You are on page 1of 9

PAPER

Interactions Between Microorganisms and


Marine Microplastics: A Call for Research
AUTHORS ABSTRACT
Jesse P. Harrison Synthetic thermoplastics constitute the majority by percentage of anthropogenic
Department of Animal and Plant debris entering the Earth’s oceans. Microplastics (≤5-mm fragments) are rap-
Sciences, University of Sheffield idly emerging pollutants in marine ecosystems that may transport potentially toxic
Melanie Sapp chemicals into macrobial food webs. This commentary evaluates our knowledge
Michaela Schratzberger concerning the interactions between marine organisms and microplastics and iden-
The Centre for Environment, tifies the lack of microbial research into microplastic contamination as a significant
Fisheries and Aquaculture knowledge gap. Microorganisms (bacteria, archaea, and picoeukaryotes) in coastal
Science, Lowestoft Laboratory sediments represent a key category of life with reference to understanding and mitigat-
ing the potential adverse effects of microplastics due to their role as drivers of the global
A. Mark Osborn
functioning of the marine biosphere and as putative mediators of the biodegradation of
Department of Animal and Plant
plastic-associated additives, contaminants, or even the plastics themselves. As such,
Sciences, University of Sheffield
research into the formation, structure, and activities of microplastic-associated micro-
Department of Biological Sciences,
bial biofilms is essential in order to underpin management decisions aimed at safe-
University of Hull
guarding the ecological integrity of our seas and oceans.
Keywords: microplastics, microorganisms, marine, sediment, biodegradation

Introduction egy Framework Directive (Cheshire synthetic polymers sink in seawater,

W e live in the Plastic Age, with in-


dustrialized nations now reliant on
synthetic polymers in most aspects
et al., 2009; Galgani et al., 2010;
GESAMP, 2010).
Plastic waste is globally distributed
sediments function as sinks for the ac-
cumulation of plastic debris (Moore,
2008; Barnes et al., 2009). For exam-
of our lives. The worldwide demand across both surface waters and sedi- ple, up to 47.4 kg/km 2 of anthro-
for plastics is estimated to have annually ments within the marine environment, pogenic debris have been discovered
increased by 10% since the 1950s, with reflecting the widespread use of poly- in the Eastern Mediterranean seabed,
their total mass of production reaching mer products and their ability to resist over half of which was comprised by
245 million tons in 2006 (Andrady physical and biological degradation for plastic (Koutsodendris et al., 2008).
and Neal, 2009; PlasticsEurope, centuries (Galgani et al., 2000; Moore In comparison, 5.1 kg/km2 of floating
2008). Given this 600-fold increase in et al., 2001; Katsanevakis and Katsarou, plastics have been described in the
predicted consumption during the 2004; Sudhakar et al., 2007a, 2007b; North Pacific Central Gyre (Moore
past 60 years, synthetic thermoplastics Andrady and Neal, 2009). The envi- et al., 2001; Ryan et al., 2009).
(e.g., polyethylene) comprise the most ronmental fate of this waste is controlled The ubiquity and persistence of syn-
abundant and rapidly growing com- by human activities and hydrogeological thetic polymers are promoting global
ponent of anthropogenic debris enter- factors (e.g., littering, accidental dis- public concern about the impacts of
ing the Earth’s oceans (Derraik, 2002; posal, and oceanic circulation), with plastic pollution on marine wildlife.
Moore, 2008; Barnes et al., 2009; an excess of 200,000 plastic fragments These impacts are most apparent
Law et al., 2010). The increasing sig- having been discovered within a square when considering the risks of entangle-
nificance of this debris as a descriptor of kilometer of water in the North Atlan- ment in and ingestion of readily visible
the ecological integrity of marine eco- tic Subtropical Gyre (Galgani et al., (≥5 mm) fragments of plastic by higher
systems is recognized in environmental 2000; Katsanevakis and Katsarou, organisms, such as birds and fish (Laist,
treaties across the globe, including the 2004; Morishige et al., 2007; Law 1987; Derraik, 2002; Moore, 2008;
multilateral European Marine Strat- et al., 2010). Since the majority of Gregory, 2009). Other impacts of plastic

12 Marine Technology Society Journal


waste on marine animals include the ond, a brief appraisal of the role of two billion microscopic fragments of
transport of invasive species and altera- microorganisms as drivers of the func- plastic have been estimated to have
tions in the structure of macrobial com- tioning of marine ecosystems is pro- entered Californian coastal waters over
munities in the seabed (Barnes, 2002; vided. Third, published studies into 3 days, merely via two rivers (Moore
Katsanevakis et al., 2007; Gregory, microbial-plastic interactions are ex- et al., 2005). Moreover, at an intertidal
2009). plored with the aim of identifying site near a ship-wrecking yard in India,
Within the last decade, increasing key opportunities for future research. microplastics have been discovered in
attention has been directed toward Given the role of the sediment envi- the sediment at a concentration of
the proliferation and potential envi- ronment as a sink for plastic pollution, 81 parts per million (Reddy et al., 2006).
ronmental impacts of microplastics emphasis is given to microbial-plastic While microplastics may represent
(≤5-mm fragments) in marine eco- interactions in the seabed. a physical hazard to marine animals
systems (Figure 1) (Thompson et al., as in the case of larger plastic fragments
2004; Arthur et al., 2009; Barnes (e.g., via ingestion), their prevalence,
et al., 2009). However, we only possess high bioavailability and surface area-
an elementary understanding of the The Emergence and to-volume ratio have promoted signifi-
interactions of this debris with higher Potential Impacts cant additional concern over the ability
organisms (Barnes et al., 2009). In ad- of Microplastics of this type of debris to function as a
dition, although microorganisms (bac- Although the accumulation of substrate for the accumulation on and
teria, archaea, and picoeukaryotes) small fragments of plastics in the ma- transport of plastic additives and persis-
mediate functions that sustain life in rine environment has been recognized tent organic pollutants (e.g., polycyclic
our oceans and could facilitate the since the 1970s, research into their aromatic hydrocarbons and polychlori-
breakdown of microplastic-associated sources, distribution, fate, and ecolog- nated biphenyls) (Mato et al., 2001;
chemical compounds or even of the ical impacts has only gained momen- Masó et al., 2003; Rios et al., 2007;
debris itself, little research has been di- tum during the last decade, following Teuten et al., 2007; Karapanagioti and
rected toward assessing the interactions the identification of microplastics as a Klontza, 2008; Teuten et al., 2009;
between microplastics and microbial distinct category of anthropogenic de- Colabuono et al., 2010). The selective
communities in marine ecosystems. bris (Carpenter et al., 1972; Carpenter ingestion and subsequent bioaccu-
This commentary assesses our and Smith, 1972; Colton et al., 1974; mulation of microplastics has been
knowledge concerning the potential Morris and Hamilton, 1974; Thompson demonstrated for suspension- and
ecological impacts of microplastics on et al., 2004; Arthur et al., 2009). Since deposit-feeding invertebrates at the
marine organisms in order to identify then, it has become evident that micro- base of marine food webs, and there is
avenues for novel microbial research. plastics are entering marine habitats at partial evidence for the transport of
First, our understanding concerning a global scale, either as a result of the these fragments to higher trophic levels
the interactions between microplastics photo-oxidative, hydrolytic, and me- (Eriksson and Burton, 2003; Thompson
and higher organisms is evaluated. Sec- chanical breakdown of larger plastics et al., 2004; Teuten et al., 2007; Browne
or as components of industrial and do- et al., 2008; Graham and Thompson,
mestic waste (Thompson et al., 2004; 2009; Teuten et al., 2009). It has
FIGURE 1 Koutny et al., 2006; Ng and Obbard, been estimated that the presence of a
2006; Browne et al., 2007; Moore, single microgram of phenanthrene-
Scanning electron microscope image of poly-
ethylene microfragments. 2008; Barnes et al., 2009; Corcoran contaminated polyethylene in a gram
et al., 2009; Fendall and Sewell, of sediment significantly increased the
2009). Therefore, microplastics are body burden of this priority contami-
likely to constitute the numerically nant for the lugworm Arenicola marina
most abundant type of plastic debris (Teuten et al., 2007). The desorption of
in marine ecosystems, particularly in plastic-associated contaminants in the
coastal environments (Barnes et al., gut has also been demonstrated for sea-
2009; Corcoran et al., 2009; Browne birds (Teuten et al., 2009). As such,
et al., 2010). For example, at least microplastics may constitute a threat to

March/April 2011 Volume 45 Number 2 13


the functioning of marine ecosystems, and light) are thought to structure the their ingestion (Deines et al., 2007;
which parallels that of engineered nano- local composition and activities of mi- Graham and Thompson, 2009). A
materials (Zhu et al., 2006; Blickey and crobial communities in the seafloor at general summary of the potential yet
McClellan-Green, 2008; Koehler et al., the scale of millimeters (Edlund et al., primarily uncharacterized interactions
2008). 2008; Köster et al., 2008; Wu et al., between microplastics, plastic-associated
In the following sections, the signif- 2008). The responsiveness of these additives, contaminants, microbial as-
icance of microorganisms in the main- communities to variation in habitat semblages, and higher organisms is pro-
tenance of the ecological integrity of the physicochemistry and the availability vided in Figure 2.
marine environment and in potential in- of growth substrata render the com- Despite long-standing evidence for
teractions with synthetic microplastics is position and metabolic activities of mi- the ability of floating fragments of
further illustrated. For a comprehensive crobial assemblages within the seafloor plastic to function as sites for microbial
discussion of how microorganisms drive potentially vulnerable to perturbation. attachment and the subsequent forma-
the biogeochemistry of marine ecosys- Moreover, most of the biogeochemical tion of plastic-associated biofilms, the
tems, the reader is referred to reviews transformations mediated by marine interactions between microorganisms
by Arrigo (2005), Azam and Malfatti microorganisms occur in coastal sedi- and plastic debris in aquatic ecosys-
(2007), Karl (2007), Falkowski et al. ments, which are at greater risk of ex- tems have received limited attention
(2008), and Strom (2008). posure to human activities (including (Carpenter et al., 1972; Carpenter
the disposal of synthetic plastics) than and Smith, 1972; Morris and Hamilton,
off-shore sites (Walsh, 1991; Moore, 1974). In fact, evidence for the ecolog-
2008; Wu et al., 2008). ical impacts of plastic debris on micro-
Microorganisms and the Given the high metabolic potential organisms in these environments is
Marine Biosphere of microbial communities in the sea- largely restricted to demonstrations of
Microorganisms are incredibly floor, coastal habitats represent an un- the colonization of and survival on poly-
abundant in marine ecosystems and tapped resource of microbial taxa that mer surfaces by bacteria and algae in sea-
may reach up to hundreds of millions may contribute to the biodegradation water (Masó et al., 2003; Webb et al.,
of bacterial cells in a gram of wet ma- of plastics and plastic-associated com- 2009; Dang et al., 2008; Tatchou-
rine sediment (Amann et al., 1995; pounds (Wu et al., 2008). In order to Nyamsi-König et al., 2008, 2009).
Sievert et al., 1999). The metabolically guide both environmental and applied Detailed accounts of our understand-
active fraction of these cells underpins research into the responses of micro- ing concerning the prerequisites and
the functioning of marine food webs organisms to marine microplastics, it mechanisms underlying the microbial
by catalyzing redox reactions that con- is pertinent to consider existing research biodegradation of plastics have been
trol primary productivity and the cy- into microbial-plastic interactions. provided by Chiellini et al. (2003), Gu
cling of nutrients (including nitrogen, (2003), Kawai et al. (2004), Koutny
phosphorus, and sulphur) in the oceans et al. (2006), Lucas et al. (2008), Shah
(López-Urrutia et al., 2006; Hamasaki et al. (2008), and Eubeler et al. (2010).
et al., 2007; Falkowski et al., 2008; Interactions Between The biodegradability of synthetic
Gasol et al., 2008). As such, the entire Plastics and Microorganisms polymers is thought to depend on the
marine carbon cycle is tightly coupled Microbial assemblages in marine type and chemical properties of the
to elemental cycles that are exclusively sediments may catalyze metabolic re- plastic, the environment (e.g., season-
mediated by microorganisms (Arrigo, actions that contribute to the absorp- ality and the availability of oxygen) and
2005; Madsen, 2008). tion, desorption and breakdown of metabolic interactions within plastic-
Marine sediments provide habitats microplastic-associated compounds or associated biofilms (Bonhomme et al.,
for microbial growth that are funda- even the breakdown of the debris itself. 2003; Gilan et al., 2004; Artham
mentally different from those in the Moreover, microplastics may function et al., 2009). Although research into
water column (Falk et al., 2007). Hor- as sites for the colonization of micro- the biotransformation of plastics has
izontal and vertical gradients of physi- organisms that possess the capacity to focused on microorganisms from ter-
cal and geochemical parameters (e.g., influence the ecology and resident mi- restrial habitats (e.g., Chiellini et al.,
pH, oxygen, organic carbon, nutrients, croflora of higher organisms following 2003; Arkatkar et al., 2009), a limited

14 Marine Technology Society Journal


FIGURE 2 et al., 2008). This control of eco-
system functioning by microbial
A schematic illustrating potential interactions between marine microorganisms (bacteria, archaea,
and picoeukaryotes) and synthetic microplastics in relation to the wider environmental impacts interactions, coupled to advances
of this debris. The filled arrows indicate interactions for which experimental evidence exists, and in molecular methodologies, has
the white arrows correspond to interactions that have not been explored within marine sediments. encouraged interest in the utiliza-
The colonization of microplastics by microbial assemblages may (a) occur directly, (b) depend on tion of prokaryotes and microbial
the presence of plastic-associated organic compounds, (c) occur following ingestion by higher eukaryotes as sensitive indicators
organisms and/or become influenced by the gut microflora, (d) mediate activities contributing
of ecosystem health (Paerl et al.,
to the biodegradation of plastic-associated chemicals or the plastics themselves, potentially influ-
encing the extent and severity of the (e) chemical and (f) physical impacts of microplastics on
2003; Cao et al., 2006; Chiu et al.,
higher organisms. 2008; Mars hall et al., 2008;
Mojtahid et al., 2008; Tett et al.,
2008). In this respect, research
into the potential for the deposi-
tion of microplastics into the ma-
rine environment to impact on
microbially mediated biogeo-
chemical processes is of signifi-
cant interest.
2. Wider research into the colonization
and biodegradation of synthetic poly-
mers by microorganisms
number of experiments have character- search into the interactions between There is a fundamental lack of in-
ized the capacity of microbial assem- marine microorganisms and synthetic formation concerning the potential
blages in the water column to utilize microplastics: for microplastics in marine ecosys-
synthetic polymers as a resource for 1. Fundamental research into the eco- tems to function as hotspots for the
growth (Table 1). Only two studies logical responses of microorganisms attachment of microbial assemblages
have examined the potential for sedi- to the deposition of microplastics and originating from the wider environ-
ment microorganisms in marine ecosys- plastic-associated chemicals into our ment. Furthermore, our understand-
tems to biodegrade plastic debris (Kumar seas and oceans ing concerning the biodegradation
et al., 2007; Balasubramanian et al., In order to facilitate the manage- of plastics and plastic-associated
2010). Overall, the rates of degradation ment of microplastic pollution, compounds is constrained by the
of plastics in marine systems are likely to our efforts must be focused on un- fact that most research into this
be significantly lower than in their ter- derstanding how the deposition of topic has been based on the utiliza-
restrial counterparts due to the low avail- this debris into sediment habitats tion of culture-based methodologies
ability of oxygen and light (Barnes et al., affects those taxa and life stages or unidentified microbial assem-
2009). Moreover, unequivocal evidence that are most likely to be exposed blages (Table 1). Only 1% or fewer
for the biodegradation of plastics is yet to microplastics and which mediate of all bacterial taxa are thought to be
to emerge because it is unclear whether ecosystem services that sustain ma- cultivable in the laboratory (Amann
microbial activities actively degrade the rine life (Arthur et al., 2009; Galgani et al., 1995). Therefore it is likely
plastic, exploit plastic-associated chem- et al., 2010). While we are beginning that most marine microorganisms
icals, or both (Koutny et al., 2006; to address these questions with refer- potentially participating in the
Lucas et al., 2008; Eubeler et al., 2010). ence to invertebrate species at the degradation of plastic debris and
base of macrobial food webs, it is plastic-associated chemicals remain
pertinent to recognize that micro- undiscovered and could be charac-
Opportunities for organisms underpin the functioning terized by culture-independent
Future Research of marine ecosystems by driving pri- molecular analyses. Since culture-
This commentary has highlighted mary productivity and elemental independent methods (e.g., mi-
several potential avenues for novel re- cycling (Madsen, 2005; Falkowski croscopy, gene sequencing and

March/April 2011 Volume 45 Number 2 15


TABLE 1
Examples of existing research into the biodegradation of synthetic plastics by pelagic microorganisms.

Microbial Taxa Plastic Type Environment Exposure Comments References


Pseudomonas sp. B2 Polycarbonate film Marine In situ and in vitro 9% loss of mass over Artham and Doble
containing bisphenol 12 months, leaching of (2009)
A (BPA) BPA
Unidentified consortium Polycarbonate, Marine In situ Degradation dependent Artham et al.
polyethylene and on plastic type and (2009)
polypropylene season
coupons
Unidentified consortium Polyethylene film Freshwater In situ Degradation dependent Chiellini et al.
containing pro-oxidant on degree of polymer (2007)
additives oxidation
Unidentified consortium Polyethylene films with Marine In situ and in vitro Little or no evidence Rutkowska et al.
and without starch for degradation over (2002a)
additive 20 months
Unidentified consortium Polyurethane sheets Marine In situ and in vitro Degradation dependent on Rutkowska et al.
polymeric cross-linking (2002b)
Bacillus cereus, Nylon pellets Marine In vitro Degradation varied Sudhakar et al.
B. sphericus, Vibrio across microbial taxa (2007a)
furnisii, Brevundimonas (highest for B. cereus)
vesicularis
Pseudomonas spp., Polyethyelene and Marine In situ Degradation dependent Sudhakar et al.
Clostridium spp., polypropylene sheets on study site, plastic (2007b)
unidentified anaerobic, type and season
hetetrophic and iron-
reducing bacteria, fungi
B. cereus subgroup A, Polyethylene sheets Marine In vitro Degradation dependent Sudhakar et al.
B. sphericus GC on type of polyethylene (2008)
subgroup IV

community fingerprinting) are sediment and in contact with higher Acknowledgments


also pivotal in the monitoring of organisms JPH was funded by a Collaborative
marine environmental change, These investigations must be com- Awards in Science and Engineering
the applications of microbial ecol- bined with attempts to characterize (CASE) Ph.D. studentship awarded
ogy in improving our ability to the potential for the in situ bio- by the Natural Environment Research
understand the potential adverse transformation of microplastic- Council (reference NE/G524136/1),
effects of global microplastic pol- associated additives, contaminants, with CASE funding from the Centre
lution are bound to offer sig- and the polymers themselves. for Environment, Fisheries, and Aqua-
nificant opportunities for future Together with a combination of culture Science.
research (Osborn et al., 2000; traditional and molecular micro-
Daims et al., 2005; Röling and biological tools, an experimental Lead Author:
Head, 2005). approach to unraveling microbial- Jesse P. Harrison
3. Research in order to determine spatio- microplastic interactions will be es- Department of Animal
temporal patterns in the taxonomic sential to the translation of primary and Plant Sciences
composition and functional poten- research into management mea- University of Sheffield, Sheffield
tial of plastic-colonizing microbial sures aimed at the safeguarding of S10 2TN, U.K.
assemblages in different types of marine life. Email: bop08jph@sheffield.ac.uk

16 Marine Technology Society Journal


References Barnes, D.K.A., Galgani, F., Thompson, Westphalen, G. 2009. UNEP/IOC Guide-
Amann, R.I., Ludwig, W., & Schleifer, K.-H. R.C., & Barlaz, M. 2009. Accumulation and lines on Survey and Monitoring of Marine
1995. Phylogenetic identification and in situ fragmentation of plastic debris in global envi- Litter. UNEP Regional Seas Reports and
detection of individual microbial cells without ronments. Philos Trans R Soc B. 364:1985-98. Studies, No. 186. IOC Technical Series
cultivation. Microbiol Rev. 59:143-69. doi: 10.1098/rstb.2008.0205. No. 83. xii + 120 pp.

Andrady, A.L., & Neal, M.A. 2009. Blickey, T.M., & McClellan-Green, P. 2008. Chiellini, E., Corti, A., & D’Antone, S.
Applications and societal benefits of plastics. Toxicity of aqueous fullerene in adult and 2007. Oxo-biodegradable full carbon back-
Philos Trans R Soc B. 364:1977-84. larval Fundulus heteroclitus. Environ Toxicol bone polymers—Biodegradation behaviour of
doi: 10.1098/rstb.2008.0304. Chem. 27:1964-71. doi: 10.1897/07-632.1. thermally oxidized polyethylene in an aqueous
medium. Polym Degrad Stabil. 92:1378-83.
Arkatkar, A., Arutchelvi, J., Bhaduri, S., Bonhomme, S., Cuer, A., Delort, A.-M.,
doi: 10.1016/j.polymdegradstab.2007.03.007.
Uppara, P.V., & Doble, M. 2009. Degradation Lemaire, J., Sancelme, M., & Scott, G. 2003.
of unpretreated and thermally pretreated Environmental biodegradation of polyethylene. Chiellini, E., Corti, A., & Swift, G. 2003.
polypropylene by soil consortia. Int Biodeter Polym Degrad Stabil. 81:441-52. doi: 10.1016/ Biodegradation of thermally-oxidized, frag-
Biodegr. 63:106-11. doi: 10.1016/ S0141-3910(03)00129-0. mented low-density polyethylenes. Polym
j.ibiod.2008.06.005. Degrad Stabil. 81:341-51. doi: 10.1016/
Browne, M.A., Dissanayake, A., Galloway,
S0141-3910(03)00105-8.
Arrigo, K.R. 2005. Marine microorganisms T.S., & Thompson, R.C. 2008. Ingested
and global nutrient cycles. Nature. 437:349-55. microscopic plastic translocates to the circu- Chiu, J.M.Y., Zhang, R., Wang, H.,
doi: 10.1038/nature04159. latory system of the mussel, Mytilus edulis (L). Thiyagarajan, V., & Qian, P.Y. 2008. Nutrient
Environ Sci Technol 42:5026-31. effects on intertidal community: From bacteria to
Artham, T., & Doble, M. 2009. Fouling and doi: 10.1021/es800249a. invertebrates. Mar Ecol Prog Ser. 358:41-50.
degradation of polycarbonate in seawater: doi: 10.3354/meps07310.
Field and lab studies. J. Polym. Environ. Browne, M.A., Galloway, T.S., & Thompson,
17:170-80. doi: 10.1007/s10924-009-0135-x. R.C. 2007. Microplastic—An emerging con- Colabuono, F.I., Taniguchi, S., & Montone,
taminant of potential concern. Integr Environ R.C. 2010. Polychlorinated biphenyls and
Artham, T., Sudhakar, M., Venkatesan, R., organochlorine pesticides in plastics ingested
Assess Manage 3:559-66. doi: 10.1002/
Nair, C.M., Murty, K.V.G.K., & Doble, M. by seabirds. Mar Pollut Bull. 60:630-4.
ieam.5630030412.
2009. Biofouling and stability of synthetic doi: 10.1016/j.marpolbul.2010.01.018.
polymers in sea water. Int Biodeter Biodegr. Browne, M.A., Galloway, T.S., & Thompson,
63:884-90. doi: 10.1016/j.ibiod.2009.03.003. R.C. 2010. Spatial patterns of plastic debris Colton, J.B., Knapp, F.D., & Burns, B.R.
along estuarine shorelines. Environ Sci Technol 1974. Plastic particles in surface waters of the
Arthur, C., Baker, J., & Bamford, H. (eds.) northwestern Atlantic. Science. 185:491-7.
44:3404-9. doi: 10.1021/es903784e.
2009. Proceedings of the International Research doi: 10.1126/science.185.4150.491.
Workshop on the Occurrence, Effects and Cao, Y., Cherr, G.N., Córdova-Kreylos,
Fate of Microplastic Marine Debris. Sep. 9-11, A.L., Fan, T.W.-M., Green, P.G., Higashi, Corcoran, P.L., Biesinger, M.C., & Grifi, M.
2008. NOAA Technical Memorandum NOS- R.M., … Holden, P.A. 2006. Relationships 2009. Plastics and beaches: A degrading
OR&R-30. pp. 530. Silver Spring, MD: NOAA. between sediment microbial communities and relationship. Mar Pollut Bull. 58:80-4.
pollutants in two California salt marshes. doi: 10.1016/j.marpolbul.2008.08.022.
Azam, F., & Malfatti, F. 2007. Microbial
Microbial Ecol. 52:619-33. doi: 10.1007/
structuring of marine ecosystems. Nat Rev Daims, H., Stoecker, K., & Wagner, M.
s00248-006-9093-1.
Microbiol. 5:782-91. doi: 10.1038/nrmicro1747. 2005. Fluorescence in situ hybridization for
Carpenter, E.J., Anderson, S.J., Harvey, the detection of prokaryotes. In: Molecular
Balasubramanian, V., Natarajan, K.,
G.R., Miklas, H.P., & Beck, B.B. 1972. Microbial Ecology, eds. Osborn, A.M., Smith,
Hemambika, B., Ramesh, N., Sumathi, C.S.,
Polystyrene spherules in coastal waters. C.J., 213-39. New York; Abingdon, U.K.:
Kottaimuthu, R., & Kannan, V.R. 2010.
Science. 178:749-50. doi: 10.1126/ Taylor and Francis Group.
High-density polyethylene (HDPE)-degrading
science.178.4062.749.
potential bacteria from marine ecosystem of Dang, H., Li, T., Chen, M., & Huang, G.
Gulf of Mannar, India. Lett Appl Microbiol. Carpenter, E.J., & Smith, K.L., Jr. 1972. 2008. Cross-ocean distribution of Rhodobacterales
51:205-11. doi: 10.1111/j.1472- Plastics on the Sargasso Sea surface. bacteria as primary surface colonizers in temperate
765X.2010.02883.x Science. 175:1240-41. doi: 10.1126/ coastal marine waters. Appl Environ Microbiol.
science.175.4027.1240. 74:52-60. doi: 10.1128/AEM.01400-07.
Barnes, D.K.A. 2002. Invasions by marine
life on plastic debris. Nature. 416:808-9. Cheshire, A.C., Adler, E., Barbière, J., Deines, P.D., Bodelier, P.L.E., & Eller, G.
doi: 10.1038/416808a. Cohen, Y., Evans, S., Jarayabhand, S., … 2007. Methane-derived carbon flows through

March/April 2011 Volume 45 Number 2 17


methane-oxidizing bacteria to higher trophic Galgani, F., Leaute, J.P., Moguedet, P., of virgin plastic pellets and plastic eroded
levels in aquatic systems. Environ Microbiol. Souplet, A., Verin, Y., Carpentier, A., … pellets founds on Lesvos Island beaches
9:1126-34. doi: 10.1111/j.1462- Nerisson, P. 2000. Litter on the seafloor along (Greece). Mar Environ Res. 65:283-90.
2920.2006.01235.x. European coasts. Mar Pollut Bull. 40:516-27. doi: 10.1016/j.marenvres.2007.11.005.
doi: 10.1016/S0025-326X(99)00234-9.
Derraik, J.G.B. 2002. The pollution of the Karl, D.M. 2007. Microbial oceanography:
marine environment by plastic debris: A Gasol, J.M., Pinhassi, J., Alonso-Sáez, L., Paradigms, processes and promise. Nat Rev
review. Mar Pollut Bull. 44:842-52. Ducklow, H., Herndl, G.J., Koblížek, M., … Microbiol. 5:759-69. doi: 10.1038/
doi: 10.1016/S0025-326X(02)00220-5. Simon, M. 2008. Towards a better understand- nrmicro1749.
ing of microbial carbon flux in the sea. Aquat
Edlund, A., Hårdeman, F., Jansson, J.K., & Katsanevakis, S., & Katsarou, A. 2004.
Microb Ecol. 53:21-38. doi: 10.3354/ame01230.
Sjöling, S. 2008. Active bacterial community Influences on the distribution of marine debris
structure along vertical redox gradients in GESAMP (IMO/FAO/UNESCO-IOC/ on the seafloor of shallow coastal areas in
Baltic Sea sediment. Environ Microbiol. UNIDO/ WMO/IAEA/UN/UNEP Joint Greece (Eastern Mediterranean). Water Air
10:2051-63. doi: 10.1111/j.1462-2920. Group of Experts on the Scientific Aspects Soil Pollut. 159:325-37. doi: 10.1023/B:
2008.01624.x. of Marine Environmental Protection). 2010. WATE.0000049183.17150.df.
Eriksson, C., & Burton, H. 2003. Origins Report of the thirty-seventh session of
GESAMP, Bangkok, 14–19 February 2010. Katsanevakis, S., Verriopoulos, G., Nicolaidou,
and accumulation of small plastic particles in
Rep. Stud. GESAMP No. 81. 109 pp. A., & Thessalou-Legaki, M. 2007. Effect of
fur seals from Macquarie Island. AMBIO.
marine litter on the benthic megafauna of
32:380-4. Gilan, I., Hadar, Y., & Sivan, A. 2004. coastal soft bottoms: A manipulative field
Eubeler, J.P., Bernhard, M., & Knepper, T.P. Colonization, biofilm formation and biodeg- experiment. Mar Pollut Bull. 54:771-8.
2010. Environmental biodegradation of syn- radation of polyethylene by a strain of doi: 10.1016/j.marpolbul.2006.12.016.
thetic polymers: II. Biodegradation of different Rhodococcus ruber. Appl Microbiol Biotechnol.
65:97-104. Kawai, F., Watanabe, M., Shibata, M.,
polymer groups. Trends Anal Chem. 29:84-100.
Yokoyama, S., Sudate, Y., & Hayashi, S.
doi: 10.1016/j.trac.2009.09.005.
Graham, E.R., & Thompson, J.T. 2009. 2004. Comparative study on biodegrad-
Falk, S., Hannig, M., Gliesche, C., Wardenga, Deposit- and suspension-feeding sea cucumbers ability of polyethylene wax by bacteria and
R., Köster, M., Jürgens, K., & Braker, G. 2007. (Echinodermata) ingest plastic fragments. fungi. Polym Degrad Stabil. 86:105-14.
nirS-containing denitrifier communities J Exp Mar Biol Ecol. 368:22-9. doi: 10.1016/ doi: 10.1016/j.polymdegradstab.2004.03.015.
in the water column and sediment of the j.jembe.2008.09.007.
Baltic Sea. Biogeosciences. 4:255-68. Koehler, A., Marx, U., Broeg, K., Bahns, S.,
Gregory, M.R. 2009. Environmental impli- & Bressling, J. 2008. Effects of nanoparticles
doi: 10.5194 /bg-4-255-2007.
cations of plastic debris in marine settings— in Mytilus edulis gills and hepatopancreas—
Falkowski, P.G., Fenchel, T., & Delong, E.F. Entanglement, ingestion, smothering, hangers- A new threat to marine life? Mar Environ
2008. The microbial engines that drive Earth’s on, hitch-hiking and alien invasions. Philos Res. 66:12-4. doi: 10.1016/j.marenvres.
biogeochemical cycles. Science. 320:1034-9. Trans R Soc B. 364:2013-25. doi: 10.1098/ 2008.02.009.
doi: 10.1126/science.1153213. rstb.2008.0265.
Köster, M., Wardenga, R., & Blume, M.
Fendall, L.S., & Sewell, M.A. 2009. Con- Gu, J. 2003. Microbiological deterioration 2008. Microscale investigations of microbial
tributing to marine pollution by washing your and degradation of synthetic polymeric mate- communities in coastal surficial sediments.
face: Microplastics in facial cleansers. Mar rials: Recent research advances. Int Biodeter. Mar Ecol. 29:89-105. doi: 10.1111/
Pollut Bull. 58:1225-8. doi: 10.1016/ Biodegr. 52:69-91. doi: 10.1016/S0964- j.1439-0485.2007.00219.x.
j.marpolbul.2009.04.025. 8305(02)00177-4.
Koutny, M., Lemaire, J., & Delort, A. 2006.
Galgani, F., Fleet, D., Van Franeker, J.,
Hamasaki, K., Taniguchi, A., Tada, Y., Long, Biodegradation of polyethylene films with pro-
Katsanevakis, S., Maes, T., Mouat, J., …
R.A., & Azam, F. 2007. Actively growing oxidant additives. Chemosphere. 64:1243-52.
Janssen, C. 2010. Marine Strategy Framework
bacteria in the Inland Sea of Japan, identified by doi: 10.1016/j.chemosphere.2005.12.060.
Directive–Task Group 10 Report Marine
combined bromodeoxyuridine immunocapture
Litter. JRC Scientific and Technical Reports, Koutsodendris, A., Papatheodorou, G.,
and denaturing gradient gel electrophoresis.
Publications Office of the European Union, Kougiourouki, O., & Georgiadis, M. 2008.
Appl Environ Microbiol. 73:2787-98.
Ed. Zampoukas, N., 57. EUR 24340 N Benthic marine litter in four Gulfs in Greece,
doi: 10.1128/AEM.02111-06.
OPOCE LB-NA-24340-EN-N. Luxembourg: Eastern Mediterranean; abundance, composition
Office for Official Publications of the European Karapanagioti, H.K., & Klontza, I. 2008. and source identification. Est Coast Shelf Sci.
Communities. Testing phenanthrene distribution properties 77:501-12. doi: 10.1016/j.ecss.2007.10.011.

18 Marine Technology Society Journal


Kumar, S., Hatha, A.A.M., & Christi, K.S. Environ Sci Technol. 35:318-24. Valdes, L.M. 2003. Microbial indicators of
2007. Diversity and effectiveness of tropical doi: 10.1021/es0010498. aquatic ecosystem change: Current applica-
mangrove soil microflora on the degradation tions to eutrophication studies. FEMS
Mojtahid, M., Jorissen, F., & Pearson, T.H.
of polythene carry bags. Rev Biol Trop. Microbiol Ecol. 46:233-46. doi: 10.1016/
2008. Comparison of benthic foraminiferal
55:777-86. S0168-6496(03)00200-9.
and macrofaunal responses to organic pollu-
Laist, D.W. 1987. Overview of the biological tion in the Firth of Clyde (Scotland). PlasticsEurope. 2008. The Compelling Facts
effects of lost and discarded plastic debris in the Mar Pollut Bull. 56:42-76. doi: 10.1016/ About Plastics, Analysis of Plastics Production,
marine environment. Mar Pollut Bull. 18:319-26. j.marpolbul.2007.08.018. Demand and Recovery for 2006 in Europe,
doi: 10.1016/S0025-326X(87)80019-X. January 2008. Brussels, Belgium: PlasticsEurope
Moore, C.J. 2008. Synthetic polymers in the
Association for Plastics Manufacturers.
Law, K.L., Morét-Ferguson, S., Maximenko, marine environment: A rapidly increasing,
N.A., Proskurowski, G., Peacock, E.E., long-term threat. Environ Res. 108:131-9. Reddy, M.S., Basha, S., Adimurthy, S., &
Hafner, J., & Reddy, C.M. 2010. Plastic doi: 10.1016/j.envres.2008.07.025. Ramachandraiah, G. 2006. Description of the
accumulation in the North Atlantic Sub- small plastics fragments in marine sediments
Moore, C.J., Lattin, G.L., & Zellers, A.F.
tropical Gyre. Science. 329:1185-8. along the Alang-Sosiya ship-breaking yard,
2005. Working our way upstream: A snapshot
doi: 10.1126/science.1192321. India. Est Coast Shelf Sci. 68:656-60.
of land-based contributions of plastic and
doi: 10.1016/j.ecss.2006.03.018.
López-Urrutia, A., San Martin, E., Harris, R.P., other trash to coastal waters and beaches of
& Irigoien, X. 2006. Scaling the metabolic Southern California. In: Proceedings of the Plastic Rios, L.M., Moore, C., & Jones, P.R. 2007.
balance of the oceans. Proc Natl Acad Sci USA. Debris Rivers to Sea Conference. Long Beach, Persistent organic pollutants carried by syn-
103:8739-44. doi: 10.1073/pnas.0601137103. CA: Algalita Marine Research Foundation. thetic polymers in the ocean environment.
Moore, C.J., Moore, S.L., Leecaster, M.K., & Mar Pollut Bull. 54:1230-7. doi: 10.1016/
Lucas, N., Bienaime, C., Belloy, C.,
Weisberg, S.B. 2001. A comparison of plastic j.marpolbul.2007.03.022.
Queneudec, M., Silvester, F., & Nava-Saucedo,
J.-E. 2008. Polymer biodegradation: Mecha- and plankton in the North Pacific Central
Röling, W.F.M., & Head, I.M. 2005.
nisms and estimation techniques. Chemo- Gyre. Mar Pollut Bull. 42:1297-300.
Prokaryotic systematic: PCR and sequence
sphere. 73:429-42. doi: 10.1016/ doi: 10.1016/S0025-326X(01)00114-X.
analysis of amplified 16S rRNA genes.
j.chemosphere.2008.06.064. In: Molecular Microbial Ecology,
Morishige, C., Donohue, M.J., Flint, E.,
Swenson, C., & Woolaway, C. 2007. Factors eds. Osborn, A.M., Smith, C.J., 25-63.
Madsen, E.L. 2005. Identifying microorgan-
affecting marine debris deposition at French New York; Abingdon, U.K.: Taylor and
isms responsible for ecologically significant
Frigate Shoals, Northwestern Hawaiian Francis Group.
biogeochemical processes. Nat Rev Microbiol.
3:439-46. doi: 10.1038/nrmicro1151. Islands Marine National Monument,
Rutkowska, M., Heimowska, A., Krasowska,
1990-2006. Mar Pollut Bull. 54:1162-9.
Madsen, E.L. 2008. Environmental Micro- K., & Janik, H. 2002a. Biodegradability of
doi: 10.1016/j.marpolbul.2007.04.014.
biology: From Genomes to Biogeochemistry polyethylene starch blends in seawater.
(1st Ed.). Malden, MA: Wiley-Blackwell Morris, A.W., & Hamilton, E.I. 1974. Pol J Environ Stud. 11:267-74.
Publishing. 496 pp. Polystyrene spherules in the Bristol Channel.
Rutkowska, M., Krasowska, K., Heimowska,
Mar Pollut Bull. 5:26-7. doi: 10.1016/
Marshall, M.M., Amos, R.N., Henrich, V.C., A., Steinka, I., & Janik, H. 2002b. Degrada-
0025-326X(74)90311-7.
& Rublee, P.A. 2008. Developing SSU rDNA tion of polyurethanes in seawater. Polym
metagenomic profiles of aquatic microbial Ng, K.L., & Obbard, J.P. 2006. Prevalence Degrad Stabil. 76:233-9. doi: 10.1016/
communities for environmental assessments. of microplastics in Singapore’s coastal marine S0141-3910(02)00019-8.
Ecol Indicat. 8:442-53. doi: 10.1016/ environment. Mar Pollut Bull. 52:761-7.
Ryan, P.G., Moore, C.J., van Franeker, J.A.,
j.ecolind.2007.04.007. doi: 10.1016/j.marpolbul.2005.11.017.
& Moloney, C.L. 2009. Monitoring the
Masó, M., Garcés, E., Pagès, F., & Camp, J. Osborn, A.M., Moore, E.R.B., & Timmis, K.N. abundance of plastic debris in the marine
2003. Drifting plastic debris as a potential 2000. An evaluation of terminal-restriction frag- environment. Philos Trans R Soc B.
vector for dispering harmful algal bloom ment length polymorphism (T-RFLP) analysis 364:1999-2012. doi: 10.1098/rstb.2008.0207.
(HAB) species. Sci Mar. 67:107-11. for the study of microbial community structure
Shah, A.A., Hasan, F., Hameed, A., &
and dynamics. Environ Microbiol. 2:39-50.
Mato, Y., Isobe, T., Takada, H., Kanehiro, Ahmed, S. 2008. Biological degradation
doi: 10.1046/j.1462-2920.2000.00081.x.
H., Ohtake, C., & Kaminuma, T. 2001. of plastics: A comprehensive review. Bio-
Plastic resin pellets as a transport medium for Paerl, H.W., Dyble, J., Moisander, P.H., technol Adv. 26:246-65. doi: 10.1016/
toxic chemicals in the marine environment. Noble, R.T., Piehler, M.F., Pinckney, J.L., … j.biotechadv.2007.12.005.

March/April 2011 Volume 45 Number 2 19


Sievert, S.M., Brinkhoff, T., Muyzer, G., hydrophobic contaminants. Environ Sci
Ziebis, W., & Kuever, J. 1999. Spatial Technol. 41:7759-64. doi: 10.1021/es071737s.
heterogeneity of bacterial populations along
Teuten, E.L., Saquing, J.M., Knappe, D.R.
an environmental gradient at a shallow sub-
U., Barlaz, M.A., Jonsson, S., Björn, A., …
marine hydrothermal vent near Milos Island
Takada, H. 2009. Transport and release
(Greece). Appl Environ Microbiol. 65:3834-42.
of chemicals from plastics to the environment
Strom, S.L. 2008. Microbial ecology of and to wildlife. Philos Trans R Soc B.
ocean biogeochemistry: A community per- 364:2027-45. doi: 10.1098/rstb.2008.0284.
spective. Science. 320:1043-5. doi: 10.1126/
Thompson, R.C., Olsen, Y., Mitchell, R.P.,
science.1153527.
Davis, A., Rowland, S.J., John, A.W.G., …
Sudhakar, M., Doble, M., Murthy, P.S., & Russell, A.W. 2004. Lost at sea: Where is all
Venkatesan, R. 2008. Marine microbe-mediated the plastic? Science. 304:838. doi: 10.1126/
biodegradation of low- and high-density poly- science.1094559.
ethylenes. Int Biodet Biodegr. 61:203-13.
Walsh, J.J. 1991. Importance of continental
doi: 10.1016/j.ibiod.2007.07.011.
margins in the marine biogeochemical cycling
Sudhakar, M., Priyadarshini, C., Doble, M., of carbon and nitrogen. Nature. 350:53-5.
Murthy, P.S., & Venkatesan, R. 2007a. doi: 10.1038/350053a0.
Marine bacteria mediated degradation of nylon
Webb, H.K., Crawford, R.J., Sawabe, T., &
66 and 6. Int Biodet Biodegr. 60:144-51.
Ivanova, E.P. 2009. Poly(ethylene terephthalate)
doi: 10.1016/j.ibiod.2007.02.002.
polymer surfaces as a substrate for bacterial
Sudhakar, M., Trishul, A., Doble, M., attachment and biofilm formation. Microbes
Kumar, K.S., Jahan, S.S., Inbakandan, D., … Environ. 24:39-42. doi: 10.1264/
Venkatesan, R. 2007b. Biofouling and bio- jsme2.ME08538.
degradation of polyolefins in ocean waters.
Wu, L., Kellogg, L., Devol, A.H., Tiedje,
Polym Degrad Stabil. 92:1743-52.
J.M., & Zhou, J. 2008. Microarray-based
doi: 10.1016/j.polymdegradstab.2007.03.029.
characterization of microbial community
Tatchou-Nyamsi-König, J.-A., Dague, E., functional structure and heterogeneity in
Mullet, M., Duval, J.F.L., Gaboriaud, F., & marine sediments from the Gulf of Mexico.
Block, J.-C. 2008. Adhesion of Campylobacter Appl Environ Microbiol. 74:4516-29.
jejuni and Mycobacterium avium onto poly- doi: 10.1128/AEM.02751-07.
ethylene terephtalate (PET) used for
Zhu, S., Oberdörster, E., Haasch, M.L. 2006.
water bottles. Water Res. 42:4751-60.
Toxicity of an engineered nanoparticle
doi: 10.1016/j.watres.2008.09.009.
(fullerene, C60) in two aquatic species,
Tatchou-Nyamsi-König, J.-A., Dailloux, M., Daphnia and fathead minnow. Mar
& Block, J.-C. 2009. Survival of Mycobacterium Environ Res. 62:S5-9. doi: 10.1016/
avium attached to polyethylene terephthalate j.marenvres.2006.04.059.
(PET) water bottles. J Appl Microbiol.
106:825-32. doi: 10.1111/j.1365-2672.
2008.04050.x.

Tett, P., Carreira, C., Mills, D.K., van


Leeuwen, S., Foden, J., Bresnan, E., &
Gowen, R.J. 2008. Use of a phytoplankton
community index to assess the health of
coastal waters. ICES J Mar Sci. 65:1475-82.
doi: 10.1093/icesjms/fsn161.

Teuten, E.L., Rowland, S.J., & Galloway,


T.S. 2007. Potential for plastics to transport

20 Marine Technology Society Journal

You might also like