syringae) only in the microplastic biofilm, but not in biofilms formed on natural substrates.
Furthermore, the potential human pathogens Vibrio parahaemolyticus, V. vulnificus and V. cholerae associated with floating microplastics (polyethylene, polypropylene and polystyrene) was reported from North and Baltic sea (Kirstein et al., 2016). Metabolic
pathway analysis suggested adaptations of such bacterial assemblages to the plastic surface colonization lifestyle (Jiang et al., 2018).
There are only very few studies on how microplastics affect fungal communities. However, Kettner et al. explored the diversity of fungi attached to PE and polystyrene (PS) particles in different aquatic systems and a wastewater treatment plant (Kettner et al., 2017). They found that the fungal communities on microplastics differ from the mycobiota in the surrounding water and on wood as natural substrate. Members of Chytridiomycota, Cryptomycota and Ascomycota dominated the fungal assemblages, suggesting that both parasitic and saprophytic fungi thrive in microplastic biofilms. These fungal taxa might benefit from microplastic pollution in the aquatic environment with yet unknown impacts on their worldwide distribution, as well as biodiversity and food web dynamics at large (Kettner et al., 2017).
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6.3 Formation and stability of biofilms
The development and stability of microbial biofilms in natural environments need to be explored further. Most of the research on these topics have so far only been performed on bacterial biofilm formation after short-term exposure or on floating plastic. However, in a study of bacterial and fungal communities on polyethylene plastic sheets and dolly ropes during long-term exposure on the seafloor, none of the typical features of a late stage biofilm were displayed (De Tender et al., 2017). Foulon et al. (Foulon et al., 2016) observed a longer bacterial attachment (6 d) on irregular microparticles compared to smooth particles (<10 h), but complete decolonization of all particles eventually occurred. These results indicate that biofilm formation is severely hampered in the natural environment where most plastic debris accumulates.
6.4 Antibiotic resistance
Antibiotic resistance of bacteria can be acquired from other bacteria through horizontal gene transfer or through mutations of antibiotic targets. Biofilms create an environment that protect bacteria from effects of antibiotics. Therefore, biofilm formation is considered an antibiotic resistance mechanism in bacteria (Imran et al., 2019).Multiple resistance against antibiotics belonging to cephalosporins, quinolones and beta-lactams were demonstrated in bacteria from a macro-plastic piece stranded on the shores in King George Island (South Shetlands, Antarctica) (Lagana et al., 2019). Furthermore, metagenomic analyses have revealed microplastic with broad -spectrum and distinctive resistome (Wu et al., 2019).
Plastic can be transported long distances, and several studies have thus suggested plastics as possible vectors for the spread of antibiotic resistance (Arias-Andres et al., 2018b).
Heavy colonization of microplastics by bacteria commonly associated with antibiotic resistance made Oberbeckman et al. suggest microplastics as a possible hotspot for horizontal gene transfer (Oberbeckmann et al., 2018). This theory is supported by Arias-Andres et al. (Arias-Andres et al., 2018b), who demonstrated increased frequency of plasmid transfer in bacteria associated with microplastics compared to free-living bacteria or bacteria in natural aggregates. Furthermore, it has been demonstrated that microplastics in an aquatic environment can adsorb antibiotics (sulfadiazine, ciprofloxacin, amoxicillin, trimethoprim and tetracycline) on their surfaces (Imran et al., 2019).
The plastisphere may thus contribute to the spread of antibiotic resistance, which
consequently could affect the diversity and ecology of aquatic microbial communities on a global scale and consequently also long-range dispersion and entry into food chain (Arias-Andres et al., 2018b) and (Imran et al., 2019).
6.5 Wastewater and sewage sludge
The composition of microplastic-attached bacterial assemblages in domestic wastewater have been shown to differ from that of assemblages in water and sediment and supports domestic wastewater as a point source of microplastic (e.g., gastrointestinal taxa) (Hoellein
95 et al., 2017). As microplastic particles promote persistence of typical indicators of microbial anthropogenic pollution in natural waters, their removal from treated wastewater should consequently be prioritised (Eckert et al., 2018).
6.6 Biodegradation
The microbial biofilms can also have a significant role in biodegradation of microplastics.
Both bacteria and fungi have been found to form efficient consortiums for degrading weathered plastics in seawater (Morohoshi et al., 2018; Paco et al., 2017; Syranidou et al., 2017) and soil (Huerta Lwanga et al., 2018).
6.7 Carbon dynamics
Functional differences between microplastic-associated and pelagic microorganisms in different freshwater lake types have been demonstrated (Arias-Andres et al., 2018a)b).
Consequently, increasing microplastic pollution has the potential to globally impact carbon dynamics of pelagic environments by altering heterotrophic activities (Arias-Andres et al., 2018a)b).
6.8 Summary
EFSA (2016) and FAO (2017) both recognized that plastic debris can act as a substrate for diverse microbial communities, including pathogens, but concluded that the relevance to human health still remains unknown. Microbial contamination of microplastic was basically not covered by SAPEA (2019).
VKM found:
Microplastics biofilms have unique microbial community structures compared to the surrounding environments.
Microplastics can serve as vectors for microorganisms that are potentially pathogenic to humans, animals or plants.
Opportunistic human pathogens have been found to be enriched in microplastic biofilm.
Microplastics biofilms are considered possible hotspots for horizontal gene transfer.
Several studies have suggested that the plastisphere may contribute to the spread of antibiotic resistance.
VKM concludes that the available information on microplastic biofilms does not provide sufficient basis to characterize potential effects on human health.
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