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 International Biodeterioration & Biodegradation 88 (2014) 83e90

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journal homepage: www.elsevier.com/locate/ibiod

Review

Microbial degradation and deterioration of polyethylene e A review

Juan-Manuel Restrepo-Flórez a, Amarjeet Bassi a, *, Michael R. Thompson b
a
Chemical and Biochemical Engineering, University of Western Ontario, 1151 Richmond Street, London, Ontario, Canada N6A 3K7
b
Department of Chemical Engineering, McMaster University, 1280 Main Street West, Hamilton, Ontario, Canada L8S 4L8

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

Article history: The ability of microorganisms to use polyethylene as a carbon source has only been recently established.
Received 4 November 2013 This result has significance both from an environmental point of view, due to the accumulation of
Received in revised form millions of tons of waste plastics every year, but also regarding the conservation of integrity for in-
19 December 2013
frastructures incorporating this plastic. A number of microorganisms with the ability to grow on poly-
Accepted 20 December 2013
Available online
ethylene have been isolated. The effects of these microorganisms on the physiochemical properties of
this polymer have been described; these include changes in crystallinity, molecular weight, topography
of samples and the functional groups found on the surface. Although the bio-degradation and bio-
Keywords:
Polyethylene
deterioration of polyethylene has been demonstrated by several researchers, the enzymes involved
Biodegradation and mechanisms associated with these phenomena are still unclear. Nevertheless, it is recognized that
Biodeterioration both enzymatic and abiotic factors (such UV light) can mediate the initial oxidation of polyethylene
chains, and given the chemical similarity between polyethylene and olefins it has been suggested that
the metabolic pathways for degradation of hydrocarbons can be used once the size of polyethylene
molecules decrease to an acceptable range for enzyme action (typically from 10 to 50 carbons). The long-
range structure and morphology of polyethylene have shown important roles, with amorphous regions
being more prone to microbial attack than crystalline ones. This review focuses on the recent hypotheses
and experimental findings regarding the biodegradation of polyethylene.
Ó 2014 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1
2. Microorganisms involved in polyethylene degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .2
3. Effect of microbial activity on polyethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3
3.1. Functional groups on the surface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.2. Hydrophobicity/Hydrophilicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.3. Crystallinity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.4. Molecular weight distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.5. Surface topography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.6. Mechanical properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.7. Consumption of the polymer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Mechanisms of polyethylene biodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .5
5. Conclusion and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .6
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

1. Introduction

Polyethylene is known for being a remarkably resistant polymer

to degradation. Its chemical and biological inertness has fostered its
application into various products from plastic bags and piping to
* Corresponding author. Tel.: þ1 519 661 2111x88324/88219. the construction of fuel storage tanks. From an ecological point of
E-mail address: abassi@uwo.ca (A. Bassi).

0964-8305/$ e see front matter Ó 2014 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ibiod.2013.12.014
84 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90
view, the accumulation of plastic debris in the environment is a
growing concern, as the rate of plastics manufacture goes over
25 million tons per year (Orhan and Büyükgüngör, 2000). However,
the study of degradation pathways of polyethylene is not only of
interest because of its ecological impact. Polyethylene has become a
critical material in the construction of key infrastructures to several
industries, making its degradation and deterioration necessary to
understand from the view point of stability and integrity.
Degradation of polyethylene can be classified as abiotic or biotic,
the former being defined as deterioration caused by environmental
factors such as temperature, UV irradiation, while the latter is
defined as biodegradation caused by the action of microorganisms
that modify and consume the polymer leading to changes in its
properties. It is important to highlight that although the damage to
polyethylene is classified by only one of these two damage modes,
in nature it is typical that both act cooperatively (Hakkarainen and
Albertsson, 2004). The abiotic mechanisms of deterioration of
polyethylene have been described extensively elsewhere
(Hakkarainen and Albertsson, 2004), thus this review will be
focusing instead on the biodegradation of polyethylene and
mechanisms associated with this process.The biodegradation of
polyethylene has been reported in a number of research studies
published over the last 30 years; however, there is general agree-
ment that the process under normal conditions is extremely slow
(Gu, 2003; Hakkarainen and Albertsson, 2004; Koutny et al., 2006a;
Arutchelvi et al., 2008; Eubeler et al., 2010). The utilization of this
polymer by microorganisms is physically limited by its insolubility
in aqueous media, lack of functional groups, and high molecular
weight (Arutchelvi et al., 2008). Although there is enough evidence
that proves biodegradation of polyethylene, there is still a lack of
knowledge on the complete metabolic pathways involved in the
process and in the structure and identity of all the enzymes
involved. Only some advances have been made in this regard and
even then the conclusions outlined require verification
(Wasserbauer et al., 1990; Pometto et al., 1992; Santo et al., 2012;
Yoon et al., 2012).
The present review will cover three different topics, the first
being a comprehensive summary of the microorganisms reportedly
involved with polyethylene biodegradation; secondly, the effects of
these microorganisms on polyethylene properties will be pre-
sented; and finally an outline of the degradation process of poly-
ethylene based on published literature will be discussed.
2. Microorganisms involved in polyethylene degradation
Biodegradation of polyethylene is complex and not fully un-
derstood. In order to elucidate the potential mechanisms, two
different strategies have been followed in the literature. In the first
approach, degradation studies have been performed using pure
strains able to degrade polyethylene (Pometto et al., 1992;
Albertsson et al., 1995; Yamada-Onodera et al., 2001; Volke-
Sepulveda et al., 2002; Gilan et al., 2004; Hadad et al., 2005;
Sivan et al., 2006; Koutny et al., 2006b; Balasubramanian et al.,
2010; Fontanella et al., 2010; Rajandas et al., 2012; Santo et al.,
2012; Yoon et al., 2012; Tribedi and Sil, 2013). This approach has the
advantage of using pure strains, which is a convenient way to
investigate metabolic pathways or to evaluate the effect of different
environmental conditions on polyethylene degradation. A disad-
vantage of this approach is that it ignores the possibility that
polyethylene biodegradation can be the result of a cooperative
process between different species. These limitations are avoided by
the second approach, in which the use of complex environments
and microbial communities are applied (Albertsson, 1980;
Albertsson et al., 1987; Karlsson et al., 1988; Pegram and Andrady,
1989; Albertsson and Karlsson, 1990; Orhan and Büyükgüngör,
2000; Chiellini et al., 2003; Artham et al., 2009; Mumtaz et al.,
2010; Lobelle and Cunliffe, 2011; Nowak et al., 2011). Table 1
summarizes some of the different microenvironments that have
been employed to study polyethylene biodegradation using mixed
and complex microbial communities. Marine water, soil or compost
are examples of the environments whereby polyethylene has been
investigated under the second approach.
The structure of a microbial community isolated on a poly-
ethylene surface during biodegradation experiments can also be
influenced by the type of polymer used as the substrate. In several
studies it has been proven that the physicochemical nature of a
surface determines the ability of microorganisms to form biofilm
structures (Al-Makhlafi et al., 1994; Cunliffe et al., 1999; Donlan,
2002; Wang et al., 2012). The most common polyethylene types
are: Low Density Polyethylene (LDPE), High Density Polyethylene
(HDPE), Linear Low Density Polyethylene (LLDPE) and Cross Linked
Polyethylene (XLPE). They differ in their density, degree of
branching and availability of functional groups on the surface. It is
important to highlight that polyethylene can be also found mixed
with additives such as pro-oxidants or starch (Zheng et al., 2005;
Koutny et al., 2006a), both of these being applied to improve the
biodegradability of the polymer. The presence of these additives
can affect the kinds of microorganisms colonizing the surfaces of
these polymers.
Over the past 50 years, a number of strains have been identified
for their ability to interact with polyethylene causing some kind of
deterioration, this has been done based on the two approaches
mentioned before, and using different kinds of polyethylene.
Tables 2and 3 present an extensive list of the microorganisms that
in some way have been related with polyethylene colonization,
biodegradation or both. This list has to be approached carefully
because in some studies not all the tests required to prove poly-
ethylene biodegradation were performed. The richness of micro-
organisms able to degrade polyethylene is so far limited to 17
genera of bacteria and 9 genera of fungi; however, these numbers
are likely to increase based on the more sensitive isolation and
characterization techniques based on sequencing of rDNA. This
technology allows a broader approach to assessing the composition
of a community, including the non-culturable fraction of microor-
ganisms that is invisible by traditional microbiology methods yet
that constitutes up to the 90% of the real biodiversity in an
ecosystem (Hugenholtz et al., 1998).
3. Effect of microbial activity on polyethylene
Microorganisms able to colonize the surfaces of polyethylene
have diverse effects on its properties; seven different characteris-
tics are usually monitored for change in order to establish the
extent of biodegradation of the polymer: functional groups on the
surface, hydrophobicity/hydrophilicity, crystallinity, surface
topography, mechanical properties, molecular weight distribution
Table 1
Different microenvironments used in the study of polyethylene biodegradation.
Microenvironment Reference
Marine exposure conditions Pegram and Andrady, 1989;
Artham et al., 2009; Lobelle
and Cunliffe, 2011
Soil burial conditions Albertsson, 1980; Albertsson
et al., 1987; Karlsson et al., 1988;
Albertsson and Karlsson, 1990;
Orhan and Büyükgüngör, 2000;
Chiellini et al., 2003; Mumtaz
et al., 2010; Nowak et al., 2011
Composting conditions Chiellini et al., 2003
 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90 85

Table 2 Table 3
Bacterial strains associated with polyethylene biodegradation. Fungal strains associated with polyethylene biodegradation.

Genus Species Reference Genus Species Reference

Acinetobacter Baumannii Nowak et al., 2011 Acremonium Kiliense Karlsson et al., 1988
Arthrobacter spp Balasubramanian et al., 2010; Aspergillus Niger Raghavan and Torma, 1992,
Satlewal et al., 2008 Volke-Sepulveda et al., 2002,
Paraffineus Albertsson et al., 1995; Manzur et al., 2004
Albertsson et al., 1998 Versicolor Karlsson et al., 1988;
Viscosus Nowak et al., 2011 Pramila and Ramesh, 2011b
Bacillus Amyloliquefaciens Nowak et al., 2011 Flavus Koutny et al., 2006b; Pramila
Brevies Watanabe et al., 2009 and Ramesh, 2011a
Cereus Roy et al., 2008; Nowak Chaetomium spp Sowmya et al., 2012
et al., 2011; Satlewal Cladosporium Cladosporioides Bonhomme et al., 2003;
et al., 2008; Sudhakar et al., 2008 Koutny et al., 2006b
Circulans Watanabe et al., 2009 Fusarium Redolens Albertsson, 1980; Karlsson
Halodenitrificans Roy et al., 2008 et al., 1988; Albertsson and Karlsson, 1990
Mycoides Nowak et al., 2011; Glioclodium Virens Manzur et al., 2004
Seneviratne et al., 2006 Mortierella Alpina Koutny et al., 2006b
Pumilus Roy et al., 2008; Satlewal Mucor Circinelloides Pramila and Ramesh, 2011a
et al., 2008; Nowak et al., 2011 Penicillum Simplicissimum Yamada-Onodera et al., 2001
Sphericus Kawai et al., 2004; Pinophilum Volke-Sepulveda et al., 2002;
Sudhakar et al., 2008 Manzur et al., 2004
Thuringiensis Nowak et al., 2011 Frequentans Seneviratne et al., 2006
Brevibacillus Borstelensis Hadad et al., 2005 Phanerochaete Chrysosporium Manzur et al., 1997; Orhan and
Delftia Acidovorans Koutny et al., 2009 Büyükgüngör, 2000; Manzur et al., 2004
Flavobacterium spp Koutny et al., 2009 Verticillium Lecanii Karlsson et al., 1988
Micrococcus Luteus Nowak et al., 2011
Lylae Nowak et al., 2011
Microbacterium Paraoxydans Rajandas et al., 2012
Nocardia Asteroides Bonhomme et al., 2003;
these groups are common whenever biological activity on the
Koutny et al., 2006b
Paenibacillus Macerans Nowak et al., 2011 surface of a substrate has been detected (Albertsson et al., 1987,
Pseudomonas spp Balasubramanian et al., 1995, 1998; Albertsson and Karlsson, 1990; Raghavan and Torma,
2010; Yoon et al., 2012; 1992; Orhan and Büyükgüngör, 2000; Volke-Sepulveda et al.,
Tribedi and Sil, 2013 2002; Bonhomme et al., 2003; Chiellini et al., 2003; Gilan et al.,
Aeruginosa Koutny et al., 2009;
Rajandas et al., 2012
2004; Manzur et al., 2004; Hadad et al., 2005; Sudhakar et al., 2008;
Fluorescens Nowak et al., 2011 Artham et al., 2009; Balasubramanian et al., 2010; Fontanella et al.,
Rahnella Aquatilis Nowak et al., 2011 2010; Nowak et al., 2011; Santo et al., 2012). In general, it is
Ralstonia spp Koutny et al., 2009 accepted that in the presence of microorganisms the concentra-
Rhodococcus Ruber Gilan et al., 2004; Sivan
tions of these surface functional groups will decrease, which is
et al., 2006; Santo et al., 2012
Rhodochrous Bonhomme et al., 2003; commonly reported as a decrease in the carbonyl indices
Koutny et al., 2006b; (Albertsson et al., 1987; Raghavan and Torma, 1992; Gilan et al.,
Fontanella et al., 2010 2004; Manzur et al., 2004; Hadad et al., 2005). The other com-
Erythropolis Koutny et al., 2009 mon finding in the literature is that there should be a corre-
Staphylococcus Epidermidis Chatterjee et al., 2010
Cohnii Nowak et al., 2011
sponding increase in the number of double bonds in the presence of
Xylosus Nowak et al., 2011 microorganisms (Raghavan and Torma, 1992; Gilan et al., 2004;
Stenotrophomonas spp Koutny et al., 2009 Manzur et al., 2004; Chiellini et al., 2007; Balasubramanian et al.,
Streptomyces Badius Pometto et al., 1992 2010; Nowak et al., 2011). However, these reported results have
Setonii Pometto et al., 1992
not been universal and some reports have stated that after incu-
Viridosporus Pometto et al., 1992
bation with microorganisms there will instead be an increase in
carbonyl groups (Volke-Sepulveda et al., 2002; Balasubramanian
and mass balance. Table 4 summarized the main changes observed et al., 2010; Nowak et al., 2011) or a reduction in the number of
on polyethylene after microbial attack and the main techniques double bonds (Yamada-Onodera et al., 2001; Sudhakar et al., 2008;
used to follow these changes. It is important to highlight that Artham et al., 2009).
modifications to surface chemistry are evidence of interactions by Although the FTIR findings discussed might seem contradictory
microorganisms with the surface; however, more conclusive evi- at first glance they reveal the degradation of polyethylene to be a
dence of polymer degradation can be obtained when polymer complex process that can differ for different microorganisms and
consumption is determined over the course of experiments. So far different communities. What is certainly true is that incubation
there have been no studies in the literature that prove incorpora- with microorganisms generates changes in the concentrations of
tion of polyethylene’s carbon into a microorganism’s macromo- functional groups at the surface of a polyethylene substrate either
lecular structure such as its DNA or polysaccharides. because of their consumption or production. In a complex microbial
community in which abiotic factors are also affecting the chemistry
3.1. Functional groups on the surface of the polymer the net effect observed (accumulation or con-
sumption of functional groups) will depend on the balance of rates
The nature and occurrence of functional groups on the surface of of oxidation and degradation, which in turn will depend on the
polyethylene substrate is usually studied by FTIR spectroscopy. In nature of the microorganisms present.
the analysis of the polymer’s spectral information special emphasis The study of the chemistry of polyethylene surface turns out to
by researchers has been placed on the following functional groups: be very important, because oxidized groups are more easily
carbonyls (1715 cm1), esters (1740 cm1), vinyls (1650 cm1) and degraded by microorganisms (Albertsson et al., 1995) and because
double bonds (908 cm1). Literature studies concur that changes in oxidized groups modulate microbial attachment by increasing the
86 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90

Table 4
Changes observed on polyethylene surfaces after treatment with microorganisms.

Changes observed Techniques used Property measured Reference

Functional groups FTIR Keto-carbonyl index (I1715/I1565) Albertsson et al., 1987; Albertsson and Karlsson, 1990; Raghavan
on the surface and Torma, 1992; Albertson et al., 1995; Albertsson et al., 1998;
Orhan and Büyükgüngör, 2000; Volke-Sepulveda et al., 2002;
Bonhomme et al., 2003; Chiellini et al., 2003; Gilan et al., 2004;
Manzur et al., 2004; Hadad et al., 2005; Sudhakar et al., 2008;
Artham et al., 2009; Balasubramanian et al., 2010; Fontanella
et al., 2010; Nowak et al., 2011; Santo et al., 2012
Ester-carbonyl index (I1740/I1465) Albertsson et al., 1987; Albertsson and Karlsson, 1990; Sudhakar
et al., 2008; Artham et al., 2009; Balasubramanian et al., 2010
Vinyl-bound index (I1640/I1465) Albertsson et al., 1987; Albertsson and Karlsson, 1990; Raghavan
and Torma, 1992; Yamada-Onodera et al., 2001; Volke-Sepulveda
et al., 2002; Manzur et al., 2004; Sudhakar et al., 2008; Artham
et al., 2009; Balasubramanian et al., 2010
Double bound index (I908/I1465) Albertsson et al., 1987; Albertsson and Karlsson, 1990; Raghavan
and Torma, 1992; Albertsson et al., 1998; Orhan and Büyükgüngör,
2000; Yamada-Onodera et al., 2001; Chiellini et al., 2003; Gilan
et al., 2004; Sudhakar et al., 2008; Balasubramanian et al., 2010
CeO stretching (I1100) Satlewal et al., 2008
Hydrophobicity/Hydrophilicity Contact angle Contac angle with water Roy et al., 2008; Sudhakar et al., 2008
Surface energy Artham et al., 2009
Drop deposition Diameter of a drop Lobelle and Cunliffe, 2011
Crystallinity FTIR % Crystallinity Sudhakar et al., 2008; Balasubramanian et al., 2010
DSC % Crystallinity Raghavan and Torma, 1992; Albertsson et al., 1995; Albertsson
et al., 1998; Volke-Sepulveda et al., 2002; Santo et al., 2012
Melting temperature Volke-Sepulveda et al., 2002; Manzur et al., 2004; Sudhakar
et al., 2008
Relative crystallinity Manzur et al., 2004
Lamellar thickness Volke-Sepulveda et al., 2002
XRD % Crystallinity Albertsson et al., 1995; Manzur et al., 1997; Volke-Sepulveda et al., 2002
Lamellar thickness Albertsson et al., 1995
Molecular weight HT-SEC/GPC Molecular weight distribution Pometto et al., 1992; Albertson et al., 1995; Albertsson et al., 1998;
distribution Yamada-Onodera et al., 2001; Bonhomme et al., 2003; Chiellini
et al., 2003; Koutny et al., 2006b; Fontanella et al., 2010
Rheology Molecular weight distribution Hadad et al., 2005
Surface topography SEM Topography Albertsson et al., 1995; Volke-Sepulveda et al., 2002; Bonhomme
et al., 2003; Chiellini et al., 2003; Gilan et al., 2004; Manzur et al.,
2004; Koutny et al., 2006b; Sivan et al., 2006; Fontanella et al.,
2010; Mumtaz et al., 2010; Nowak et al., 2011; Pramila and
Ramesh, 2011a; Tribedi and Sil, 2013
AFM Topography Sudhakar et al., 2008; Artham et al., 2009; Tribedi and Sil, 2013
Mechanical properties Instron Tensile strength Pegram and Andrady, 1989; Pometto et al., 1992; Sudhakar
et al., 2008; Nowak et al., 2011; Tribedi and Sil, 2013
Strain energy Pometto et al., 1992
% Elongation Pometto et al., 1992; Orhan and Büyükgüngör, 2000; Sudhakar
et al., 2008; Nowak et al., 2011
Ultimate extension Pegram and Andrady, 1989
Maximum load Sudhakar et al., 2008
Consumption of Gravimetric Weight loss Hadad et al., 2005; Sivan et al., 2006; Sudhakar et al., 2008;
the polymer Artham et al., 2009; Nowak et al., 2011; Tribedi and Sil, 2013
CO2 evolution Weight loss Albertsson, 1980; Albertsson and Karlsson, 1990; Karlsson
et al., 1988; Pramila and Ramesh, 2011a; Seneviratne et al., 2006

hydrophilicity of the surface (Tribedi and Sil, 2013). Which implies
that polyethylene degradation will be boosted if a more oxidized
surface is used as substrate.
3.2. Hydrophobicity/Hydrophilicity
The hydrophobicity/hydrophilicity of a surface depends on the
nature, concentration and exposition of the functional groups
present in the material. In polyethylene degradation two phe-
nomena can be observed depending on the relation of oxidation
and consumption of oxidized groups by microorganisms. If the
extent of the oxidation process due to the action of abiotic factors
such as UV light or activity of enzymes is higher than the extent of
consumption of functional groups then an increase in the hydro-
philicity will be observed. Conversely, if the rate of consumption of
functional groups is higher than the rate of oxidation then an in-
crease in the hydrophobicity will be observed. Hydrophobicity is an
important property of the surface in biodegradation studies,
because the relation between surface and microorganisms hydro-
phobicity will determine the extent of colonization on the polymer
substrate. In general, it is accepted that more hydrophilic surfaces
are more easily colonized by microorganisms (Al-Makhlafi et al.,
1994; Cunliffe et al., 1999; Donlan, 2002; Wang et al., 2012).
Hydrophobicity is usually determined by the contact angle of
the surface with a probe liquid such as water, the more hydrophilic
the surface the smaller the contact angle with water (Roy et al.,
2008; Sudhakar et al., 2008). A more advance approach to study
hydrophilicity of surfaces is the use of YoungeDupré equation
(Equation (1)), which allows the estimation of the energy of
adhesion to the solid as well as its acid ðgþ g
S Þ, basic ð S Þ and Van der
Waals ðgLW Þ components (Artham et al., 2009).
S
3.3. Crystallinity
Polyethylene is a semi-crystalline polymer comprised of crys-
talline microstructures which are processing history-related, that
 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90
are surrounded by amorphous regions. It is generally accepted and
it has been corroborated experimentally, that amorphous regions
are consumed first because it is the thought they are more acces-
sible to microorganisms. Experimentally this is observed as an
initial increase in percentage crystallinity due to consumption of
amorphous portions (Raghavan and Torma, 1992; Albertsson et al.,
1995; Manzur et al., 1997; Volke-Sepulveda et al., 2002; Sudhakar
et al., 2008; Santo et al., 2012). Yet there is insufficient research to
date to state definitively what happens after the amorphous re-
gions are consumed. Nevertheless, it has been proposed that once
the accessible amorphous regions have been depleted, microor-
ganisms will progress to consuming the smaller crystals present
(Manzur et al., 1997), resulting in an increase in the proportion of
larger crystals (Albertsson et al., 1995; Manzur et al., 1997; Volke-
Sepulveda et al., 2002; Sudhakar et al., 2008).
3.4. Molecular weight distribution
One of the main limitations to polyethylene biodegradation is its
high molecular weight. One common effect observed after microbial
attack, is an increase in the average molecular weight as a result of
consumption of the lower molecular weight chains (Pometto et al.,
1992; Yamada-Onodera et al., 2001; Hadad et al., 2005; Santo
et al., 2012). This result however is not universal, with some authors
observing only a slight if any change in the molecular weight dis-
tribution (Bonhomme et al., 2003; Fontanella et al., 2010). Some
others have concluded that the main factor affecting the molecular
weight is the effect of abiotic factors such as UV irradiation rather
than direct microbial attack (Fontanella et al., 2010). Some results
showing the extent of reduction based the number-average molec-
ular weight (Mn) of polyethylene samples are presented in Table 5.
Two different approaches have been used for the determination
of molecular weight distribution, the most common one is the use of
size exclusion chromatography techniques at high temperature
(Pometto et al., 1992; Albertsson et al., 1995, 1998; Yamada-Onodera
et al., 2001; Bonhomme et al., 2003; Chiellini et al., 2003; Koutny
et al., 2006b; Fontanella et al., 2010). The other possibility is the use
of rheological measurements that correlate indirectly with the
molecular weight distribution (Hadad et al., 2005).
3.5. Surface topography
Colonization of polyethylene surfaces by microorganisms usually
generates changes in the surface topography as has been proven
extensively in different research papers. Development of micro-
colonies of different microorganisms on the surface of the polymer
(Bonhomme et al., 2003; Gilan et al., 2004; Sivan et al., 2006; Koutny
et al., 2006b; Fontanella et al., 2010; Pramila and Ramesh, 2011a;
Tribedi and Sil, 2013) as well as penetration of hyphal structures
(Raghavan and Torma, 1992; Manzur et al., 1997; Volke-Sepulveda
et al., 2002) have been reported as common features after microbial
attack. Evidently surface topography will be modified by microbial
colonization, but the real question is how the topography is modified
if the microorganisms are removed, in other words, is it possible to
observe cracking and pitting in the polymer surface after biodegra-
dation processes? The answer to this question has not been thor-
oughly addressed, even though there is enough evidence which
proves that some superficial damage will be observed after poly-
ethylene surfaces have been exposed to biodegradation (Watanabe
et al., 2009; Mumtaz et al., 2010; Nowak et al., 2011).
3.6. Mechanical properties
Most of the studies on polyethylene biodegradation have
focused on thin films, with results showing that in this form of the
87
substrate deterioration of the mechanical properties such as
breaking load, is common. Oxidation-induced changes in crystal-
linity and in the average molecular weight cause modification of
the mechanical properties. Table 6 presents results showing
changes to different mechanical properties for polyethylene after
biodegradation. The results presented correspond to pure poly-
ethylene not exposed to pre-oxidation treatments before the
biodegradation experiments.
Although rheological analysis can be performed to determine
the storage and loss modulus of the polymer, in biodegradation
studies authors have been preferred the use of a universal me-
chanical testing system (UMTS) for determination of mechanical
properties of a polymer specimen (Pegram and Andrady, 1989;
Sudhakar et al., 2008; Nowak et al., 2011).
The effects of biological activity on polyethylene samples have
been studied mainly in thin films; however thick walls are also a
very common application of this polymer in the manufacture of
tanks. Therefore the changes in the mechanical properties due to
microbial activity are still an active area or research. However, it is
likely that a microorganism’s effect will only be superficial in that
case since the resolution of bulk testing methods commonly
employed for such measurements diminish as the local surface-
related damage influences less of the overall sample.
3.7. Consumption of the polymer
Whilst the consumption of a polymer by microorganisms pro-
vides evidence of its assimilation, the slowness of this process can
make it very difficult to detect. Nevertheless, some studies have
reported a reduction in the weight of samples determined either by
gravimetric measurements (Hadad et al., 2005; Sivan et al., 2006;
Sudhakar et al., 2008; Artham et al., 2009; Nowak et al., 2011;
Tribedi and Sil, 2013) or by CO2 evolution from the samples
(Albertsson, 1980; Karlsson et al., 1988; Albertsson and Karlsson,
1990; Seneviratne et al., 2006; Pramila and Ramesh, 2011a). Be-
tween the two techniques commonly used to estimate poly-
ethylene consumption by microorganisms, CO2 evolution is the one
that provides a greater insight. In this technique it is assumed that
polyethylene used by microorganisms as a carbon source will be
finally converted to CO2 during respiration and can therefore be
used as an indirect measurement of the amount of polyethylene
that has been used by microorganisms. Since CO2 evolution out of
the system can be monitored continuously it allow determining not
only the total consumption of the polymer but also the rate of
degradation (Albertsson, 1980; Karlsson et al., 1988; Albertsson and
Karlsson, 1990; Seneviratne et al., 2006; Pramila and Ramesh,
2011a). Some authors have used this technique successfully to
verify the ability of some strains to degrade polyethylene of very
low molecular weight (Yoon et al., 2012).
Results in weight reduction have to be read with special care
when polyethylene mixed with starch is used; in this case initial
reduction in weight can be due to starch consumption rather than
polyethylene usage. Table 7 presents the main results obtained for
the extent of biodegradation found in different polyethylene types
prepared without any oxidative treatment.
It is important to note that the rate and extent of polymer
consumption can be extensively influenced by abiotic factors that
promote oxidation. Albertsson and Karlsson (1990) proved that
biodegradation rate can increase from 0.2% to 8.4% by irradiating
the samples with UV light before a biotic treatment.
4. Mechanisms of polyethylene biodegradation
The mechanisms of biodegradation for polyethylene can be
studied from three different perspectives: colonization of the
88 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90

Table 5 2009; Balasubramanian et al., 2010; Chatterjee et al., 2010; Lobelle

Changes in molecular number due to microbial activity in different studies. and Cunliffe, 2011; Nowak et al., 2011; Tribedi and Sil, 2013).
Substrate %D molecular number (Mn) Reference Studies on microorganism attachment to polyethylene have iden-
LDPE UV irradiated 34 Hadad et al., 2005
tified that the main limitation of the colonization process is the
LDPE 15 Santo et al., 2012 relatively high hydrophobicity of the polymer in contrast to the
LDPE þ Starch 17 Pometto et al., 1992 regularly hydrophilic surfaces of most microorganisms (Gilan et al.,
2004; Tribedi and Sil, 2013). It has been proposed that strains with
more hydrophobic surfaces can play an important role in the initial
Table 6 colonization of the polymer. The other metabolic adaptation that
Changes in mechanical properties due to microbial activity in different polyethylene can be important in polymer colonization is the production of
samples.
surfactants, molecules that can mediate the attachment process of
Substrate Environment Time %D %D Tensile Reference microorganisms to the hydrophobic surface (Karlsson et al., 1988;
elongation strength Tribedi and Sil, 2013).
LDPE Waste coal 225 þ4% 16.4 Nowak Theoretically, polyethylene can be used as a carbon source for
et al., 2011 microorganisms similar to many other hydrocarbons; however, its
Forrest soil 225 4% 16.4 Nowak high molecular weight limits its use as a substrate for enzymatic
et al., 2011
Crater soil 225 1.5% 19.5 Nowak
reactions to take place. In terms of the chemical/biochemical pro-
et al., 2011 cesses involved in polyethylene biodegradation it can be stated that
Sea water 365 12% 15 Pegram and there are two key reactions, the first one being the reduction of its
Andrady, 1989 molecular weight and the second being the oxidation of the mol-
Sterile sea water 365 þ2.7% 3.8 Sudhakar
ecules. Reduction of molecular weight is required for two reasons,
þ B. sphericus et al., 2008
Mineral media 45 NR 30 Sudhakar firstly to enable transport of molecules through the cell membrane,
þ Pseudomonas sp et al., 2008 and secondly because enzymatic systems present in the microor-
HDPE Sterile sea water 365 þ8.9 9.7 Sudhakar ganisms are only able to attack certain molecular weights, usually
þ B. sphericus et al., 2008 in the range of 10e50 carbons, though there has been a report of
enzymatic activity up to 2000 carbons (Yoon et al., 2012). Once the
size of the molecule is reduced, oxidation is required in order to
polymer by microorganisms; chemical/biochemical reactive path- transform the hydrocarbon into a carboxylic acid that can be
ways; and the impact of macromolecular structure of the polymer metabolized by means of b-oxidation and the Krebs cycle
on microbial usage. (Albertsson et al., 1987). Fig. 1 presents the proposed mechanisms
Polyethylene is a hydrophobic, high molecular weight molecule, of biodegradation for polyethylene.
and therefore it is commonly accepted that biofilm colonization is Both oxidation and molecular weight reduction during the
the initial step for degradation of this polymer (Gilan et al., 2004). biodegradation process are a result of synergistic effects between
Biofilms are sessile communities of microorganisms developed on a biotic and abiotic factors (photoxidation or heat treatment). There
surface that can be composed of individuals from the same or are several papers reporting both the formation of carbonyl groups
different species (Donlan, 2002). Complex biofilm communities (oxidation) and reduction of molecular weight after treatment with
comprised of different microorganisms have been detected on UV light (Albertsson et al., 1987; Karlsson et al., 1988; Albertsson
polyethylene surfaces once they were exposed to different biotic and Karlsson, 1990; Koutny et al., 2006b; Fontanella et al., 2010).
environments (Albertsson et al., 1995; Orhan and Büyükgüngör, The biotic factor is determined by groups of enzymes able to
2000; Yamada-Onodera et al., 2001; Shimada et al., 2002; Gilan degrade oxidized or reduced polyethylene molecules. However,
et al., 2004; Hadad et al., 2005; Sivan et al., 2006; Chiellini et al., there are very few works devoted to studying the enzymes involved
2007; Sudhakar et al., 2007; Satlewal et al., 2008; Koutny et al., in these processes. Breaking down large polyethylene molecules
can be accomplished by enzymatic action, as proven by Santo et al.
(2012), who found that by incubation with the enzyme laccase the
Table 7 molecular weight of a polyethylene was reduced and its keto-
Weight loss percentage due to biological action for different types of polyethylene in
carbonyl index increased. These two factors were felt to indicate
various environments without pre-oxidative treatment.
that both scission and oxidation reactions were taking place by the
Substrate Environment Time % Of Reference same enzyme. In regards to the oxidation process there was
weight
another important work, this one by Yoon et al. (2012), that isolated
loss
an alkane hydroxylase from the AlkB family that was active to
LDPE Waste coal 225 0.26 Nowak et al., 2011
polyethylene samples with molecular weights up to 27,000 Da. It is
Forrest soil 225 0.13 Nowak et al., 2011
Crater soil 225 0.28 Nowak et al., 2011 interesting to note that enzymes of this family have been described
Sea water 365 1.9 Artham et al., 2009 as microorganisms that are able to degrade hydrocarbons. In gen-
Soil þ Fusarium 3650 0.2 Albertsson and eral, it is accepted that alkane hydroxylase performs the first
redolens Karlsson, 1990 oxidation that leads to the subsequent degradation of a hydrocar-
Soil 800 0.1 Albertsson, 1980
Mineral media 56 7.5 Sivan et al., 2006
bon (Rojo, 2010).
þ Rhodococcus ruber
Mineral media 30 2.5 Santo et al., 2012 5. Conclusion and perspectives
þ Rhodococcus ruber
Mineral media 30 2.5 Hadad et al., 2005
Research performed in polyethylene biodegradation, both using
þ Brevibacillus
borstelensis pure strains as well as complex microbial communities has proved
Mineral media 45 5 Tribedi and Sil, 2013 that biodegradation of this material although slow is actually
þ Pseudomonas sp happening in nature. The rate of this process is modulated by the
HDPE Sea water 365 1.6 Artham et al., 2009 intensity and presence of abiotic factors such as UV light or other
Soil 800 0.4 Albertsson, 1980
oxidizing agents as well as by the physical and chemical properties
 J.-M. Restrepo-Flórez et al. / International Biodeterioration & Biodegradation 88 (2014) 83e90
Fig. 1. Hypothetical mechanisms of polyethylene degradation. This mechanism is result of adaptation of the works presented by different authors (Albertsson et al., 1987; Pometto
et al., 1992; Rojo, 2010; Santo et al., 2012).
of the polymer. Factors such as crystallinity, degree of oxidation and
molecular weight distribution can have an important impact on the
degree and rate of usage of the polymer by microorganisms.
Research performed so far is mainly of descriptive nature, with
a few studies devoted to polyethylene degradation mechanisms
or the isolation of enzymes belonging related to this process.
However these findings are limited and further evidence is
required to identify the complete mechanisms for polyethylene
degradation.
It is likely that future investigations will use a more mechanistic
approach to the problem of polyethylene biodegradation. Isolation
and identification of the enzymes able to oxidize and break poly-
ethylene chains as well as the size of polyethylene chains that they
are able to use as substrate is a primary goal to elucidate the
mechanisms of degradation of polyethylene.
Another important area of research is the identification of the
fate of polyethylene inside microorganisms, so far it has been
suggested that it is metabolized by means of the tricarboxylic acid
cycle (TCA), however isotopic marking has not been used to prove
that this is actually happening.
The effect of microbial degradation on the morphology of the
polyethylene it is only partially studied, it is known that amorphous
regions are more easily degraded and that small crystals are likely
used by microorganisms, however it is still unknown if highly
organized crystalline regions would be also susceptible to microbial
attack and at what rate.
Finally it would be important to establish the role of ecological
interactions between microorganisms in the process of degradation
of polyethylene. It is possible that in real ecosystems biodegrada-
tion of this polymer is a cooperative process, identifying the roles of
different microorganisms is a relevant research goal.
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