Microplastics and the gut microbiome: How chronically exposed species may suffer from gut dysbiosis

Marine Pollution Bulletin 143 (2019) 193–203

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Review

Microplastics and the gut microbiome: How chronically exposed species may suffer from gut dysbiosis

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Gloria Fackelmann , Simone Sommer Institute of Evolutionary Ecology and Conservation Genomics, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany

A R T I C LE I N FO

A B S T R A C T

Keywords: Microplastics Pollution Gut microbiome Dysbiosis Wildlife health

As small pieces of plastics known as microplastics pollute even the remotest parts of Earth, research currently focuses on unveiling how this pollution may affect biota. Despite increasing awareness, one potentially major consequence of chronic exposure to microplastics has been largely neglected: the impact of the disruption of the symbiosis between host and the natural community and abundance pattern of the gut microbiota. This so-called dysbiosis might be caused by the consumption of microplastics, associated mechanical disruption within the gastrointestinal tract, the ingestion of foreign and potentially pathogenic bacteria, as well as chemicals, which make-up or adhere to microplastics. Dysbiosis may interfere with the host immune system and trigger the onset of (chronic) diseases, promote pathogenic infections, and alter the gene capacity and expression of gut microbiota. We summarize how chronically exposed species may suffer from microplastics-induced gut dysbiosis, deteriorating host health, and highlight corresponding future directions of research.

1. Introduction Ever since the mass-productions of plastics, they have littered the environment (Barnes et al., 2009; Moore, 2008). Plastics that break down into smaller pieces are known as microplastics (< 5 mm; Moore, 2008; Thompson et al., 2009a; Hohenblum et al., 2015) and have been found in all corners and crevices of the Earth, from polar ice (Obbard et al., 2014), to the deep sea (Woodall et al., 2014), and in human lungs (Prata, 2018) and feces (Liebmann et al., 2018). The great majority of microplastic pollution originates from land (Andrady, 2011), where microplastics end up in wastewater treatment plants (Cieślik et al., 2015) and are not fully filtered out before they escape to the sea and eventually to the ocean (Horton et al., 2017a; Rochman et al., 2015). Research began by exploring the extent of microplastic pollution (Ryan, 2015): Where can we find microplastics in the environment? Which animals harbor microplastics? Can microplastics be transferred up the food chain? Recently, interests have shifted towards understanding which impacts microplastics may have on the organisms they are found in and around. These investigations are manifold and diverse, ranging from assessing the physical impacts of microplastic presence in the gastrointestinal tract (Kramm and Völker, 2018; Possatto et al., 2011) and chemical evaluations (Pittura et al., 2018), to determining how fitness of organisms that come into contact with these pollutants is impacted (Besseling et al., 2013; Zhu et al., 2018; Zhu et al., 2018a).

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However, not enough research has shifted from observing presence/ absence of plastics to uncovering the biological fate of impacted organisms, especially in non-model, vertebrate species, which are often difficult to examine under a microscope and observe around the clock. In this review, we aim to shine the spotlight on an overlooked, yet critical aspect in (wildlife) health that we believe suffers greatly under the influence of microplastics: the gut microbiome. We will pave the way to understand the history of microplastics, how and where they form, which known impacts microplastics have on wildlife health and how this evidence points towards the gut microbiome as a hidden victim of microplastic pollution. 1.1. From plastics to microplastics: history and environmental accumulation During the first half of the twentieth century, the synthesis of a score of new polymer classes marked the birth of the plastic age (Andrady and Neal, 2009; Thompson et al., 2009b; Zalasiewicz et al., 2016). However, it took several decades until, in the 1970s, the issue of plastic pollution in the oceans began to be reported in scientific literature (Azzarello and Van-Vleet, 1987; Carpenter et al., 1972; Carpenter and Smith, 1972; Jambeck et al., 2015). Soon thereafter, seabird guts were found to be polluted with plastic debris (Laist, 1987), reports of wildlife entanglement emerged (Derraik, 2002), and initial concerns were raised about chemicals leaching from plastic to wildlife (Ryan et al.,

Corresponding author. E-mail address: [email protected] (G. Fackelmann).

https://doi.org/10.1016/j.marpolbul.2019.04.030 Received 11 February 2019; Received in revised form 10 April 2019; Accepted 11 April 2019 Available online 28 April 2019 0025-326X/

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oceans are not the only collecting sites, as microplastics have also been found in freshwater bodies – even in rivers that originate in the remote Tibet Plateau (Jiang et al., 2019) – and in diverse freshwater sediments around the globe (Alam et al., 2019; Bordós et al., 2019; Driedger et al., 2015; Mani et al., 2015; Peng et al., 2018; Shruti et al., 2019; Turner et al., 2019). Growing evidence suggests microfibers are in the air around us (Prata, 2018), in our offices (Dris et al., 2017), and outside in the streets (Dris et al., 2016). In fact, plastic pollution has become so ubiquitous and innumerable in scope and is so permanent in nature, that is has been proposed as an indicator for the Anthropocene (Zalasiewicz et al., 2016). Although we have become familiar with images of plastic pollution at sea, the sources of this pollution most often originate from land, accounting for 80% of plastic pollution (Andrady, 2011; Duis and Coors, 2016). Litter caused by human activity and recreation, debris from landfills, or synthetic fibers released into wastewaters from washing clothes may all ultimately travel along freshwater bodies to collect in seas and oceans (Dris et al., 2016; Herzke et al., 2016; Horton et al., 2017b; Imhof et al., 2013). A single garment, which nowadays often contains synthetic fibers, can release upwards of 1900 fibers per wash (Browne et al., 2011), some of which may be too small to be filtered directly out of the washing machine drainage (Hernandez et al., 2017). Microbeads are microplastics used in cosmetics and personal care products as exfoliants and in toothpaste (Xanthos and Walker, 2017). These single-use beads accounted for 4130 tons of microplastic particles in the European Union, Norway, and Switzerland in 2012 (Duis and Coors, 2016). It has been estimated that eight trillion microbeads are released into the aquatic environment every day in the United States alone (Rochman et al., 2015). This is enough to cover over 300 tennis courts every day (Rochman et al., 2015). Marine plastic debris may also originate directly from the sea from the spillage of virgin plastic pellets during ocean transports; the fishing industry, which may lose or purposefully abandon fishing gear whilst at sea (Andrady, 2011); or from equipment used in mussel farming and aquaculture (Hinojosa and Thiel, 2009). No matter through which channel plastics enter the environment, humans are always the polluters and thus carry the responsibility to study which impacts this pollution has on the environment, organisms, and even themselves.

1988; Thompson et al., 2009b). At the same time, the production of modern plastics has been thriving, with 348 million tons of plastics having been produced in 2017 (PlasticsEurope (PEMRG), 2018), a near sevenfold increase from 50 tons in 1976 (PlasticsEurope (PEMRG) / Consultic, 2018). This upward trend is far from over and forecasts predict a steady growth in the production of primary plastics (PlasticsEurope (PEMRG), 2018). The reasons for the endurance of the plastic age are understandable: plastics are inexpensive and lightweight, yet strong and robust (Barnes et al., 2009; Thompson et al., 2009a). Consequently, they have been incorporated into many aspects of our lives, ranging from clothing and food packaging to building materials and transportation. However, the very properties that make plastics desirable pose a myriad of problems to the environment (Pruter, 1987; Ryan, 2015). Plastics are non-biodegradable, meaning most of the plastic produced in the past still persists in the environment today (Geyer et al., 2017; Zalasiewicz et al., 2016) and the plastic we manufacture daily will continue to exist for hundreds or thousands of years to come (Barnes et al., 2009; Holland et al., 2016). Plastics can fragment into smaller pieces and are referred to as microplastics when particles are smaller than 5 mm (Hohenblum et al., 2015; Moore, 2008; Thompson et al., 2009a). They are differentiated by their mode of formation and can thus be termed primary or secondary microplastics. Primary microplastics are deliberately manufactured plastic pellets designed for further production processes of plastics, as abrasives for industrial applications, or for use in cosmetics (Hohenblum et al., 2015; Rillig, 2012). Secondary microplastics are formed by the breakdown of mesoplastics (plastic particles between 5 and 20 mm; Besseling et al., 2015; Eerkes-Medrano et al., 2015) or larger plastic items by chemical or mechanical processes (Hanvey et al., 2017). UV radiation from sunlight may turn plastics brittle, whilst wave action and turbulence further contribute to the fragmentation of plastics (Horton et al., 2017b; Moore, 2008). These non-biodegradable particles (Thompson et al., 2004) have been shown to accumulate in marine environments (Law and Thompson, 2014), freshwater habitats, and terrestrial soils (Castañeda et al., 2014; Driedger et al., 2015). The application of wastewater sludge and organic fertilizers to agricultural fields accounts for direct microplastic pollution of soil and potential, indirect pollution of aquatic systems due to runoff (Cieślik et al., 2015; Horton et al., 2017a; Rochman et al., 2015; Weithmann et al., 2018). Although freshwater systems are also impacted by runoff (Horton et al., 2017a), historically, research has been greatly centered around microplastic pollution in marine habitats, with less focus attributed to freshwater and terrestrial ecosystems (Hohenblum et al., 2015; Horton et al., 2017b). However, as publications unveiled microplastic pollution to be pervasive in freshwater environments as well (Castañeda et al., 2014; Driedger et al., 2015; Imhof et al., 2013; Lechner et al., 2014; Mani et al., 2015), research focus has shifted to include microplastic pollution in non-marine environments (Huerta Lwanga et al., 2018; Triebskorn et al., 2018; Weithmann et al., 2018). Microplastics have become ubiquitous in the marine environment (Cole et al., 2011; Critchell et al., 2019; Forrest et al., 2019; Ivar do Sul and Costa, 2014), where they have received great media attention. Eriksen et al. (2014) estimated that 35,500 tons of microplastics are afloat at sea. However, a recent study conducted by Hurley et al. (2018) suggests that this figure grossly underestimates the vast amount of microplastics in the world's oceans. Plastic pollution has been found concentrated in gyres (Critchell et al., 2019; Eriksen et al., 2013; Goldstein et al., 2012), on the sea floor (Pham et al., 2014), or along coastlines (Chubarenko and Stepanova, 2017; Martins and Sobral, 2011; Nel and Froneman, 2015), where they have become an eyesore and constitute the most common pollutant of beach habitats (Bancin et al., 2019; Moore, 2008). Even the remotest of areas, ranging from the deep sea (Courtene-Jones et al., 2019; Kanhai et al., 2019; Woodall et al., 2014) to the Arctic Sea ice (Obbard et al., 2014) and Arctic snow (Bergmann et al., 2018) have not been spared. However, the world's

2. Evidence of microplastic ingestion and impacts A wide spectrum of animals from the wild has been found to ingest microplastics (Besseling et al., 2015; Desforges et al., 2015; Goldstein and Goodwin, 2013; Holland et al., 2016; Lusher et al., 2015; Pham et al., 2017; Reynolds and Ryan, 2018), which may be transferred trophically (Nelms et al., 2018; Setälä et al., 2014). Animals from low trophic levels, such as zooplankton – who appear to mistake microplastics for food – not only ingest microplastics in the wild (Desforges et al., 2015), but are able to transfer these particles to the next trophic level as well (Setälä et al., 2014). From small to large, microplastics are ingested by filter-feeding gooseneck barnacles (Lepas spp.; Goldstein and Goodwin, 2013) and have been found in the intestines of one of the largest filter-feeders in the world: the humpback whale (Megaptera novaeangliae; Besseling et al., 2015). Even the rare, oceanic cetacean True's beaked whale (Mesoplodon mirus), which forages in the deep ocean, was found to harbor microplastic debris (Lusher et al., 2015). Microplastic particles were also uncovered in 83% of oceanic-stage loggerheads (Caretta caretta) collected off the North Atlantic subtropical gyre (Pham et al., 2017). The fate of microplastics after ingestion encompasses accumulation, translocation, and finally egestion – processes, which are heavily impacted by the size of these particles (Browne et al., 2008; EFSA CONTAM Panel, 2016). In mice, toxicokinetics and toxicodynamics were largely impacted by microplastic size, whereby smaller fragments (5 μm) showed a greater uptake rate constant and a higher steady-state bioaccumulation factor than the larger microplastics tested (20 μm; 194

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Mechanical Disruption

Pathogen Vector

● Malnutrition ● Inflammation ● Nanoplastics cross biological barriers

● Hitchhiking, non-core bacteria ● Potential pathogens ● Competition for limited resources

Inmmune system

Chemical Disturbances ● Endocrine disruptors ● Environmental pollutants

Direct

Host hormone signaling

Fig. 1. Conceptual model of the possible impact points of microplastic ingestion on the gut microbiome and the mechanisms which could lead to gut dysbiosis. Microplastics can 1) cause mechanical disruption, leading to malnourished individuals, inflammation of the gastrointestinal tract, and the breakdown of microplastics to form nanoplastics able to cross biological barriers; 2) act as a vector for potential pathogens and foreign, non-core bacteria, leading to competition for limited resources with resident bacteria; 3) harbor chemicals known to disrupt the endocrine system and environmental chemicals such as persistent organic pollutants (POPs), polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), and dichlorodiphenyltrichloroethane (DDT). These factors may either directly or indirectly induce gut dysbiosis, the latter of which may involve the immune system, activated by inflammatory processes or pathogens; or host hormone signaling, engaged by endocrine disruptors. The disruption of the symbiosis between host and gut microbiome may trigger the onset of (chronic) diseases, deteriorate host health, promote pathogenic infections, and alter the gene capacity and expression of gut microbiota, leading to consequences not yet fathomed.

Indirect

(Chronic) diseases ● Deteriorated host ● Pathogenic infections ● Altered gene capacity and expression health

if microplastics impact the health of various animals, the mechanisms behind these impacts still require further attention (Anbumani and Kakkar, 2018; Ogonowski et al., 2017; Wang et al., 2019). It has been argued that small plastic particles themselves are hazardous (Rochman, 2013) and should urgently be classified as such, in order to reduce pollution and any possible negative health risks these polymers and their associated chemicals may pose (Rochman et al., 2013a). Considering the fact that microplastics have been detected in tap water from around the globe (Kosuth et al., 2017), in bottled water (Schymanski et al., 2018), in human lung tissue (Prata, 2018), and in human feces (Liebmann et al., 2018), evidence suggests that humans are already chronically exposed to these pollutants. In the following sections, we have categorized some of the effects of microplastics to outline how they may contribute to gut dysbiosis.

Yang et al., 2019). Similarly, differential microplastic egestion based on size was observed in the earthworm (Lumbricus terrestris), where greater proportions of smaller plastics were retained, as opposed to larger plastics, which were more likely to be egested (Huerta Lwanga et al., 2016). Whilst Cole et al. (2013) found the retention time of microplastics in zooplankton to be within the scope of a few hours, shore crabs (Carcinus maenas) exhibited retention times of up to 14 days after microplastics were ingested (Watts et al., 2014). Although microplastics are most likely to accumulate in the gut (Browne et al., 2008), translocation of microplastics to other tissues such as the liver and kidneys, the circulatory system, and the gills and accumulation therein have also been observed (Browne et al., 2008; Collard et al., 2017; Deng et al., 2017; Lu et al., 2016), although the underlying mechanisms remain to be elucidated (Deng et al., 2017; Wang et al., 2016). However, these processes depend heavily on particle size, whereby immune responses, such as inflammation within the gut are more likely to occur (EFSA CONTAM Panel, 2016). The effects of microplastic ingestion are manifold and evidence suggests that these include – but are not limited to – the following: alteration of feeding activity (Besseling et al., 2013; Cole et al., 2015), reduction of food assimilation efficiency (Blarer and Burkhardt-Holm, 2016), stunted growth (Lo and Chan, 2018; Welden and Cowie, 2016), negative impacts on reproduction (Cole et al., 2015; Ju et al., 2019; Lee et al., 2013; Ogonowski et al., 2016; Sussarellu et al., 2016), altered gene expression (Lagarde et al., 2016; Rochman et al., 2014), oxidative stress (Chen et al., 2017; Deng et al., 2017; Qiao et al., 2019), and neurotoxicity (Guilhermino et al., 2017; Song et al., 2018). The public has also become aware of the problems associated with plastic ingestion, as it often subjected to unsettling news stories of marine wildlife found to harbor vast amounts of plastics (Ellis-Petersen, 2019; Parker, 2018; Zachos, 2018). Although many studies have focused on assessing

2.1. Mechanical disruption The ingestion of microplastics may cause mechanical damage to the digestive tract and malnutrition (Kramm and Völker, 2018; Possatto et al., 2011). Microplastics were found to inhibit food assimilation (Blarer and Burkhardt-Holm, 2016; Straub et al., 2017), reduce body size and weight (Wright et al., 2013a), and negatively impact growth and thus reproductive fitness (Au et al., 2015; Besseling et al., 2014). The digestive tract may be subjected to abrasions, perforations, or even blockage due to microplastics (Wright et al., 2013b). Thus, the shape of microplastics could also play a role in the degree of damage dealt to the intestinal epithelium, as more rigid particles are more likely to perforate this important barrier than rounder and smoother fragments. The gut mucosal lining is paramount in upholding host health, since it is the first line of defense against pathogens in host immunity and prevents bacterial translocation (Pelaseyed et al., 2014; Saltzman et al., 2018; 195

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Pelaseyed et al., 2014). The dominant intestinal epithelial cells in the small intestine, Paneth cells, secrete antimicrobial proteins (AMPs), some of which, such as α-defensins, can alter the community composition of bacteria within the lumen, whilst others, such as RegIIIγ, exert their antimicrobial forces on bacteria close to the epithelial barrier (Hooper et al., 2012; Shi et al., 2017). The immune system also employs dendritic cells which are able to extend from the lamina propria, basolateral of the gut epithelium, into the gut lumen to identify and remove pathogenic bacteria. This can stimulate the differentiation towards regulatory T cells (Tregs), which play an essential role in immune tolerance (Gonçalves et al., 2018; Shi et al., 2017). In turn, the gut microbiome's influence on the immune system largely involves shortchain fatty acids (SCFAs), which are produced by some of the most abundant commensal bacteria in the gut, namely by Bacteroidetes and Firmicutes, during the fermentation of fiber and encompass, inter alia, butyrate, acetate, and propionate (Gonçalves et al., 2018; Lazar et al., 2018; Samuelson et al., 2015). SCFAs are able to influence the host immune system not only locally by regulating Treg differentiation, gene expression, and metabolism in B cells and immunoglobulin A (IgA) production, but also systemically by translocating to the circulatory system (Gonçalves et al., 2018; Samuelson et al., 2015). Commensal bacteria, such as those belonging to Clostridium clusters IV and XIVa and Bacteroides fragilis, further expand Treg differentiation via the production of polysaccharide A (PSA; Gonçalves et al., 2018; Michel et al., 2018; Samuelson et al., 2015; Shi et al., 2017). Faced with the fact that the gut microbiome influences the immune system, which in turn regulates gut microbial community composition to ensure homeostasis with its symbionts (Hooper et al., 2012), microplastics may have two leverage points: If microplastics interfere with gut microbiota, this may impact host immunity, and if microplastics interfere with host immunity, this could, in turn, cause shifts in the gut microbial community within the organism (Fig. 1).

Shi et al., 2017). Microplastics are fragmented into even smaller particles or nanoplastics in the environment (Mattsson et al., 2015) or perhaps even from within the digestive tract (Dawson et al., 2018). At such sizes, these pollutant-laden particles could cross biological barriers (da Costa et al., 2016), with evidence already pointing towards immune and inflammatory responses (Deng et al., 2017; Lehner et al., 2019) as well as re-structuring of gut epithelial villi (Mahler et al., 2012). This raises the question of how not only the host organism may respond to these stressors, but also how its gut microbial symbionts may be impacted (Fig. 1). Increased phagocytic activity of immune cells following microplastic consumption has been observed, further pointing towards costly immune-driven inflammation processes (Von Moos et al., 2012; Wright et al., 2013a). Such processes are often associated with shifts in gut bacterial communities (so-called dysbiosis), possibly because the oxidative state triggered by inflammation promotes the growth of bacterial taxa able to cope with this hostile host environment, such as Actinobacteria and Proteobacteria (Ni et al., 2017). A further mechanism which could drive shifts in gut bacterial communities could be the inflammatory-driven rise in anaerobic respiratory terminal electron acceptors, which would favor the growth of (facultatively) anaerobic taxa, such as Enterobacteriaceae, which have been observed to grow rampantly during inflammation (Winter and Bäumler, 2014). Ultimately, the stressors present in an inflammatory gut could differentially select for certain bacteria and induce dysbiosis, thus facilitating the onset of diseases (Dalal and Chang, 2014; Holmes et al., 2011; Nicholson et al., 2012). Furthermore, due to the additional space microplastic particles occupy within the digestive tract, animals can suffer from a diminished sensation to feed, associated malnutrition, and may ultimately starve to death (Kramm and Völker, 2018; Possatto et al., 2011). The gut microbiome is shaped by diet: Just as certain substrates favor the growth of certain bacteria, so too do certain foods favor some bacteria over others (Voreades et al., 2014). It is recognized that the gut microbiome coevolved with its host to create a symbiotic relationship, whereby the gut community inhabits a niche with stable and favorable conditions, whilst the host benefits from access to nutrients and metabolic pathways made available by microbes and which exceed the host's own capacity (Lazar et al., 2018; Shapira, 2016; Shi et al., 2017; Wu and Wang, 2018). If a host's diet is impaired by microplastic particles, not only may the host suffer from malnutrition, but its gut symbionts will also be afflicted by a lack of nutrients and substrate necessary to feed the community, potentially leading to shifts in gut community structure. Consequently, symbiotic bacteria may not be able to provide the same functions, especially considering that microbial gene expression is also linked to host diet (Ercolini and Fogliano, 2018). Furthermore, research in humans has revealed that the gut microbiome in adults is able to rapidly shift its community structure in response to dietary changes and then quickly regain its original composition unless dietary changes are chronic (Voreades et al., 2014). In infants, on the other hand, the gut microbiome shows greater fluctuations and the diet to which it is exposed likely shapes its adult composition (Goldsmith et al., 2015; Laursen et al., 2016). Therefore, it seems probable that a diet consisting of microplastics from infancy onwards and throughout the life history of an impacted individual will alter the composition of the gut microbiome. As mentioned above, mechanical disruption of the digestive tract and malnutrition are factors found to affect both the gut microbiome and the immune system – two players whose interactions are tight-knit and who constantly influence each other (Kau et al., 2011; Michel et al., 2018; Wright et al., 2013a). The immune system upholds the homeostasis between the host and its gut microbes by maintaining a mucosal barrier between the microbes and the intestinal epithelial cells (stratification) and by anatomically separating the microbes in the gut lumen from the systemic immune system (compartmentalization), utilizing the epithelial cell barrier and its tight junctions (Hooper et al., 2012;

2.2. Pathogen vector It has already been demonstrated that microbes can enter the gut through dietary items and alter its composition (David et al., 2013), thus highlighting the possibility that microplastics may also serve as vectors for potential pathogens to enter the digestive tract of wild animals that ingest these pollutants (Wagner et al., 2014; Fig. 1). Pathogenic bacteria are able to cause dysbiosis of the gut microbial community and these microbes may also hitchhike on microplastics (Lupp et al., 2007). Not all invaders will be able to survive the defenses put up by host microbes, however, some may by beating their competition through optimal resource usage, avoiding competition by utilizing nutrients that host symbionts cannot, or eliminating competition by inducing inflammation in the host to reduce the number of symbiotic microbes (Kamada et al., 2013). Recently, the microbial community which adheres to and inhabits microplastics has been coined the plastisphere (Zettler et al., 2013) and can be seen as the microbiome of microplastics. Bacteria belonging to the genus Vibrio, including the human pathogen Vibrio parahaemolyticus, have been identified as members of the plastisphere of the North and Baltic Sea (Kirstein et al., 2016). Species belonging to the Vibrio genus are known to cause not only gastroenteritis, but also cholera and septicemia in humans, and infection is usually due to ingestion of undercooked food, such as seafood and shellfish (Daniels et al., 2000; Oliver, 2005). Consequently, ingestion of microplastics and its associated pathogenic bacteria could both directly and indirectly, via dysbiosis, cause diseases. The latter may be especially true if ingestion of non-core gut bacteria associated with microplastics, which are distinctly different than the bacteria from the surrounding environment to which wild animals are accustomed (Harrison et al., 2014; Zettler et al., 2013), is chronic throughout the life of an affected individual. Ingested bacteria, even if they are not pathogenic, may influence gut microbial community composition by creating competition for resources within 196

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dichlorodiphenyltrichloroethane (DDT), which are highly toxic, carcinogenic environmental pollutants, can be adsorbed by microplastics due to the hydrophobic nature of plastics (Andrady, 2011; Endo et al., 2005), meaning microplastics may carry an organismal-vector effect, whereby pollutants gain passage to the gastrointestinal tract of organisms (Syberg et al., 2015). Once inside the gut, the bioavailability of these pollutants depends on various factors such as fugacity gradient, duration of contact, and desorption capacity, which can be influenced by particle size, shape, weathering stage, biofilms, polymer type, and surface polarity (Beckingham and Ghosh, 2017; Holmes et al., 2012; Khan et al., 2015; Koelmans, 2015; Lead et al., 2018). Many of the aforementioned microplastics-associated environmental pollutants cause gut dysbiosis and carry negative health impacts ranging from immune and liver toxicity to obesity and diabetes (Jin et al., 2017; Fig. 1). Some studies have pointed towards microplastics as an accumulator and a possible vector for chemicals, making pollutants available to organisms that ingest microplastics (Brennecke et al., 2016; Browne et al., 2013; Chua et al., 2014; Mato et al., 2001; Pittura et al., 2018), even going so far as to cause liver toxicity and alter gene expression in model fish species, pointing towards the possibility that microplastic pollution in the environment may have already reached concentrations that can interfere with the endocrine system in wild animals (Rochman et al., 2013b, 2014). The implications that microplastics may harbor on their surface an ecocorona or a multi-layered shell of molecules, which could carry a Trojan horse effect for pollutants nested within these layers, hints at the complex nature of microplastics (Galloway et al., 2017). These particles are dynamic and do not exist in a steady state in the natural environment, as they are subjected to weathering conditions that change their surface area to volume ratio, form cracks and niches, and turn plastic brittle (Andrady, 2017; Galloway et al., 2017). Adding to the complexity is the fact that associated pollutants are not isolated from one another in the environment, so the possible combined effects of everchanging microplastics and their associated toxic compounds, which have been seen as a cause of concern and still constitutes a knowledge gap within the scientific community (Gallo et al., 2018), on the gut microbiome of wild animals remains to be uncovered. This also explains why the relative importance of microplastics as vectors and drivers of bioaccumulation of hydrophobic organic chemicals – including additives – when compared to other particles has been controversially discussed (Bakir et al., 2016; Diepens and Koelmans, 2018; Koelmans et al., 2016).

the gut (Fig. 1). The long lifespan and lightweight properties of microplastics enable these particles to travel long distances (AmaralZettler et al., 2015) and act as long-lasting vectors for the plastisphere community (Zettler et al., 2013). Considering the potentially pathogenic bacteria that may live on microplastics together with the wide range of animals, including those destined for human consumption, which ingests these particles, human-driven plastic pollution may come full circle to ultimately pose health risks to the initial polluters: mankind. 2.3. Chemical disturbances Microplastics may cause harm to the animals that ingest these particles because of chemical disturbances caused by environmental chemicals that are attracted to plastics and by components of plastics and additives, most notably bisphenol A (BPA) and plasticizers, which are known to exert a wide variety of biological effects (Teuten et al., 2009; Welshons et al., 2006). Bisphenol A is a commonly used starting material for the synthesis of plastics designed for food and beverage storage and a known endocrine disrupter, able to leach from plastics to the environment (Alonso-Magdalena et al., 2012; Erler and Novak, 2010). Studies in rats have suggested that exposure to BPA, even under the tolerable daily intake for humans, can induce permanent changes in the central nervous system (Kubo et al., 2003). Following the evaluation of scientific evidence stating BPA's hormonal effects and under consideration of this chemical's ability to leach from food and beverage packaging, Canada and the European Union banned the use of BPA in baby bottles (Environment and Climate Change Canada, 2018; The European Union, 2018). A similar ban was also introduced in the United States of America (Food and Drug Administration, 2013). Plasticizers added to plastics are intended to raise their flexibility and malleability, and although they are integrated between the polymer chains in plastics, they are not bound to the polymer matrix and are not particularly stable (Oehlmann et al., 2009). Thus, plasticizers can become available for exposure, meaning they can leach into the surrounding environment (Oehlmann et al., 2009). The “new car smell” is often attributed to plasticizers or their degradation products (Farag, 2015). Common endocrine disruptors and plasticizers are phthalates (De Toni et al., 2017), which have been shown to possess estrogenic activity (Diamanti-Kandarakis et al., 2009). Up to 40% of soft polyvinyl chloride (PVC) may be comprised of the plasticizer di(2-ethylhexyl) phthalate (DEHP; Koch et al., 2006), which is known to have toxic impacts on reproductive organs, the heart, liver, kidneys, and lungs, even at low exposures (Tickner et al., 2001). DEHP and its primary metabolite MEHP (mono(2-ethylhexyl) phthalate) are the most abundant phthalates detected in the blubber of four wild cetacean species, including the fin whale (Balaenoptera physalus) and bottlenose dolphin (Tursiops truncates; Baini et al., 2017). Due to the fact that gut bacteria are affected by hormones secreted by their host because they possess the necessary hormone receptors (Hughes and Sperandio, 2008; Neuman et al., 2015) and given that certain plasticizers are known endocrine disruptors (De Toni et al., 2017; Diamanti-Kandarakis et al., 2009), consumption of microplastics could impact gut microbes either directly, by the binding of plasticizers to microbial hormone receptors, or indirectly, by interfering with host hormone signaling (Fig. 1). Ways in which host hormones influence gut bacteria encompass, inter alia, regulation of bacterial growth and virulence (Neuman et al., 2015). Since the gut microbiome is not only influenced by host hormones but also influences these hormones (Neuman et al., 2015), alterations in the growth and/or virulence of gut bacteria could cause changes in enteroendocrine signaling and, ultimately, have unknown, downstream impacts on the health of the countless animals dependent on their holobionts. Moreover, hydrophobic chemicals or persistent organic pollutants (POPs) found in the surrounding environment, such as polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), and

3. Linking microplastic ingestion to gut microbiome dysbiosis and health Taken together, the question arises of how the gut microbiome of microplastic consumers copes with this lingering and ever-present cocktail of foreign bacteria, mechanical disturbances, and chemicals. Dysbiosis of the gut microbiome might be the missing link between microplastic ingestion and host health (Fig. 1). The gut microbiome is now known to provide essential functions to its host and play a major role as a defender of good health (Montalban-Arques et al., 2015). Recent research emphasizes the functional importance of gut microbial communities in the development and performance of the immune system, in addition to its well-known, central role in food digestion and synthesis of vital nutrients (Hollister et al., 2014; Kau et al., 2011; LeBlanc et al., 2013). The gut microbiome is shaped by intrinsic host traits and extrinsic environmental factors, influencing host-bacteria relationships (Amato, 2013; Amato et al., 2013; Menke et al., 2014; Wasimuddin et al., 2017). Changes in gut microbial community composition and abundance pattern beyond the natural variation can cause functional dysbiosis, leading to an increased susceptibility to pathogenic infections or the development of chronic diseases (Turnbaugh et al., 2007; McKenna et al., 2008; Looft et al., 2012; Ellis et al., 2013). Thus, it comes as no surprise that evidence has been accumulating 197

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interactions between essential gut bacteria, which constitute the core microbiome, and potential pathogens. It has been proposed that not all stressors may follow a simple pattern of always causing either a decrease or increase in beta diversity, but may instead have stochastic effects on gut microbial community compositions. This pattern, or rather lack thereof, has been coined the Anna Karenina principle, which states that whilst healthy microbiomes are alike in composition, microbiomes in dysbiosis are all unlike from one another and exhibit no uniform pattern of dissimilarity (Zaneveld et al., 2017). Whilst the Anna Karenina principle may stand for field studies, laboratory experiments are limited by the degree to which they can replicate real-life scenarios. Bacterial biofilm communities on microplastics appear to be polymer-specific (Frère et al., 2018), meaning that laboratory experiments using one polymer or another, instead of mixtures of several polymers as appear in the environment, will favor the growth of a certain bacterial community structure. Should bacterial communities be polymer-specific and if environmental microplastic mixtures are comprised of differing and ever-changing polymer proportions, then more weight is lent to the argument that gut dysbiosis driven by microplastic ingestion may follow the Anna Karenina principle. Preliminary findings point towards the possibility that the relative abundance of certain bacterial genera differ depending on if microplastic particles are pristine or polluted (Rosato et al., 2018). In this study, microplastics polluted with PCBs harbored a greater proportion of PCB-transforming (by way of reductive dechlorination) bacteria. Considering that microplastics can be rapidly colonized (Harrison et al., 2014; Michels et al., 2018), it is safe to assume that wild animals are more likely to be exposed to non-pristine particles in the environment. Another study found that hydrocarbon-degrading genera colonized microplastics (Harrison et al., 2014). This brings with it the possibility that animals which ingest microplastics also take in bacteria able to break down plastics or to partially detoxify the chemicals associated with them. This raises the question if the relative abundance of such genera increases with increasing microplastic ingestion so as to alter the core microbiome significantly when compared to animals not chronically exposed to these pollutants or if these genera can be found only in low abundances, thus appearing to maintain the integrity of the core microbiome. However, it is not only the gut microbiome that should be assessed but also its hologenome, or the sum of all genes possessed by the microbiome. Microplastics have been flagged as potential hot spots where bacteria may horizontally transfer antibiotic resistance genes due to their heightened readiness to acquire plasmids on the surface of microplastics as opposed to in open waters (Arias-Andres et al., 2018). Therefore, to truly assess if the gut microbiome is impacted by microplastics, is it not enough to simply investigate community structure, but rather gene capacity and expression should be taken into account as well. In humans, the establishment of the gut microbiome is heavily influenced by the mode of delivery and infant feeding methods, but factors such as postnatal drug administration and delivery room environment also play fundamental roles is early gut colonization (Tamburini et al., 2016). Improper colonization leading to dysbiosis can have dire consequences, as the gut microbiome plays a pivotal role in maintaining the integrity of the gut mucosal barrier and thus the immune-competent cells that inhabit this mucosa (Goulet, 2015). Impairment of the gut mucosal barrier, which continues to develop and is shaped even after birth, has been linked with various conditions ranging from type 2 diabetes to irritable bowel syndrome (IBS) and allergies (CerfBensussan and Gaboriau-Routhiau, 2010; De Medina et al., 2014; Natividad and Verdu, 2013). Considering this, wild animals subjected to microplastic pollution in the environments they inhabit and from the food they eat, from the moment of birth onwards throughout fetal development, may harbor an altered gut microbiome, influencing the health of wild animals in ways yet to be explored.

which shows that a balanced and healthy gut microbiome acts as a powerful buffer, preventing bacterial, viral, and fungal diseases (Man et al., 2017). With the advent of high-throughput sequencing and the extension of bacterial genetic databases to include pathogens, largescale screening and identification of bacterial infections in wildlife are now feasible (Menke et al., 2015; Wasimuddin et al., 2017, 2018). Yet the potential negative effects of microplastic consumption on the microbiome in wild animals have not received any attention. Research connecting microplastics with the gut microbiome is in its absolute infancy, as only very little scientific work has investigated this issue (Caruso et al., 2018; Horton et al., 2018; Jin et al., 2018, 2019; Lu et al., 2018; Qiao et al., 2019; Wan et al., 2018; Zhu et al., 2018; Zhu et al., 2018a, but see van Gestel and Selonen, 2018 and Zhu et al., 2018b). In all cases but two (Caruso et al., 2018; Horton et al., 2018), exposure to microplastic particles induced gut dysbiosis and altered bacterial diversity, and was even accompanied by further negative health effects, such as stunted growth and reproduction in soil oligochaetes (Zhu et al., 2018) and soil springtails (Zhu et al., 2018a), hepatic lipid metabolism disorder (Lu et al., 2018) and gut inflammation in mice (Jin et al., 2018), and changes in gut metabolic profiles linked to oxidative stress and inflammation in zebrafish (Qiao et al., 2019). The most common observation was that exposure to microplastics altered gut microbial beta diversity, leading to microbial communities distinct from the controls without microplastic treatments (Ju et al., 2019; Lu et al., 2018; Qiao et al., 2019; Zhu et al., 2018). Significant shifts in the relative abundances of certain phyla, often Bacteroidetes, Firmicutes, and Proteobacteria, which are commonly detected in gut microbiome studies, were also observed (Jin et al., 2019; Lu et al., 2018; Qiao et al., 2019; Wan et al., 2018; Zhu et al., 2018; Zhu et al., 2018a). Another common denominator was the significantly reduced alpha diversity in groups exposed to microplastics (Ju et al., 2019; Qiao et al., 2019; Wan et al., 2018; Zhu et al., 2018), although the study conducted by Zhu et al. (2018a) found the opposite to be true. Of the two studies that did not observe gut dysbiosis and altered bacterial diversity after exposure to microplastic particles, one was carried out in European sea bass (Dicentrarchus labrax), which were kept in aquaculture (Caruso et al., 2018). This study was limited not only by its sample size of only one replicate per three treatments, but also with regards to its outdated method of assessing bacterial diversity (combing denaturing gradient gel electrophoresis of the 16S rRNA gene with Sanger sequencing), which underestimates bacterial diversity and does not permit deep sequencing (Gloor et al., 2010). The other of the two studies, conducted by Horton et al. (2018), was also limited by a sample size of three great pond snail (Lymnaea stagnalis) individuals for microbial analysis. Furthermore, the digestive tract was not isolated for this study, but rather the entire snail biomass was used for bacterial DNA isolation and extraction, rending the analysis of the actual gut microbiome response to microplastic ingestion in this species impossible. Therefore, the resulting lack of impact on the gut microbiome in these studies should be viewed critically. To conclude, all available studies so far were either performed under experimental conditions and on model species or encompassed sequencing too superficial to allow for deep microbial community analyses. Thus, the detection of real-life effects of microplastics in environmentally relevant concentrations on the gut microbiomes of wild animals remains a mystery. How could microplastics influence the gut microbiome? Considering that the ingestion of microplastics is accompanied by a wide range of factors known to drive gut dysbiosis, such as malnutrition, inflammation, the introduction of pathogens, endocrine disruptors, and environmental chemicals, we believe that the ingestion of microplastics may alter the gut microbiome (Fig. 1). How such dysbiosis may take form has been discussed by Wasimuddin and co-authors (2018)and includes perturbations of alpha and beta diversity, an increase in potential pathogenic bacteria, a reduction in bacteria characteristic of a healthy gut microbial community, and the rise of negative 198

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4. Conclusions and directions for future work

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Microplastics are everywhere. They have been shown to cause fatal malnutrition, act as long-distance vectors for potential pathogens, harbor chemicals that can interfere with organismal biochemistry and hormone balance, and attract environmental chemicals that may be partially and temporarily hidden like a hoard of soldiers armed with different weapons inside a Trojan horse. Research linking microplastics with the gut microbiome is absolutely necessary, especially in light of mankind's increasing use of plastic and the fact that plastic does not biodegrade within our lifespans, but rather fragments into increasingly smaller pieces. Directions of future work should tackle the questions: How does the gut microbiome react to chronic microplastic ingestion? Does the abundance of potential pathogens increase? Does the community structure of the core microbiome shift? Does beta diversity decrease or increase? Are there similar patterns of dysbiosis across populations or even species? How many microplastic particles need to be ingested or accumulated before dysbiosis sets in? Is dysbiosis chronic or does it fluctuate according to levels of microplastic ingestion? Answering these questions will help to understand the health effects of microplastics-induced gut microbial changes. Whilst a significant amount of scientific work aims to determine if microplastics are harmful to biota (Baini et al., 2017; Besseling et al., 2013; Browne et al., 2013; Fossi et al., 2012; Sussarellu et al., 2016; Von Moos et al., 2012; Wright et al., 2013a), we propose that the gut microbiome may be the key to answering this burning question. Acknowledgments Declarations of interest: none. References Alam, F.C., Sembiring, E., Muntalif, S., Suendo, V., 2019. Microplastic distribution in surface water and sediment river around slum and industrial area (case study: Ciwalengke River, Majalaya district, Indonesia). Chemosphere 224, 637–645. https://doi.org/10.1016/j.chemosphere.2019.02.188. Alonso-Magdalena, P., Ropero, A.B., Soriano, S., García-Arévalo, M., Ripoll, C., Fuentes, E., Quesada, I., Nadal, Á., 2012. Bisphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol. Cell. Endocrinol. 355, 201–207. https://doi. org/10.1016/j.mce.2011.12.012. Amaral-Zettler, L.A., Zettler, E.R., Slikas, B., Boyd, G.D., Melvin, D.W., Morrall, C.E., Proskurowski, G., Mincer, T.J., 2015. The biogeography of the plastisphere: implications for policy. Front. Ecol. Environ. 13, 541–546. https://doi.org/10.1890/ 150017. Amato, K.R., 2013. Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci. Med. 1, 10–29. https://doi.org/10.2478/micsm2013-0002. Amato, K.R., Yeoman, C.J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Rex Gaskins, H., Stumpf, R.M., Yildirim, S., Torralba, M., Gillis, M., Wilson, B.A., Nelson, K.E., White, B.A., Leigh, S.R., 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353. https://doi.org/ 10.1038/ismej.2013.16. Anbumani, S., Kakkar, P., 2018. Ecotoxicological effects of microplastics on biota: a review. Environ. Sci. Pollut. Res. 25, 14373–14396. https://doi.org/10.1007/s11356018-1999-x. Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030. Andrady, A.L., 2017. The plastic in microplastics: a review. Mar. Pollut. Bull. 119, 12–22. https://doi.org/10.1016/j.marpolbul.2017.01.082. Andrady, A.L., Neal, M.A., 2009. Applications and societal benefits of plastics. Philos. Trans. R. Soc. B Biol. Sci. 364, 1977–1984. https://doi.org/10.1098/rstb.2008.0304. Arias-Andres, M., Klümper, U., Rojas-Jimenez, K., Grossart, H.P., 2018. Microplastic pollution increases gene exchange in aquatic ecosystems. Environ. Pollut. 237, 253–261. https://doi.org/10.1016/j.envpol.2018.02.058. Au, S.Y., Bruce, T.F., Bridges, W.C., Klaine, S.J., 2015. Responses of Hyalella azteca to acute and chronic microplastic exposures. Environ. Toxicol. Chem. 34, 2564–2572. https://doi.org/10.1002/etc.3093. Azzarello, M.Y., Van-Vleet, E.S., 1987. Marine birds and plastic pollution. Mar. Ecol. Prog. Ser. 37, 295–303. https://doi.org/10.3354/meps037295. Baini, M., Martellini, T., Cincinelli, A., Campani, T., Minutoli, R., Panti, C., Finoia, M.G., Fossi, M.C., 2017. First detection of seven phthalate esters (PAEs) as plastic tracers in superficial neustonic/planktonic samples and cetacean blubber. Anal. Methods 9, 1512–1520. https://doi.org/10.1039/C6AY02674E. Bakir, A., O'Connor, I.A., Rowland, S.J., Hendriks, A.J., Thompson, R.C., 2016. Relative

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