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Trends in Analytical Chemistry 112 (2019) 234e240

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Collateral effects of microplastic pollution on aquatic microorganisms:

An ecological perspective*
Maria Arias-Andres a, **, Keilor Rojas-Jimenez b, Hans-Peter Grossart c, d, *
Central American Institute for Studies on Toxic Substances (IRET), Universidad Nacional, Campus Omar Dengo, P.O. Box 86-3000, Heredia, Costa Rica
Escuela de Biología, Universidad de Costa Rica, 11501 San Jose, Costa Rica
Leibniz Institute of Freshwater Ecology and Inland Fisheries (IGB), Dept. Experimental Limnology, Alte Fischerhuette 2, D-16775 Stechlin, Germany
Potsdam University, Inst. of Biochemistry and Biology, Maulbeerallee 2, D-14469 Potsdam, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Microplastics (MP) provide a unique and extensive surface for microbial colonization in aquatic eco-
Available online 5 December 2018 systems. The formation of microorganism-microplastic complexes, such as biofilms, maximizes the
degradation of organic matter and horizontal gene transfer. In this context, MP affect the structure and
Keywords: function of microbial communities, which in turn render the physical and chemical fate of MP. This new
Microplastics (MP) paradigm generates challenges for microbiology, ecology, and ecotoxicology. Dispersal of MP is
concomitant with that of their associated microorganisms and their mobile genetic elements, including
antibiotic resistance genes, islands of pathogenicity, and diverse metabolic pathways. Functional changes
Microbial ecology
Carbon cycling
in aquatic microbiomes can alter carbon metabolism and food webs, with unknown consequences on
Aquatic ecosystems higher organisms or human microbiomes and hence health. Here, we examine a variety of effects of MP
Health risk assessment pollution from the microbial ecology perspective, whose repercussions on aquatic ecosystems begin to
be unraveled.
© 2018 Elsevier B.V. All rights reserved.

1. Introduction volume ratio of MP increases the absorption of organic matter and

represents a new habitat for diverse microbial assemblages, often
Recently, plastic pollution has caught the attention of both the referred to as the “plastisphere” [3]. However, very few studies
scientific community and the public. Increasing amounts of man- analyze microbial activities in MP biofilms and their potential re-
ufactured plastic polymers end up accumulating in landfills or the percussions for ecosystem functioning.
natural terrestrial and aquatic environments [1]. Environmental Biofilms are comprised of complex, diverse and dynamic mi-
surveys show that accumulation of mega- and macro-plastic items crobial communities that are sometimes surface-associated and
stays constant or diminishes while that of microplastic increases embedded in a self-produced matrix of extracellular polymeric
[2]. It has been proven that, in the environment, this plastic litter is substances (EPS) [4]. They are essential for sustaining both biodi-
fragmented into particles of less than a few millimeters denomi- versity and functioning of ecosystems, especially in aquatic biomes
nated as “microplastics” (MP), whose complete mineralization in the inland [5,6]. Cell proximity together with an EPS matrix
could last for centuries [3,4]. These particles can travel from land or protecting them from multiple environmental stressors (e.g.,
wastewater treatment facilities to natural freshwater ecosystems, physical abrasion and UV radiation), provides conditions to maxi-
and finally end up in the oceans [5], where they contribute to an mize interactions between different and even phylogenetically
estimated 4.85 trillion MP particles [2]. The higher surface area to distant groups [7]. These interactions result in a complex network
of metabolic co-operation which transform organic matter and
shape biogeochemical cycles with profound ecological implications
Special Issue on Analysis, Fate and Toxicity of Microplastics in the Environment. for the functioning of entire aquatic food webs.
* Corresponding author. Dept. Experimental Limnology, Leibniz Institute of In biofilms, increased horizontal gene transfer (HGT) can influ-
Freshwater Ecology and Inland Fisheries (IGB), Alte Fischerhuette 2, D-16775
ence the metabolic diversity of different microorganisms, whereby
Stechlin, Germany.
** Corresponding author. mobile genetic elements (MGEs) are frequently shared between
E-mail addresses: (M. Arias-Andres), keilor.rojas@ biofilm organisms affecting the interplay of various biochemical (K. Rojas-Jimenez), (H.-P. Grossart).
0165-9936/© 2018 Elsevier B.V. All rights reserved.
M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240 235

functions, e.g., exchanging different degradation pathways [4]. HGT Generally, impacts of MP on aquatic ecosystems can include the
is also a very relevant process for the spread of antibiotic resistance spread of “invasive” species and thus changes in microbial bioge-
genes (ARGs) worldwide, a long-recognized threat by the World ography [25,26]. Ecologically, these two effects are linked to the loss
Health Organization [8]. It is, therefore, reasonable to expect that of biodiversity and the spread of pathogens [27,28]. Although mi-
microbial biofilm formation on the ever-increasing amounts of MP crobes are less limited by dispersal processes at broader
in the environment can influence not only the fate of MP [9] but geographical scales than higher organisms, observations at finer
also their effects on the functioning of entire microbiomes, water resolution scale show dispersal shapes the ecological structure of
quality, ecosystem, and public health. microbial communities [29]. Indeed, geographical variation in the
This critical overview aims to cover the little-explored aspects of structure of MP microbial communities has been frequently
MP effects on aquatic microbial communities that can alter the observed in aquatic ecosystems [18,30], indicating the high po-
ecology and thus functioning of entire aquatic food webs. It high- tential of MP as vectors for transferring microorganisms between
lights the possible ecological consequences of MP biofilm formation even distant habitats, including pathogens or toxin-producing mi-
on HGT among aquatic bacteria, as well as on cycling of organic crobes. These hypotheses are supported by the expected longevity
matter mediated by microbes. Finally, we call for incorporating a of MP in the environment [31], by laboratory studies where plastics
microbial ecology centered analytical and conceptual approach for potentiate the survival of specific groups of microorganisms and
the assessment of potential hazards caused by MP in the their mobile genetic elements [32e34], and by studies that have
environment. found potential human or animal pathogenic bacteria on MP
[35,36]. However, more long-term and different-spatial scale
2. MP alter the ecology of aquatic microbial populations studies are still required to comprehensively evaluate the relevance
of MP for microbial dispersal and biogeography.
Ecologists have long emphasized the importance of human ac- Marine and freshwater organisms are known to ingest MP, and
tivities for microbial dispersal across the globe [10e12]. Human these often contain chemical substances [40]. Some laboratory
interference on Earth's biomes accelerated after the mid-20th studies or analyses of sorption coefficients indicate that the
century and caused substantial alterations of the structure and transfer of adsorbed chemicals from ingested MP to the biota is
function of microbial communities, perceptible as pronounced often lower than expected, while other studies demonstrate the
changes in human microbiota or biogeochemical cycling of ele- opposite effect [41e45]. The analysis of a broader set of contami-
ments (e.g., carbon, nitrogen, and phosphorus), and distribution of nants, polymers, and environmental conditions remains to be
specific genes (e.g., antibiotic resistance genes) [13,14]. An expo- evaluated [46], but in the case of ingested MP chemicals, it is
nential increase in the production of synthetic plastic polymers and relevant that gut microbiota can influence both the organism's
its omnipresence in the environment coincides, among other fac- health and the fate of organic pollutants [34,47]. Therefore, a new
tors, with the period of increasing industrialization and the approach should consider MP-induced alterations of the biota's
observed changes in the planet's microbiome [15]. microbiomes and at the same time their connection to the fate of
Evidence of the last five years strongly indicates that MP mi- organic pollutants after MP contact with aquatic biota. Further,
crobial communities in the environment exhibit a different comparisons should be made with other vectors for chemical
composition and structure than other natural aquatic habitats substances such as natural particles or food.
(e.g., natural particulate organic matter, water column and sedi- Discussions have surged over the use of traditional methods and
ments) [16e18]. Moreover, in vitro studies by Ogonowski et al. paradigms of ecotoxicology in the case of environmental and hu-
(2018) corroborated that the same initial aquatic microbial com- man health hazards caused by pollutants in the current Anthro-
munity results in different bacterial communities when growing pocene, including MP [37,38]. Currently, there is an increasing
on plastic polymers compared to other natural or inert substrates, interest to integrate microbiology and ecological approaches in the
indicating a material-dependent sorting effect, especially during assessment of health hazards caused by MP pollution. Microbes are
the early stages of particle colonization [19]. Recently, the impor- in many ways affected by contaminants and are of great importance
tance of microbial community structure for predicting microbial for environmental and human health since they perform essential
functions in ecosystems becomes increasingly evident [20]. functions in virtually all food webs [39]. In this context, as it has
Therefore, it is relevant to study the potentially numerous conse- been shown that drinking water can be contaminated by MP
quences of anthropogenic MP pollution for emerging changes in [40,41], a microbial approach would include analyzing the potential
structure and function of microbial communities during the of MP for altering the human gut microbiome, similar to those
contemporary anthropocene, and its potential risks for human and observed in soil organisms [42,43].
environmental health. This critical overview thus resumes the need of a microbial
Properties of plastic likely drive the development of biofilm ecological perspective to better evaluate the effects of MP
communities on MP in aquatic ecosystems (e.g., polymer type, pollution on environmental and human health. In the following
additives or absorbed pollutants and size of particles). Other factors sections, two specific and yet little-noted processes are high-
of influence could be the biological interactions among colonizers, lighted as being relevant for MP hazard assessment: a) horizontal
environmental conditions, weathering of the material and trans- gene transfer (HGT) and b) carbon metabolism of microbial
port among environmental matrixes (biota, particulate material, communities.
water column and sediments) [6,9]. Thus, differences in community
structure development on MP biofilms among marine and fresh- 3. MP influence evolution by increased horizontal gene
water systems are expected. Also, freshwater systems (rivers and transfer
lakes) are closer to sources of MP and other types of pollution, as
they are among the most human-altered environments [21,22]. HGT involves three different mechanisms for the movement of
Meanwhile, the oceans are considered the main long-term sink for genetic material between organisms, other than by transmission
MP [23], and interactions occur with the entire planktonic micro- from parent to offspring [44]. Among these, conjugation requires
organisms that contribute to a significant part of the biomass direct cell-to-cell exchange from a donor to a recipient, while
production worldwide [24]. Therefore, MP impacts can reach transduction and transformation represent virus-mediated trans-
different dimensions within these two systems. port and environmental uptake of DNA, respectively [45]. All these
236 M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240

mechanisms have provided microorganisms with the ability to 4. Microplastics increase heterotrophic activity and alter
adapt to changing conditions rapidly [46]. Consequently, the carbon cycling
incorporation of those genetic changes in their genomes causes an
accelerated evolution of microbial life [46]. Human interventions on the biogeochemical activity of mi-
There is a high potential of MP biofilms to transfer mobile ge- crobes comprise the increase in CO2 emissions or alterations in the
netic elements among habitats, including some genes of human global CH4 cycle [13,53]. The impact of MP biofilm communities on
origin. This mechanism was verified for microcosms by using the the ecological interactions of microbes and the evolution of the
class 1 integron gene, a marker of anthropogenic pollution from microbial genomes as discussed in section 2 and 3, can have po-
wastewater effluent bacteria [34]. Moreover, the development of a tential consequences over one of the most critical ecosystem
much permissive community to gene exchange in MP biofilms has functions of microorganisms, i.e. the cycling of organic carbon and
also been experimentally demonstrated with aquatic bacterial its transfer to the rest of the aquatic food web [54]. These potential
communities [47]. These changes in HGT could affect microbial effects raise the question if MP biofilms represent new and unique
evolution at a planetary scale, and as a result facilitate the wide- niches of heterotrophic activity?
spread distribution of antibiotic resistance genes, clusters of Recent physiological and metagenomic evidence suggest that
biodegradation pathways, as well as pathogenicity determinants, MP biofilm communities are characterized by a different metabolic
and alter bacterial speciation processes [48]. In this regard, the structure in comparison to microbial communities in the sur-
influence of MP on the distribution of mobile genetic elements rounding water, including natural particle-associated microbes
would bring another facet to the effects of these so-called emergent [55,56]. Other studies indicate the potential of MP biofilm com-
pollutants. munities for degradation of hydrocarbon compounds, or incom-
Furthermore, MP particles are in close contact with humans on a plete break down and fragmentation of plastic polymers [19,57,58].
daily basis, e.g., in personal care products, drinking water, food and The magnitude and characteristics of MP pollution and biofilm
other types of environmental exposure in the aquatic, terrestrial formation makes this a relevant scenario to be addressed, yet the
and atmospheric realms. This situation calls for the urgent need for evidence obtained is preliminary and sparsely quantitative.
evaluating their effects on humans following the manifold and For instance, plastics add significant amounts of allochthonous
differing types of exposure [61,62]. Previously, several important organic and inorganic carbon to aquatic ecosystems. According to a
questions have been identified, e.g. (i) to what extent are MP par- recent study in seawater, annually, up to 23,600 metric tons of
ticles entering and subsequently accumulating in the human body? dissolved organic carbon (DOC) escape from the 4.8e12.7 million
(ii) How do our bodies react when exposed to MP and their asso- tons of plastics, which have entered the ocean in 2010 [59].
ciated contaminants? [63]. Although several indications exist that Furthermore, it has been shown that some plastic polymers emit
HGT in the human microbiome is strongly related to human health the greenhouse gases methane and ethylene [60]. Conversely,
[64], HGT between MP biofilms and human microbes has been plastics have a large capacity to adsorb organic matter and other
greatly neglected, yet it may represent another relevant hazard of substances from the surrounding water [61] and contain additives
this emergent universal pollutant. inserted during manufacture [62].
For example, MP could potentiate the distribution of antibiotic The activities of MP biofilm communities are the result of the
resistance determinants in the environment and eventually harm synergy of organisms belonging to different domains of life (i.e.,
humans and farm animals, as part of other massive anthropogenic eukaryotes and prokaryotes) [3,18,63] and interact with the en-
interventions in the environment, e.g., solid waste and wastewater tirety of MP-associated substances. Since the quality of dissolved
discharges [65,66]. Also, an adaptation of Vibrio spp. (often organic matter (DOM) shapes microbial community assembly and
persistent on MP in aquatic ecosystems) to the biofilm lifestyle and metabolic activity [64,65], plastic-derived DOC could partially
other HGT-induced changes are of potential relevance for the explain a different profile of carbon substrate utilization by MP
development of pathogenic variants and their successful transfer to microbes in comparison to those in the surrounding water. The
the human microbiome [62,67,68]. To identify this potential health effect of plastic-derived DOC on microbial function is yet another
hazard, the “resistome” (the collection of all antibiotic resistance research question that could be easily tested experimentally.
genes present) of MP biofilms and a more detailed assessment on However, the released carbon from MP polymers can also influence
consequences of MP exposure to humans and animals need to be the free-living bacteria by contributing to their DOC bioavailability,
developed. as seen with particulate organic matter (POM) [66].
The mechanisms, by which plastic surfaces modulate HGT, On the other hand, organic compounds from or transported by
remain to be elucidated. Until now, a single study found that as plastics can enhance the HGT of bio-degradation pathways, as has
the abundance of a plasmid (a common type of mobile genetic been demonstrated earlier for organic compounds from waste-
element) increases in a natural microbial community, its pop- water [67]. Changes in the assimilation of organic matter can occur
ulations were rendered to be more permissive to its transfer [49]. after mobile genetic elements with new metabolic pathways have
Therefore, the abundance and characteristics of MP-associated been transferred from MP-associated bacteria to, e.g., the gut
plasmids, i.e., the MP plasmidome, require more attention. In microbiome of higher organisms [68]. Such changes most likely
addition, evidence shows that permissiveness for plasmid lead to alterations in organismic growth and life traits (e.g., nutrient
transfer in individual species is affected by the surrounding assimilation and reproduction). More detailed studies addressing
community structure and the specific environmental settings this critical aspect of MP pollution are required to assess the real
[50]. This notion suggests that specific microbial assemblages in dimension of the potential consequences for environmental and
MP biofilms can result in adaptation towards plasmid acquisition human health.
at the community level [47]. Finally, adsorption of chemical
substances by MP, e.g., antibiotics [51], could provide selective 5. Analytical considerations for hazard assessment of MP
conditions which further induce HGT processes in the natural from a microbial ecology perspective
environment. As sorption can vary widely among polymers,
substances, and environmental conditions [52], potential in- The information produced by hypothesis-driven laboratory ex-
fluences on HGT among MP-associated microbes should be periments facilitates the examination of specific MP-induced ef-
determined in more detail. fects on microorganisms. New analytical procedures should not
M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240 237

only account for physical-chemical but also biological mechanisms. although these are not commercially produced and thus remain
Specific methodological approaches for the analysis of MP micro- less used in microcosm studies [69]. A fiber can offer a higher
bial communities and their activities are summarized in Table 1. For surface to volume ratio and roughness than a bead particle. These
example, manipulating the concentration and the physical- irregularities could offer even more places for biofilm formation
chemical characteristics of MP to study the activity of their asso- and microbial activity than currently assumed.
ciated microbial communities enables predictions on MP-induced Studies intended to analyze HGT processes on MP, e.g., conju-
effects on microbial activities and their ecological consequences. gation, should consider that detection limits of traditional culture-
Furthermore, using different MP concentrations allows ac- dependent assays are in the range of 109e1010 cells [70]. However,
counting for the effect of increased MP pollution on overall mi- over the last decade, advances in reporter gene technology have
crobial dynamics in aquatic systems (e.g., the distribution of provided new insights into the extent and spatial frequencies of
microbial communities originated from different sources such as HGT in vitro and natural environments [71]. Accordingly, a set of
wastewaters or changes in biofouling intensity). Fibers are the different tools like fluorescent-based flow cytometry (FCM) and cell
prevalent form of MP particles reported in the environment, sorting (FACS), next-generation sequencing, qPCR, and metabolic

Table 1
Overview on methods for analyzing microbial and ecological aspects of MP pollution.

Methods Purpose Advantages Limitations Ref.

Fluorescence or Electron microscopy Characterization of MP- Doesn't require extensive No high-throughput, low [3,17,75]
associated microorganisms and methodological knowledge, phylogenetic resolution.
biofilm structure. allows to observe spatial
distribution of cells in biofilm.
Culture-based methods Isolation of MP-associated Direct physiological testing (e.g. A scarce portion of microbial [33,35,55]
microorganisms and plastic biodegradation or communities is culturable.
characterization of their demonstration of viable
functional capacities. pathogen survival).
Fluorescence in situ hybridization Detection of single cells of Allows phylogenetic detection Limited phylogenetic [76]
different microbial groups. and quantification at the same resolution, major phylotypes
time. need to be known, labor
Allows observation of spatial intensive, no high-throughput.
distribution of microbial groups
in the biofilm.
Illumina amplicon sequencing Prokaryotic & eukaryotic Standard method in microbial No functional information. [16e18,30,57,75]
community composition. ecology, relatively cheap, high- Limited phylogenetic
throughput and phylogenetic information, genetic
resolution. identification does not
guarantee viability of cells.
Fluorescence activated cell sorting (FACS) Detection and isolation of Allows detection of phylogeny Labor intensive, relatively [6,47]
specific cells. and functionality on a single expensive, no high-throughput
Functional analysis by cell level, quantification of and limited sample volume.
fluorescently labelled genes microbes with similar
and proteins. functions, whole genome
sequencing of single cells
Metagenomes Information on functional Detailed potential functional Relatively expensive, requires [56,75]
potential of biofilm-associated information (e.g., antibiotic intensive bioinformatics,
microbes. resistance), allows detection of functional potential needs to be
unknown potential metabolic addressed in specific tests,
pathways, reconstruction of transcriptomics or proteomic
whole genomes of specific studies.
populations and community
network analysis.
Lab. incubations, chemostats Characterization of microbial Relatively easy to perform and Limited to model systems, [14,19,34,42,43,47]
function considering biofilm to reproduce, allows for control limitation to cover the whole
complexity. of specific variables (type of complexity of natural
plastic polymer, environmental ecosystems (e.g., interactions
variables, initial community with higher trophic levels).
Metatranscriptomes Functional information on MP- Detailed functional Relatively expensive, requires e
associated microbes (gene information, allows to intensive bioinformatics,
expression), expression of reconstruct single genomes, transcription reflects a short
antibiotic resistance genes, allows detection of unknown time response to multiple
expression of HGT-related metabolic pathways, stimuli.
vectors (e.g. transposases). normalization allows for
quantification of processes.
Metaproteomes Functional information on MP- Quantification of specific Relatively expensive, requires e
associated microbes (protein pathways can be further used lots of biofilm material,
expression), quantification of for industrial applications (e.g., database of annotated protein
specific functions. biodegradation of plastic by less developed than for genes.
microbial enzymes).
Mesocosm experiments Effects of MP pollution on Allow for extrapolation of Labor and person intensive, e
ecosystem microbial function effects to whole ecosystems expensive equipment required
and changes in entire food (e.g., transfer of pathogenic for measurements.
webs. bacteria from MP biofilms
trough the aquatic food web).
238 M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240

fingerprint methods provide more sensitive alternatives to Finally, we consider that one of the most critical challenges in
cultivation-based methods, opening avenues for high-throughput studies on MP-associated microbial communities includes the
analyses [72,73]. However, it is important to bear in mind that integration of different levels of information, from micro-scale (e.g.,
biofilm communities can show different conjugation dynamics an individual cell, microbial communities, MP biofilms) up to
according to the physical structure of microbial MP biofilms. macro-scale and even global consequences (aquatic food webs and
Moreover, the potential of a specific donor-plasmid combination to ecosystems). We also consider that more ecological studies are
invade a biofilm is the result of different ecological factors in the required to demonstrate the multiple effects of MP pollution on
surrounding environment [74]. rates of gene exchange and carbon metabolism, as well as the
respective repercussions to aquatic food webs and pollutant fate
(Fig. 1). These effects also include the far-reaching consequences of
increased antibiotic resistance spread to the human microbiome
and health (Fig. 2). We thus call for updating and re-thinking how
environmental scientists analyze complex and globally-important
contaminants [38], in particular, the emerging threats of MP
pollution in our environment.

6. Conclusion

MP pollution, together with gas greenhouse emissions and

antibiotic resistance, has the potential to be among the most
pressing planetary boundary threats shortly. However, evaluation
of MP-induced effects for human and environmental health is still
in the early stage. As presented in this critical review, the re-
percussions of altering Earth and human microbiomes require
Fig. 1. Proposed effects of MP biofilms on aquatic ecosystems from a microbial
ecology perspective. Hyphenated arrows indicate either flow of carbon or changes in long-term analysis and a more microbial ecology perspective. The
water chemistry. A) Plastic fragmentation ends up in MP formation. Microbes interact magnitude of potential effects of MP on organisms' health and
with MP by biofouling and biofilm formation. These microorganisms are the base of overall ecosystem functioning is still to be determined. Microbial
the aquatic food web and carbon cycling. Ecological effects may follow: (B) Effects on communities are among the first living things to interact with MP,
water biogeochemistry: MP biofilms allow for diverse microbial groups to form
metabolic networks, degrading absorbed organic matter and releasing DOM of
from their emission to the environment to their final destination
different quality to the system including greenhouse gases (e.g., carbon dioxide and (sinking and deposition in sediments or accumulation in biota).
methane). All translates in altered rates of biochemical activity, (e.g., increased het- Consequently, they also link organic matter and elements from
erotrophy) that can affect localized water and sediment biogeochemistry (e.g., oxygen abiotic compartments (including plastics) to the rest of the aquatic
and ammonium decrease). C) Effects on health and fitness of aquatic biota. Aquatic
(and all other) food webs. The effects of MP interactions with
organisms (e.g., fish, bivalves, arthropods) ingest MP or organisms containing MP. The
MP biofilm communities interact with the biota's natural microbiomes (e.g., gut aquatic microbiomes and of higher organisms therefore should be
microbiota). Microbe-mediated matter exchange (biological and chemical) between accounted for in any hazard or health risk assessment of MP
MP biofilms and organisms' microbiota can lead to alteration in nutrient assimilation, pollution.
pathogenic invasions, or increased availability of organic pollutants, which decrease
the organism's fitness. D) The alterations in B and C are influenced by changes in the
distribution of mobile genetic elements by MP biofilms. Increased HGT and the
Declaration of interest
development of a biofilm community more permissive to gene exchange allow the
formation of new metabolic pathways across different habitats of the aquatic None.
ecosystem, influencing localized DOM fluxes, or the spread of attachment mechanisms
that allow colonization of new habitats.

A scholarship from Universidad Nacional, Costa Rica provided to

MAA, and by the Leibniz SAW project MikrOMIK (SAW-2014-IOW-
2) given to HPG enabled this work.


[1] R. Geyer, J.R. Jambeck, K.L. Law, Production, use, and fate of all plastics ever
made, Sci. Adv. 3 (2017), e1700782.
[2] R. Hurley, J. Woodward, J.J. Rothwell, Microplastic contamination of river beds
significantly reduced by catchment-wide flooding, Nat. Geosci. 11 (2018)
[3] E.R. Zettler, T.J. Mincer, L.A. Amaral-Zettler, Life in the “plastisphere”: micro-
bial communities on plastic marine debris, Environ. Sci. Technol. 47 (2013)
[4] H.-C. Flemming, J. Wingender, U. Szewzyk, P. Steinberg, S.A. Rice, S. Kjelleberg,
Biofilms: an emergent form of bacterial life, Nat. Rev. Microbiol. 14 (2016)
[5] T.J. Battin, K. Besemer, M.M. Bengtsson, A.M. Romani, A.I. Packmann, The
ecology and biogeochemistry of stream biofilms, Nat. Rev. Microbiol. 14
Fig. 2. Proposed role of MP in the spread of antibiotic resistance and pathogenicity
(2016) 251e263.
determinants through aquatic systems. A) Microbial communities in MP biofilms
[6] J.P. Harrison, T.J. Hoellein, M. Sapp, A.S. Tagg, Y. Ju-Nam, J.J. Ojeda, Micro-
adapt to increased rates of HGT activity compared to, e.g., free-living organisms (FL); B) plastic-associated Biofilms: a Comparison of Freshwater and Marine Envi-
Plasmid, integrative conjugative elements and other types of mobile genetic elements ronments, 2018, pp. 181e201.
(MGEs) are selectively transferred in MP biofilms with diverse microbial community [7] M.A. Demeter, J.A. Lemire, R.J. Turner, J.J. Harrison, Biofilm survival strategies
structures; C) Pathogenic bacteria or their MGEs, including antibiotic resistance genes, in polluted environments, in: Biofilms Bioremediation Curr. Res. Emerg.
are transported by MP from wastewaters through the aquatic system and food web and Technol, Caister Academic Press, 2016, pp. 43e56.
eventually to humans (hyphenated lines). 9781910190296.03.
M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240 239

[8] J.L. Balcazar, J. Subirats, C.M. Borrego, The role of biofilms as environmental [32] H.K. Webb, R.J. Crawford, T. Sawabe, E.P. Ivanova, Poly(ethylene tere-
reservoirs of antibiotic resistance, Front. Microbiol. 6 (2015). phthalate) polymer surfaces as a substrate for bacterial attachment and bio-
10.3389/fmicb.2015.01216. film formation, Microb. Environ. 24 (2009) 39e42.
[9] C.D. Rummel, A. Jahnke, E. Gorokhova, D. Kühnel, M. Schmitt-Jansen, Impacts jsme2.ME08538.
of biofilm formation on the fate and potential effects of microplastic in the [33] D. Lobelle, M. Cunliffe, Early microbial biofilm formation on marine plastic
aquatic environment, Environ. Sci. Technol. Lett. 4 (2017) 258e267. https:// debris, Mar. Pollut. Bull. 62 (2011) 197e200. polbul.2010.10.013.
[10] D.M. Wilkinson, Have we underestimated the importance of humans in the [34] E.M. Eckert, A. Di Cesare, M.T. Kettner, M. Arias-Andres, D. Fontaneto, H.-
biogeography of free-living terrestrial microorganisms? J. Biogeogr. 37 (2010) P. Grossart, G. Corno, Microplastics increase impact of treated wastewater on
393e397. freshwater microbial community, Environ. Pollut. 234 (2018) 495e502.
[11] E. Litchman, Invisible invaders: non-pathogenic invasive microbes in aquatic
and terrestrial ecosystems, Ecol. Lett. 13 (2010) 1560e1572. [35] I.V. Kirstein, S. Kirmizi, A. Wichels, A. Garin-Fernandez, R. Erler, M. Lo € der,
10.1111/j.1461-0248.2010.01544.x. G. Gerdts, Dangerous hitchhikers? Evidence for potentially pathogenic Vibrio
[12] Y.-G. Zhu, M. Gillings, P. Simonet, D. Stekel, S. Banwart, J. Penuelas, Microbial spp. on microplastic particles, Mar. Environ. Res. 120 (2016) 1e8. https://
mass movements, Science (80) 357 (2017) 1099e1100.
10.1126/science.aao3007.  Koren, A. Kr
[36] M.K. Virsek, M.N. Lovsin, S. zan, M. Peterlin, Microplastics as a
[13] M.R. Gillings, I.T. Paulsen, Microbiology of the anthropocene, Anthropocene 5 vector for the transport of the bacterial fish pathogen species Aeromonas
(2014) 1e8. salmonicida, Mar. Pollut. Bull. 125 (2017) 301e309.
[14] Y.-G. Zhu, M. Gillings, P. Simonet, D. Stekel, S. Banwart, J. Penuelas, Human j.marpolbul.2017.08.024.
dissemination of genes and microorganisms in Earth's Critical Zone, Glob. [37] G.A. Burton, Stressor exposures determine risk: so, why do fellow scientists
Change Biol. 24 (2018) 1488e1499. continue to focus on superficial microplastics risk? Environ. Sci. Technol. 51
[15] J. Zalasiewicz, C.N. Waters, J.A. Ivar do Sul, P.L. Corcoran, A.D. Barnosky, A. Cearreta, (2017) 13515e13516.
M. Edgeworth, A. Gałuszka, C. Jeandel, R. Leinfelder, J.R. McNeill, W. Steffen, [38] J. Kramm, C. Vo €lker, M. Wagner, Superficial or substantial: why care about
C. Summerhayes, M. Wagreich, M. Williams, A.P. Wolfe, Y. Yonan, The geological microplastics in the anthropocene? Environ. Sci. Technol. 52 (2018)
cycle of plastics and their use as a stratigraphic indicator of the Anthropocene, 3336e3337.
Anthropocene 13 (2016) 4e17. [39] S. Sabater, Microbial ecotoxicology: looking to the future, in: Microb. Eco-
[16] T.J. Hoellein, A.R. McCormick, J. Hittie, M.G. London, J.W. Scott, J.J. Kelly, toxicol., Springer International Publishing, Cham, 2017, pp. 339e352. https://
Longitudinal patterns of microplastic concentration and bacterial assemblages
in surface and benthic habitats of an urban river, Freshw. Sci. 36 (2017) [40] S.M. Mintenig, M.G.J. Lo €der, S. Primpke, G. Gerdts, Low numbers of micro-
491e507. plastics detected in drinking water from ground water sources, Sci. Total
[17] A. McCormick, T.J. Hoellein, S.A. Mason, J. Schluep, J.J. Kelly, Microplastic is an Environ. 648 (2019) 631e635.
abundant and distinct microbial habitat in an urban river, Environ. Sci. 178.
Technol. 48 (2014) 11863e11871. [41] M. Pivokonsky, L. Cermakova, K. Novotna, P. Peer, T. Cajthaml, V. Janda,
[18] M.T. Kettner, K. Rojas-Jimenez, S. Oberbeckmann, M. Labrenz, H.-P. Grossart, Occurrence of microplastics in raw and treated drinking water, Sci. Total
Microplastics alter composition of fungal communities in aquatic ecosystems, Environ. 643 (2018) 1644e1651.
Environ. Microbiol. 19 (2017) 4447e4459. 102.
2920.13891. [42] D. Zhu, Q.-L. Chen, X.-L. An, X.-R. Yang, P. Christie, X. Ke, L.-H. Wu, Y.-G. Zhu,
[19] M. Ogonowski, A. Motiei, K. Ininbergs, E. Hell, Z. Gerdes, K.I. Udekwu, Z. Bacsik, Exposure of soil collembolans to microplastics perturbs their gut microbiota
E. Gorokhova, Evidence for selective bacterial community structuring on micro- and alters their isotopic composition, Soil Biol. Biochem. 116 (2018) 302e310.
plastics, Environ. Microbiol. (2018).
[20] E.B. Graham, J.E. Knelman, A. Schindlbacher, S. Siciliano, M. Breulmann, A. [43] B.-K. Zhu, Y.-M. Fang, D. Zhu, P. Christie, X. Ke, Y.-G. Zhu, Exposure to nano-
Yannarell, J.M. Beman, G. Abell, L. Philippot, J. Prosser, A. Foulquier, J.C. Yuste, plastics disturbs the gut microbiome in the soil oligochaete Enchytraeus
H.C. Glanville, D.L. Jones, R. Angel, J. Salminen, R.J. Newton, H. Bürgmann, L.J. crypticus, Environ. Pollut. 239 (2018) 408e415.
Ingram, U. Hamer, H.M.P. Siljanen, K. Peltoniemi, K. Potthast, L. Ban ~ eras, M. j.envpol.2018.04.017.
Hartmann, S. Banerjee, R.-Q. Yu, G. Nogaro, A. Richter, M. Koranda, S.C. Castle, [44] S.M. Soucy, J. Huang, J.P. Gogarten, Horizontal gene transfer: building the web
M. Goberna, B. Song, A. Chatterjee, O.C. Nunes, A.R. Lopes, Y. Cao, A. Kai- of life, Nat. Rev. Genet. 16 (2015) 472e482.
sermann, S. Hallin, M.S. Strickland, J. Garcia-Pausas, J. Barba, H. Kang, K. Isobe, [45] C.N. Drudge, L.A. Warren, Prokaryotic horizontal gene transfer in freshwater
S. Papaspyrou, R. Pastorelli, A. Lagomarsino, E.S. Lindstro € m, N. Basiliko, D.R. lakes: implications of dynamic biogeochemical zonation, J. Environ. Prot.
Nemergut, Microbes as engines of ecosystem function: when does community (Irvine, Calif) 03 (2012) 1634e1654.
structure enhance predictions of ecosystem processes? Front. Microbiol. 7 [46] S. Linz, A. Radtke, A. von Haeseler, A likelihood framework to measure hori-
(2016). zontal gene transfer, Mol. Biol. Evol. 24 (2007) 1312e1319.
[21] R.K. Kopf, C.M. Finlayson, P. Humphries, N.C. Sims, S. Hladyz, Anthropocene 10.1093/molbev/msm052.
baselines: assessing change and managing biodiversity in human-dominated [47] M. Arias-Andres, U. Klümper, K. Rojas-Jimenez, H.-P. Grossart, Microplastic
aquatic ecosystems, Bioscience 65 (2015) 798e811. pollution increases gene exchange in aquatic ecosystems, Environ. Pollut. 237
biosci/biv092. (2018).
[22] S. Lambert, M. Wagner, Microplastics are contaminants of emerging concern [48] F. de la Cruz, J. Davies, Horizontal gene transfer and the origin of species:
in freshwater environments: an overview BT e freshwater microplastics : lessons from bacteria, Trends Microbiol. 8 (2000) 128e133.
emerging environmental contaminants?, in: M. Wagner, S. Lambert (Editors), [49] X. Bellanger, H. Guilloteau, B. Breuil, C. Merlin, Natural microbial communities
Freshw. Microplastics, Springer International Publishing, Cham, 2018, supporting the transfer of the IncP-1b plasmid pB10 exhibit a higher initial
pp. 1e23. content of plasmids from the same incompatibility group, Front. Microbiol. 5
[23] C.M. Rochman, Microplastics researchdfrom sink to source, Science (80) 360 (2014) 637.
(2018) 28e29. [50] C.I. de la Cruz-Perera, D. Ren, M. Blanchet, L. Dendooven, R. Marsch,
[24] S.J. Giovannoni, K.L. Vergin, Seasonality in ocean microbial communities, S.J. Sørensen, M. Burmølle, The ability of soil bacteria to receive the con-
Science (80) 335 (2012) 671e676. jugative IncP1 plasmid, pKJK10, is different in a mixed community compared
[25] GESAMP, Sources, Fate and Effects of Microplastics in the Marine Environ- to single strains, FEMS Microbiol. Lett. 338 (2013) 95e100.
ment: a Global Assessment, 2015. 10.1111/1574-6968.12036.
[26] A.L. Andrady, The plastic in microplastics: a review, Mar. Pollut. Bull. 119 [51] J. Li, K. Zhang, H. Zhang, Adsorption of antibiotics on microplastics, En-
(2017) 12e22. viron. Pollut. 237 (2018) 460e467.
[27] S. Amalfitano, M. Coci, G. Corno, G.M. Luna, A microbial perspective on bio- 02.050.
logical invasions in aquatic ecosystems, Hydrobiologia 746 (2015) 13e22. [52] X.-C. Shen, D.-C. Li, X.-F. Sima, H.-Y. Cheng, H. Jiang, The effects of environ- mental conditions on the enrichment of antibiotics on microplastics in
[28] A. Keswani, D.M. Oliver, T. Gutierrez, R.S. Quilliam, Microbial hitchhikers on simulated natural water column, Environ. Res. 166 (2018) 377e383. https://
marine plastic debris: human exposure risks at bathing waters and beach
environments, Mar. Environ. Res. 118 (2016) 10e19. [53] J.G. Monroe, D.W. Markman, W.S. Beck, A.J. Felton, M.L. Vahsen, Y. Pressler,
j.marenvres.2016.04.006. Ecoevolutionary dynamics of carbon cycling in the anthropocene, Trends Ecol.
[29] S.M. Gibbons, Metapopulation theory provides new insight into microbial Evol. 33 (2018) 213e225.
biogeography, Environ. Microbiol. 19 (2017) 849e850. [54] A.M. Amado, F. Roland (Editors), Microbial Role in the Carbon Cycle in Tropical
10.1111/1462-2920.13702. Inland Aquatic Ecosystems, Frontiers Media SA, 2017.
[30] L.A. Amaral-Zettler, E.R. Zettler, B. Slikas, G.D. Boyd, D.W. Melvin, C.E. Morrall, 978-2-88945-127-2.
G. Proskurowski, T.J. Mincer, The biogeography of the plastisphere: implica- [55] M. Arias-Andres, M.T. Kettner, T. Miki, H.-P. Grossart, Microplastics: new
tions for policy, Front. Ecol. Environ. 13 (2015) 541e546. substrates for heterotrophic activity contribute to altering organic matter
10.1890/150017. cycles in aquatic ecosystems, Sci. Total Environ. 635 (2018).
[31] J. Peng, J. Wang, L. Cai, Current understanding of microplastics in the envi- 10.1016/j.scitotenv.2018.04.199.
ronment: occurrence, fate, risks, and what we should do, Integr. Environ. [56] J.A. Bryant, T.M. Clemente, D.A. Viviani, A.A. Fong, K.A. Thomas, P. Kemp,
Assess. Manag. 13 (2017) 476e482. D.M. Karl, A.E. White, E.F. DeLong, Diversity and activity of communities
240 M. Arias-Andres et al. / Trends in Analytical Chemistry 112 (2019) 234e240

inhabiting plastic debris in the North Pacific Gyre, MSystems 1 (2016). https:// particle density gradient from freshwater to open ocean, J. Geophys. Res. Biogeosci. 121 (2016) 2261e2274.
[57] D. Debroas, A. Mone, A. Ter Halle, Plastics in the North Atlantic garbage [67] Y.-N. Jiao, H. Chen, R.-X. Gao, Y.-G. Zhu, C. Rensing, Organic compounds
patch: a boat-microbe for hitchhikers and plastic degraders, Sci. Total En- stimulate horizontal transfer of antibiotic resistance genes in mixed waste-
viron. 599e600 (2017) 1222e1232. water treatment systems, Chemosphere 184 (2017) 53e61.
2017.05.059. 10.1016/j.chemosphere.2017.05.149.
[58] A.K. Urbanek, W. Rymowicz, A.M. Miron  czuk, Degradation of plastics and [68] H.J. Flint, K.P. Scott, S.H. Duncan, P. Louis, E. Forano, Microbial degradation of
plastic-degrading bacteria in cold marine habitats, Appl. Microbiol. Bio- complex carbohydrates in the gut, Gut Microb. 3 (2012) 289e306. https://
technol. 102 (2018) 7669e7678.
C. Romera-Castillo, M. Pinto, T.M. Langer, X.A. Alvarez-Salgado, G.J. Herndl, [69] M. Cole, A novel method for preparing microplastic fibers, Sci. Rep. 6 (2016)
Dissolved organic carbon leaching from plastics stimulates microbial activity 34519.
in the ocean, Nat. Commun. 9 (2018) 1430. [70] K.M. Nielsen, T. Bøhn, J.P. Townsend, Detecting rare gene transfer events in
018-03798-5. bacterial populations, Front. Microbiol. 4 (2014).
[60] S.-J. Royer, S. Ferro n, S.T. Wilson, D.M. Karl, Production of methane and fmicb.2013.00415.
ethylene from plastic in the environment, PLoS One 13 (2018), e0200574. [71] A. Reisner, H. Wolinski, E.L. Zechner, In situ monitoring of IncF plasmid transfer on semi-solid agar surfaces reveals a limited invasion of plasmids in
[61] H. Hirai, H. Takada, Y. Ogata, R. Yamashita, K. Mizukawa, M. Saha, C. Kwan, recipient colonies, Plasmid 67 (2012) 155e161.
C. Moore, H. Gray, D. Laursen, E.R. Zettler, J.W. Farrington, C.M. Reddy, j.plasmid.2012.01.001.
E.E. Peacock, M.W. Ward, Organic micropollutants in marine plastics debris [72] R. Pinilla-Redondo, V. Cyriaque, S. Jacquiod, S.J. Sørensen, L. Riber, Monitoring
from the open ocean and remote and urban beaches, Mar. Pollut. Bull. 62 plasmid-mediated horizontal gene transfer in microbiomes: recent advances
(2011) 1683e1692. and future perspectives, Plasmid (2018).
[62] A. Jahnke, H.P.H. Arp, B.I. Escher, B. Gewert, E. Gorokhova, D. Kühnel, M. 2018.08.002.
Ogonowski, A. Potthoff, C. Rummel, M. Schmitt-Jansen, E. Toorman, M. [73] W. Loftie-Eaton, A. Tucker, A. Norton, E.M. Top, Flow cytometry and real-time
MacLeod, Reducing uncertainty and confronting ignorance about the possible quantitative PCR as tools for assessing plasmid persistence, Appl. Environ.
impacts of weathering plastic in the marine environment, Environ. Sci. Microbiol. 80 (2014) 5439e5446.
Technol. Lett. 4 (2017) 85e90. [74] X. Bellanger, H. Guilloteau, S. Bonot, C. Merlin, Demonstrating plasmid-based
[63] S. Oberbeckmann, M.G.J. Lo €der, M. Labrenz, Marine microplastic-associated horizontal gene transfer in complex environmental matrices: a practical
biofilms e a review, Environ. Chem. 12 (2015) 551e562. approach for a critical review, Sci. Total Environ. 493 (2014) 872e882. https://
[64] C. Ruiz-Gonza lez, J.P. Nin
~ o-García, J.-F. Lapierre, P.A. del Giorgio, The quality of
organic matter shapes the functional biogeography of bacterioplankton across [75] C. De Tender, C. Schlundt, L.I. Devriese, T.J. Mincer, E.R. Zettler, L.A. Amaral-
boreal freshwater ecosystems, Glob. Ecol. Biogeogr. 24 (2015) 1487e1498. Zettler, A review of microscopy and comparative molecular-based methods to characterize “Plastisphere” communities, Anal. Methods 9 (2017) 2132e2143.
[65] J. Pernthaler, Competition and niche separation of pelagic bacteria in fresh-
water habitats, Environ. Microbiol. 19 (2017) 2133e2150. [76] J.P. Harrison, M. Schratzberger, M. Sapp, A.M. Osborn, Rapid bacterial colo-
10.1111/1462-2920.13742. nization of low-density polyethylene microplastics in coastal sediment mi-
[66] Y. Zhang, W. Xiao, N. Jiao, Linking biochemical properties of particles to crocosms, BMC Microbiol. 14 (2014) 232.
particle-attached and free-living bacterial community structure along the 014-0232-4.