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Appl Microbiol Biotechnol

DOI 10.1007/s00253-014-6267-5

MINI-REVIEW

Biodegradable plastic agricultural mulches and key features


of microbial degradation
Marion Brodhagen & Mark Peyron & Carol Miles & Debra Ann Inglis

Received: 16 September 2014 / Accepted: 27 November 2014


# Springer-Verlag Berlin Heidelberg 2014

Abstract The development of biodegradable plastic mulch Introduction


films for use in agriculture has been ongoing for decades.
These films consist of mixtures of polymers with various The use of plastics in agriculture is called plasticulture and
additives. As a result, their physical and chemical properties dates back to the post-WWII era (Emmert 1955, 1957). Cur-
differ from those of the pure polymers often used for in vitro rently, agriculture has a multitude of uses for various plastic
enzymatic and microbial degradation studies, raising ques- products such as containers, trays, pots, packaging, tunnel and
tions about the biodegradation capability of mulch films. crop row covers, drip irrigation tubing, and crop mulch films.
Currently, standards exist for the biodegradation of plastics Plastic mulch films are applied to the soil surface in vegetable
in composting conditions but not in soil. Biodegradation in (e.g., tomato, cucumber, eggplant, watermelon) and strawber-
soil or compost depends on a complex synergy of biological ry production systems to reduce weed competition, increase
and abiotic degradative processes. This review discusses the days to harvest, and enhance crop yield and water and fertil-
physicochemical and structural properties of biodegradable izer use efficiency (Hill et al. 1982; Lamont 2005). Plastic
plastic mulches, examines their potential for on-site decom- mulch films are most commonly made of low-density poly-
position in light of site-to-site variance due to environmental ethylene (LDPE) and linear low-density polyethylene
and biological conditions, and considers the potential for long- (LLDPE), are thin (0.015–0.025 mm), lightweight (20 g.m−2
term effects on agroecosystem sustainability and functionality. for 0.025 mm thickness), and generally used for one cropping
season (Hayes et al. 2012). Usually, crop rows are mulched,
but not the area between, so one-half the field space contains
Keywords Biodegradable plastic . Biodegradable polymers . plastic (Fig. 1). Thus, 1 ha of mulched ground contains ap-
Biodegradable mulch . Compostable plastic . proximately 5,000 m2 (100 kg) of mulch film.
Compostable mulch . Compostable polymers . By 1999, plastic mulch film was used on 10 million hect-
Plastic-degrading fungi ares in China, and by 2006, on 160,000 hectares in the U.S. (1
million and 16,000 tonnes of plastic mulch film, respectively)
(Espí et al. 2006; Miles et al. 2012). However, use has not
come without cost. In Europe, agricultural plastic waste was
estimated at more than 1.3 million tonnes in 2011, and only
M. Brodhagen (*)
Biology Department, Western Washington University, Mailstop one-half was recovered for recycling and secondary uses
9160, 516 High Street, Bellingham, WA 98225-9160, USA (Plastics et al. 2012). There are few recycling facilities that
e-mail: Marion.Brodhagen@wwu.edu will accept plastic mulch film, because up to 50 % of the
weight might have soil, vegetation, pesticide, and fertilizer
M. Peyron
Department of Engineering, Western Washington University, 516 contaminants (Amidon Recycling 1994). Many growers in the
High Street, Bellingham, WA 98225-9086, USA U.S. dispose of plastic mulch film in the landfill, which is
costly ($359–584 per ha) (Galinato et al. 2012; Galinato and
C. Miles : D. A. Inglis
Walters 2012; Johnston 2012) and labor-intensive, while
Northwestern Washington Research and Extension Center,
Washington State University, 16650 State Route 536, Mount Vernon, others in the U.S. and worldwide bury or burn plastic mulch
WA 98273, USA film on-site, which can release airborne dioxane pollutants
Appl Microbiol Biotechnol

Jandas et al. 2013; Hayes et al. 2012; Kasirajan and Ngouajio


2012; Riggi et al. 2011; Kyrikou and Briassoulis 2007; Espí
et al. 2006; Briassoulis 2004; Martin-Closas and Pelacho
2011). In addition, the literature on both biodegradable poly-
mers and their in vitro biodegradation by pure cultures of
microorganisms under controlled conditions is extensive.
However, biodegradable mulch films are not pure polymers,
and in an agricultural setting, these products need to degrade
under variable environmental conditions via the native micro-
organisms, which may or may not include those with the
ability to break down the polymer. Because of the complexity
of mulch film biodegradation under agricultural conditions,
our review brings together the different points of view of a
microbiologist, a polymer engineer, a horticulturalist, and a
plant pathologist, to address the following questions: (1) In the
degradation of compostable plastic mulch products, what
features of the mulch film and of the environment must be
considered for breakdown in agroecosystems or compost sys-
tems, and (2) how might biodegradable agricultural mulch
films affect agroecosystem sustainability?
Fig. 1 Laying biodegradable mulch with a tractor (a); illustration of Whether in soil or compost, any plastic breakdown that
biodegradable mulch with dimensions typically above ground (0.7 m) occurs does so through a complex synergy of abiotic and
and buried on either side (approximately 10 cm), such that approximately
biological processes, as illustrated in Fig. 2. For a truly bio-
50 % of the surface area of soil contains plastic, and approximately 20 %
of the plastic is buried under soil during the cropping season (b) degradable plastic, the ultimate result is a reduction in the
molar mass (length) of polymers, followed by bioassimilation
and pose other serious consequences for the environment and/or biological conversion of the polymer breakdown prod-
(Garthe and Kowal 1993; Levitan 2005; Lemieux 1997; Olsen ucts, and ultimately, biological conversion to carbon dioxide
and Gounder 2001; Shogren 2000). Methods to incinerate and/or methane, and water (e.g., Lucas et al. 2008). Many
plastic for energy production have been developed but are standards and test methods have been developed for environ-
not widely adopted (Garthe and Kowal 1993). Tilling plastic mental degradation of polymers (Eubeler et al. 2009a). Plas-
mulch film into the soil has been an attractive end-of-life goal tics labeled “compostable” represent an important class of
but is not practical for the commonly used LDPE and LLDPE potentially biodegradable plastics currently used in agricultur-
mulch films because of these polymers’ very slow degradation al systems. To be labeled as such, these materials must adhere
rate (e.g., 0.35 % in 2.5 years; Albertsson and Ranby 1979). to ASTM 6400-12 (2012) and ISO 17088 (2012). The limita-
Innovations in plastic formulations to make mulch films tion of ASTM 6400-12 (2012) and ISO 17088 (2012) for
more biodegradable began several decades ago (e.g., Albregts testing biodegradable plastics intended for agricultural sys-
and Howard 1972; Otey et al. 1974) and remain a significant tems is that degradation is assessed under optimal conditions
focus of research and development today. Advances in bio- in a controlled laboratory setting that does not resemble the
synthesis and processing methods, along with investments in diverse and complex environmental field conditions which
commercial facilities, have lowered the resin prices and dra- occur in agricultural settings. While no standards exist for
matically increased the worldwide supply of bioplastics measuring breakdown of plastics in the soil environment,
(Kersh 2012; Babu et al. 2013). The overall market for one is in draft (ASTM WK29802 2014).
bioplastics is expected to increase by about 19 % per year Many polymers labeled “biodegradable” in the past were
(Laird 2013) concomitant with the development of many new actually partially degradable through a combination of abiotic
applications and products (Karpušenkaitė and Varžinskas (e.g., photooxidation, erosion, fragmentation) and biotic pro-
2014). cesses (Kyrikou and Briassoulis 2007; Rudnik 2008). Biode-
gradable mulches may be better described by the terms used
by Kyrikou and Briassoulis (2007), i.e., bioerodable,
hydrobiodegradable, photodegradable, or partially biodegrad-
Biodegradable mulch films able. One early manufacturing practice involved blending
polyolefins (e.g., polypropylene or PE) with starch in order
Many reviews have been written specifically about the use of to achieve a more readily biodegradable product, but the result
biodegradable plastics in agriculture (Corbin et al. 2013; was principally biofragmentation since only the starch
Appl Microbiol Biotechnol

Fig. 2 Relationships between


soil/composting environmental
conditions, biological and abiotic
agents present, the polymer
structure of agricultural mulches,
and the disposition of degradation
products and persistent mulch
components. Examples of three
classes of polymer mulch
components are shown. Curving
arrows indicate chemical bonds
susceptible to hydrolysis
(enzymatic or chemical);
oxidation may occur at multiple
sites

biodegraded, and the polyolefin solids, if reduced in size at all, and chemical properties of pure polymers is inadequate to
were not mineralized. While ASTM still was formulating evaluate the biodegradable properties of agricultural mulch
standard testing procedures for plastics labeled as “biodegrad- films, which usually are proprietary blends of unpublished
able,” Yabannavar and Bartha (1994) demonstrated that: (1) composition. Therefore, this review focuses on well-
CO2 evolution in some test plastics likely reflected breakdown researched features from which widely applicable conclusions
of the additives—starch, and the plasticizers dioctyladipate can be made (e.g., Tokiwa et al. 2009; Kijchavengkul and
and epoxidized soybean oil—rather than a shortening of the Auras 2008). These features are categorized in Table 1 and in
polymers, and (2) CO2 evolution and tensile strength changes Fig. 2 and discussed below. Although the rapid increase in
did not correlate well with shortening of the polymers as innovation and investment in biopolymers will influence the
measured by gel permeation chromatography (GPC). The commercial products available for agricultural applications in
authors stated that “decrease in the size of polymer resin coming years (Babu et al. 2013; Miller 2013; Queiroz and
molecules, as measured by GPC, is likely to be crucial for Collares-Queiroz 2009), the key factors described below are
definition of degradation, while changes in additives will be likely to remain valid.
defined as deterioration.” Twenty years later, ASTM and ISO
still rely on CO 2 evolution, an indirect measure, to
demonstrate plastic breakdown. A range of other analytical Morphological features key to biodegradable polymer
methods are available for estimating biodegradation of breakdown
polymers. Their limitations and applications have been
compared by Lucas et al. (2008) and Eubeler et al. (2009a). Properties of naturally occurring biodegradable polymers used
In light of the example above, it is important to appreciate in mulch films
that agricultural mulch films are blends of polymers, with
plasticizers, compatibilizers, and other additives to improve Microbes secrete enzymes that reduce the molecular weight
processing, properties, chemical compatibility, and uniformity (chain length) of naturally occurring polymers, and then trans-
of the mulches (e.g., Imre and Puklasnszky 2013). This blend- port the oligomers, dimers, and monomers into their cells for
ing is usually accomplished by melting and screw extrusion, metabolic use. Thus, the natural substrates of the
followed by blow molding to form the thin films; all of these depolymerases normally secreted by soil- and plant-
processing steps can alter the physical and chemical morphol- associated microorganisms are logical starting substances for
ogy of the mulch produced. As a result, the propensity of the products expected to degrade in agroecosystems. Naturally
component materials to form amorphous or semi-crystalline occurring polymers used in biodegradable mulch films are
regions may be quite different than for the pure components starch, cellulose, and polyhydroxyalkanoates (Fig. 3). We briefly
alone (e.g., Ferrarezi et al. 2013). Thus, knowledge of thermal describe these polymers below. The remainder of the paper
Appl Microbiol Biotechnol

Table 1 Classification of polymers commonly used in commercial agricultural mulches and the chemical origin, principal method of synthesis, and
relative rates of in-soil biodegradation of each

General polymer category Polymers common in Chemical Polymer Monomer Estimated comparative rate of
agricultural mulchesa originb synthesisc feedstockd biodegradation in soile

Polyolefins (Aliphatic thermoplastics) PE S C HC Extremely low


Polysaccharides (Sugar-based polymers) Cellulose N B BB Moderately high
Starch (TPS) N Bf BB High
Starch (CMS) S C BB High
Aliphatic polyesters (Ester groups in main, PBS & PBSA S C HC Low moderate
non-aromatic chain) PCL S C HC Moderate
PHB & PHV N B HC, BB Moderate
PLA S B&C BB Low
Aromatic polyesters (Ester groups in main, PBAT S C HC Low moderate
partially aromatic chain) PTT S C HC Low
a
Most degradable mulches are proprietary blends of these common polymers, but the list is not intended to be exhaustive: PE poly(ethylene) or
polythene, TPS thermoplastic starch (amylose and amylopectin plasticized with organic alcohols and water), CMS chemically modified starch (most
commonly esterification with organic acids), PBS poly(butylene succinate), PBSA poly(butylene succinate adipate), PCL poly(ε-caprolactone), PHB
poly(3-hydroxybutyrate), PHV poly(3-hydroxyvalerate), PLA poly(lactic acid) or poly(lactide), PBAT poly(butylene-adipate-co-terephthalate), PTT
poly(trimethylene terephthalate). Note that PHB and PHV represent two of the most important commercial PHAs
b
Naturally occurring polymers (N) are unreacted, unmodified polymers found in nature. Synthetic polymers (S) are not produced nor widely found in
nature
c
Current commercial polymer production is classified principally as either synthetic chemical synthesis (C) or biological synthesis (B). Biological
synthesis routes are being developed for many of the polymers currently produced using chemical methods
d
Monomer or pre-cursor feedstocks are listed as either bio-based (BB) or based on hydrocarbons (HC) from petroleum or natural gas (i.e., not bio-based)
e
Complete comparisons of all polymers are not available in the literature, so this assessment reflects the authors’ best estimates based on existing data.
The comparison assumes common soil conditions and excludes elevated temperatures of commercial composting conditions
f
Raw starch polymers are bio-based, but processed thermally/mechanically and plasticized to allow plastic film formation with the dispersed starch
polymers

focuses on synthetic polymers used in agricultural mulch prod- crystalline regions in starch, the individual molecular
ucts, whose biological breakdown cannot be assured to be an structures of amylose and amylopectin remain intact in
inherent property of agroecosystems. TPS; these polymers can be degraded by microbial amy-
lases (Vikman et al. 1995) in pure TPS and in products
1. Starch. Starch is the major carbon reserve for plants; where they are blended with other polymers (Vikman
therefore, saprophytic soil microbes have evolved to se- et al. 1999). The negative consequences of hydrogen
crete abundant starch-degrading hydrolases (amylases). bonding and moisture sensitivity of TPS products can be
Starch is a mixture of straight-chain amylose and short- diminished by esterification at the R group shown on
chain, branched amylopectin (Fig. 3). Starch polymers are amylose in Fig. 3. In these chemically modified starches
capable of strong hydrogen bonding, and thus do not melt, (CMS), the R group includes esters of organic acids and
so they require additional processing steps to be incorpo- other derivatives, including cross-linkable vinyl anhy-
rated into blended plastic materials. In thermoplastic drides (Da Roz et al. 2011; Shanks and Kong 2012).
starch (TPS), aqueous dispersions of high-amylose starch TPS and derivatives are the most common additives to
and water are processed at high temperature to disrupt agricultural mulches and in other applications for which
crystalline regions (Zhang et al. 2014). Although water biodegradation is desired (Clerici 2012; Wang et al. 2003;
acts, in part, as a plasticizer, other plasticizers are added to Avérous 2004).
alter the mechanical and flow properties of the TPS. These 2. Cellulose. Cellulose (Fig. 3) is ubiquitous in nature, is
additives include alcohols (principally glycerol but also readily degraded in the environment, and is used as the
sugar alcohols), polyoxyalkenes, and surfactants (Shanks positive reference material during compostability studies
and Kong 2012). Often, the TPS is formed and blended in (ISO 14855-1 [2012]; ASTM D 5338-98 [1998]). Cellu-
screw extruders along with other polymers to produce lose is not only readily available in crude form as plant
mulch films with varying properties (e.g., Shin et al. debris, but it also has been engineered into paper products
2008; Clerici 2012). Despite processing to disrupt that are more uniform and reliable as mulches than natural
Appl Microbiol Biotechnol

Fig. 3 Chemical structures of the


most common potentially
biodegradable polymers used in
agricultural mulch products.
Thermoplastic starch (TPS) is
principally amylose with the R
group containing unmodified OH
functionality, while for CMS; the
R group varies with the reacting
species used. Note that
poly(ethylene) is not considered a
biodegradable plastic, but it is
included to complete this figure

plant debris. Owing to extensive hydrogen-bonding, un- compound is its degradation by the cells that produce it.
modified cellulose cannot be transformed into a homoge- Bacteria not only mobilize endogenous PHA reserves
neous plastic film with desirable thermoplastic properties. using intracellular enzymes, but they (as well as fungi)
However, chemically modified cellulose, such as cellu- also secrete PHA depolymerases to recycle PHA from
lose acetate, can be formed into films and fibers that are lysed cells nearby. PHAs are used commonly for plastic
biodegradable (Gross et al. 1995), although, to our knowl- production because of inherent thermoplastic properties.
edge, these products are not commercially important for These properties vary by structure. The commercially
agricultural use. important PHAs (see Fig. 3) are poly(3-hydroxybutyrate)
3. Polyhydroxyalkanoates. Polyhydroxyalkanoates (PHAs) or PHB, and poly(3-hydroxyvalerate) or PHV. Of the
are a class of at least 150 types of aliphatic, hydrophobic PHAs, PHB is the most abundant polymer among bacte-
polyesters of the same general structure, produced by ria (Jendrossek and Handrick 2002), but, as a homopol-
over 90 genera of bacteria and archaea as carbon storage ymer, it is brittle, crystalline, and undergoes thermal
compounds (Kim et al. 2007). Inherent in a storage decomposition at its melting point (Rudnik 2008). Thus,
Appl Microbiol Biotechnol

PHB’s utility as a plastic is limited. However, co- hydrophilicity, in addition to the fundamental reactivity of
polymers of PHB with other PHAs, such as with PHV the polymer structures present (Leja and Lewandowicz
(poly[3-hydroxybutyrate-co-3-hydroxyvalerate], called 2010; Chandra and Rustgi 1998). Such general features
PHBV), have more useful properties for plastic films strongly influence rates of biodegradation.
(Rudnik 2008; Divya et al. 2013). Consequently, PHB 2. Network surface area. Chemical and enzymatic hydroly-
and PHV homopolymers as well as PHA-based co-poly- sis of the polymer requires access of the attacking agent
esters are degraded readily in the environment (typically dissolved in aqueous solution) to the polymer.
(Jendrossek et al 1996; Kim et al. 2000; Jendrossek This mechanism most often is an erosive, or “outside-in,”
2001; Reddy et al. 2003; Tokiwa and Calabia 2004; mechanism (e.g., Domb et al. 1998). Abiotic weathering
Philip et al. 2007). PHA-based materials, with or without (erosion, mechanical, and thermal fragmentation) and
added starch, degrade much more rapidly than starch- chemical and enzymatic hydrolysis all increase surface
polyolefin mixtures (Gilmore et al. 1992; Imam et al. area, facilitating further hydrolysis (Fig. 2). In addition,
1999). PHA-based polymers also show promising biode- surface changes that occur from abiotic and biotic degra-
gradable characteristics in soil-based testing (Sang et al. dation can increase surface area and increase the forma-
2002; Boyandin et al. 2012; Weng et al. 2013). tion of biofilms that potentially facilitate further degrada-
tion (Woolnough et al. 2010). However, recalcitrant plas-
tics are hydrophobic (see below), and this property in-
Properties of synthetic biodegradable polymers used in mulch hibits the formation of biofilms that would contribute to
films degradation (Haddad et al. 2005).
3. Mobility of polymer chains. An increase in melting tem-
The synthetic biodegradable polymers used in commercial perature (a thermal transition for crystalline regions)
agricultural mulch films are polyesters (Figs. 2 and 3; Ta- strongly correlates with a reduction of the rate of biodeg-
ble 1), i.e., the aliphatic polyesters poly(lactic acid) or radation (Tokiwa et al. 2009). But unlike small molecules,
polylactide (PLA), poly(ε-caprolactone) (PCL), polymers contain both crystalline and amorphous regions
poly(butylene succinate) (PBS), and poly(butylene succinate that are affected by the polymer composition, additives,
adipate) (PBSA), as well as the aromatic co-polyester and other factors. When a sample is heated to the glass-
poly(butylene-adipate-co-terephthalate) (PBAT). Each of the- transition temperature (Tg), the polymer undergoes a
se polymers has been reported to degrade via the action of glassy-to-rubbery transition that is associated with mobil-
bacteria and/or fungi, as reviewed by Mohan and Srivastava ity of polymer segments and side-groups. If a polymer’s
(2010), Eubeler et al. (2009b), Swift (1993), and Kawai Tg exceeds the degradation temperature, polymer mobil-
(1995). As mentioned earlier, mulch film properties cannot ity, and therefore degradation rates, will be diminished.
be predicted based on the properties of pure polymers. Ac- The effect of thermal properties on mobility is illustrated
cordingly, when PLA was blended with PHB and other by PLA, which has a higher Tg (54–69 °C, depending on
additives, the PLA degradation behavior was altered, owing, the D- and L- isomers present) (Sin et al. 2012) and also a
in part, to changes in miscibility of the polymer components much slower rate of biodegradation than other aliphatic
(Arias et al. 2014; Gattin et al. 2001). It is very likely that polyesters like PCL and PBS (Tg values of −60 and
trends in degradation behavior of multi-component heteroge- −32 °C, respectively). PLA decomposes more rapidly in
neous films are possible to predict only under very carefully compost than in soil (e.g., Karamanlioglu and Robson
defined conditions. Even so, researchers have identified sev- 2013; reviewed by Tokiwa and Calabia 2006; Kawai
eral important properties that often correlate with biodegrad- 2010). PLA requires higher than typical soil temperatures
ability (e.g., Tokiwa et al. 2009; Kijchavengkul and Auras for both abiotic and biological degradation, and un-
2008). These are described below. dergoes significant abiotic hydrolysis above its Tg (Kawai
2010; Karamanlioglu and Robson 2013). The high tem-
1. Polymer structural features affect enzyme access. For pure peratures of municipal compost (up to 60–70 °C; Ahmad
polymers, properties that affect the rate of degradation et al. 2007; Isobaev et al. 2014; Trautman 1996) thus
measured in the laboratory and under realistic field con- provide a compelling explanation for the rapid breakdown
ditions include chemical structure, molecular weight, of PLA in compost as opposed to its slow breakdown in
crystallinity, glass-transition and melting temperatures, soil.
and enthalpy of melting (Lucas et al. 2008). These funda- 4. Aromatic content and distribution. The linear aliphatic
mental properties are the basis for more general features polyesters are hydrophobic. Historically, aromatic rings
of the heterogeneous blends that make up commercial were introduced into polyesters in order to improve me-
mulches, including the polymer network surface area, chanical properties of the polymer, but this trait also
polymer mobility, aromatic content and distribution, and increases hydrophobic character and crystallinity,
Appl Microbiol Biotechnol

decreasing the rate of biodegradation of pure polymers the biological reactions (hydrolysis and oxidation) that aug-
(Kijchavengkul et al. 2010). In addition, aromatic seg- ment abiotic degradation in soil and compost. Weathering
ments in polyesters are far less electrophilic than aliphatic results in the addition of oxygen-containing groups to the
segments (e.g., Chen et al. 2008). Poly(ethylene tere- polymer, increasing the likelihood of chain scission.
phthalate) (PET) is an example of a polyester in which Weathering-induced oxidation and fragmentation can also
each repeating unit of the polymer contains an aromatic facilitate further breakdown after incorporation into soil or
ring (from the polycondensation of terephthalic acid). compost (Singh and Sharma 2008), where the thermodynam-
PET is very resistant to microbial attack and persistent ics and kinetics of biological polymer degradation are influ-
in the environment (Müller et al. 2001). Alternatively, enced by factors similar to those affecting soil organic matter
aromatic character can be introduced in short segments, decomposition. Agroecosystems are dynamic systems where
an approach used in the random co-polyester PBAT. temporal, environmental, and site-to-site differences affect
PBAT (Fig. 3) is produced by starting with random chain real-life biodegradation outcomes. For instance, plastic mulch
lengths of the aliphatic polyester component formed from products labeled “biodegradable” degraded at different rates at
butylene diol and adipic acid (represented by m repeat each of three bioregions in the U.S. (Moore-Kucera et al.
units in Fig. 3). The aromatic co-polyester then is 2014; Li et al. 2014), variability that may have stemmed from
appended to the aliphatic portion as relatively short seg- the activity of soil microbes and their enzymes, as well as the
ments. Thus, the random m and n segments shown in environmental conditions of each agroecosystem.
Fig. 3 exist largely as blocks of aliphatic and aromatic Temperature directly affects both abiotic and biological
polyesters, yielding improved properties while maintain- chemical reaction rates. Temperatures of 60–70 °C can induce
ing the ability of the aliphatic segments to hydrolyze thermo-oxidation of PE, leading to a reduction in molecular
(Saadi et al 2013; Kijchavengkul et al 2010; Müller weight (Reddy et al. 2008; Bonhomme et al. 2003). Similar
et al. 2001). temperatures accelerate abiotic degradation of PLA (Kawai
5. Hydrophilicity. Increased aromaticity improves mechani- 2010; Karamanlioglu and Robson 2013). Biologically, the
cal properties of polyesters but decreases hydrophilicity enhancement of enzymatically catalyzed reactions by warmer
and reduces the rate of biodegradation (e.g., Müller et al. temperatures results in an increase in the overall metabolic rate
2001). Complete hydrolysis of the polymer requires bind- of microbial communities, which implies increased produc-
ing and penetration of water (and dissolved aqueous sol- tion of cells and enzymes (e.g., Davidson and Janssens 2006).
utes), as well as enzymes. Enzyme binding is promoted Note that, while 60–70 °C represents damaging heat for
not only by hydrophilicity, but also by the extent of the mesophilic bacteria and fungi, thermophilic microorganisms
amorphous structure and flexibility of the polymer chains thrive at these temperatures. Biodegradation of plastic
and film network. However, high mobility is not sufficient mulches typically has been done via commercial composting
for enzyme binding, as illustrated by LDPE, which de- conditions where higher temperatures (60–70 °C) are
spite a Tg ≈−120 °C (Mark 1999), is recalcitrant to break- achieved (Ahmad et al. 2007; Isobaev et al. 2014; Trautman
down. The structure of PE (Fig. 3) is very hydrophobic, 1996).
and prevents binding of water and enzymes. Enzyme The pH optima of cells and enzymes in soil and compost is
reaction rates depend upon the concentration of substrate likely to be near neutral in most soils, but more extreme pH
at the active site of an enzyme, so very hydrophobic conditions can speed hydrolysis of ester linkages (e.g., Jung
polymers, which do not permit water, enzymes, and aque- et al. 2006; illustrated mechanistically in Lucas et al. 2008).
ous solutes access to the polymer surface, will have Acidic pH can increase the rate of breakage of glycosidic
slower biodegradation rates. bonds in starch. The growth of microbial cells can result in
the secretion of organic acids that alter the pH of the sur-
rounding environment, further contributing to polymer
hydrolysis.
Because plastic decomposition is a process of oxidation
Environmental features key to biodegradable polymer and hydrolysis, these reactions inherently are dependent upon
breakdown oxygen and water availability. Oxygen dictates whether aero-
bic (efficient) or anaerobic (inefficient) metabolism will pre-
Plastic degradation begins at the extrusion process during dominate. However, should anaerobic conditions occur in
manufacture, and continues as the product is weathered during combination with high temperature (e.g., during thermophilic
use (Fig. 2). Photo-oxidative, thermal, mechano-chemical, anaerobic digestion), the metabolic inefficiency of anaerobic
and ozone-induced weathering processes are all abiotic, and metabolism may be balanced by the positive effect of heat on
have been well reviewed (e.g., Singh and Sharma 2008; rates of individual reactions and the community’s overall
Chiellini et al. 2011; Lucas et al. 2008). Herein, we focus on metabolism.
Appl Microbiol Biotechnol

Biological features key to biodegradable polymer present in separate organisms whose abundance differs; (5)
breakdown substrates are metabolized hierarchically according to meta-
bolic efficiency via catabolite repression (e.g., Katz and Kelly
Enzyme activity may differ under laboratory and agricultural 2010); and (6) although many enzymes relevant to degrada-
conditions tion of plastic polymers are likely to be more abundant during
nutrient limitation (e.g., Hammel 1997), microbial popula-
Underlying all polymer biodegradation is the presence of tions cannot thrive on a carbon-rich substrate if there is insuf-
enzyme(s) that have an ability to oxidize or hydrolyze the ficient nitrogen or phosphorous in the environment to synthe-
polymer. Many reports exist of individual bacterial and fungal size proteins and nucleic acids. Finally, (7) a deficiency that
species having the ability to degrade a particular polymer(s) prevents degradation of plastic polymers may be cryptic. For
in vivo (e.g., Suyama et al. 1998; Pranamuda and Tokiwa example, even in culture medium, Aspergillus nidulans, As-
1999; Tokiwa and Jarerat 2003). The literature on this topic is pergillus awamori, Aspergillus niger, Penicillium sp., and
extensive, and we refer interested readers to several good Trichoderma only partially degraded PLA oligomers when
reviews (Kim and Rhee 2003; Shah et al. 2008; Bhardwaj presented as the sole carbon source (Torres et al. 1996). Given
et al. 2012; Ghosh et al. 2013). PLA is particularly well- these environmental and enzymatic constraints, one can ap-
studied in this regard (reviewed by Tokiwa and Calabia preciate that degradation of plastic polymers in nature might
2006; Kawai 2010), but the microbial contribution to degra- be a slow and complex process.
dation in real soil and compost conditions has been under
debate for some time and appears to be temperature- General mechanisms for decomposition of plastic mulches
dependent (Karamanlioglu and Robson 2013). Caution is
necessary in extrapolating results from in vitro assays to in- 1. Photodegradation and oxo-degradation. Biodegradable
soil or in-compost degradation because (1) agricultural mulch mulch films may contain polymers with some structural
films are not composed of pure polymers; (2) laboratory similarity to PE, whose polymer backbone is fully com-
assays are performed under optimized conditions that do not posed of carbon–carbon bonds, requiring an initial oxida-
represent soil and compost over time; and (3) many studies tion step followed by hydrolysis for breakage. For PE,
represent results obtained with polymer that was solubilized in both oxidation and hydrolysis may be abiotic- or enzyme-
an organic solvent, emulsified with a surfactant, and mediated. Because the nonpolar carbon–carbon and car-
suspended in aqueous media at dilute concentration, usually bon–hydrogen bonds are minimally reactive, energy input
in parts per thousand (e.g., Pranamuda and Tokiwa 1999; is required in the form of heat, UV radiation, and mechan-
Mayumi et al. 2008; Masaki et al. 2005; Nakamura et al. ical stress (Chiellini et al. 2011). Even for more hydro-
2001). In reality, the hydrophobic polymers in mulch films philic polymers, a mix of abiotic and biological oxidation
are so concentrated that they exclude other molecules from and hydrolysis is likely. Consequently, the mechanism for
their structures, even water. PE fragmentation is informative for understanding the
Although degradation of foreign compounds in soil or degradation of more labile polymers. PE photo-
compost is often performed by microbial consortia, a single oxidation can be enhanced by incorporation of UV-
species (such as those identified in laboratory studies) might absorbing carbonyl groups into the polymer or by adding
initiate the process. So theoretically, degradation could be “pro-oxidant” additives (often complexes of transition
activated by inoculation with one degrading organism. The metals such as Co3+, Fe3+, and Mn2+) that catalyze oxi-
co-occurrence of a polymer with a microorganism or enzyme dation (Chiellini et al. 2011). Further oxidation is expect-
that has been demonstrated to degrade it in vitro does not ed to occur by biological breakdown of the oxidation
guarantee similar in situ activity, however. In addition to the products (Wiles and Scott 2006), but true biodegradation
caveats listed above: (1) bacteria and fungi have specific is limited, and the predominant degradation mechanism is
temperature, pH, and osmolarity requirements that must be fragmentation (Eubeler et al. 2009b). Although photode-
met by the agricultural environment where the mulch exists, gradable plastics have been developed for agricultural
or colonization will not occur; (2) the binding likelihood of a mulch use (Wiles and Scott 2006; Kasirajan and Ngouajio
microbial hydrolase is greater for its native substrate, for 2012), agricultural mulches typically are partially buried
which it has evolved exquisite specificity, than for plastic, so to hold them in place during use (Fig. 1) and sometimes
if the native substrate is present, it may outcompete the plastic tilled into the soil following use, thereby precluding the
for enzyme binding; (3) enzyme gene expression is regulated exposure to light required for initial photo- and oxo-
by specific inducers, repressors, and co-factors whose pres- degradation reactions.
ence in soil or compost is not guaranteed; (4) polymer and co- 2. Biological oxidation. The consideration of lignin degra-
polymer breakdown may require the action of more than one dation is informative because lignin is recalcitrant to
enzyme type (e.g., oxygenases and esterases), which may be biological breakdown, due to the characteristics listed
Appl Microbiol Biotechnol

below (Hammel 1997), some or all of which may be activation for hydrolysis of ester linkages (Fig. 2) than for
common to many biodegradable plastic mulches. Lignin polyolefins like PE (Singh and Sharma 2008; Kyrikou
is a large, highly branched polymer (and thus cannot be and Briassoulis 2007). For a mechanistic description and
transported into cells; digestion must be extracellular). It illustration of esterase cleavage of polyester substrates,
is aromatic and water-insoluble (limiting availability to see Lucas et al. (2008). Biological hydrolysis is mediated
enzymes). Lignin subunits are irregularly cross-linked by microbially secreted hydrolases, including various es-
(requiring a non-specific mode of enzymatic breakdown) terases (e.g., lipases and cutinases) and proteases, as de-
by stable carbon–carbon and ether linkages. Somewhat scribed below. Starch, cellulose, and PHAs are abundant
circumventing these issues, lignin is broken down by natural polymers, for the degradation of which a number
microbially secreted oxidases, including manganese per- of substrate-specific hydrolases have evolved. Presenting
oxidases, lignin peroxidases, and laccases. These en- a conundrum are synthetic polymers for whose degrada-
zymes can indirectly oxidize lignin (or other compounds) tion enzymes have not yet evolved. In this case, enzymes
via low-molecular-weight cofactors (mediators) whose natural substrate’s structures resemble the synthetic
(reviewed by ten Have and Teunissen 2001; Riva 2006; polymers may possibly play a role instead. Two natural
Burns et al. 2013). Laccases (secreted oxidases with a polyesters in agroecosystems that are structurally similar
reduction potential between 0.5 and 0.8 V regardless of to plastic polyesters are cutin and suberin. Cutin, part of
the producing organism; Kersten et al. 1990; Suresh the waxy surface that protects aerial plant organs, is an
Kumar et al. 2003; Riva 2006) are produced by most inter-esterified network of hydroxylated and hydroxyl
fungi tested thus far (Thurston 1994). Taken together, epoxy fatty acids. Suberin, found in the periderm of roots
ubiquitous production and indirect substrate oxidation and in many other plant parts, is a similar complex poly-
via small, diffusible mediators suggest that ligninolytic mer, but more likely to contain fatty acids, fatty alcohols,
oxidases are good candidates for the oxidative dicarboxylic acids, and aromatic groups (Kolattukudy
degradation of plastics. To our knowledge, few studies 1981, 2001; Pollard et al. 2008). The esterified fatty acids
have explored the effect of ligninolytic fungi on plastic that comprise cutin (and suberin) structurally resemble
breakdown. Lee et al. (1991) found that, following heat those found in biodegradable polymers (Fig. 3). There-
treatment (70 °C), pure cultures of three species of fore, it is not surprising that many of the enzymes reported
Streptomyces known to be ligninolytic reduced the mo- to degrade these polymers are cutinases. Following this
lecular weight of PE containing pro-oxidants and 6 % logic, Koitabashi et al. (2012) and Kitamoto et al. (2011)
starch, but the model lignin-degrading fungus isolated fungi (and the relevant enzymes) from the phyl-
Phanerochaete chrysosporium had no effect. Kerem loplane of rice, wheat, and barley and demonstrated an
et al. (1998) found that the fungus Gloeophyllum trabeum ability to degrade PBS and PBSA. The lifestyle of plant
caused a rapid internal oxidative cleavage of the C–C pathogens and saprophytes requires enzymes capable of
polymer bonds of thermoplastic polymer poly(ethylene degrading not only cutin and suberin, but cuticular waxes,
oxide), also called polyethylene glycol. Although cell membrane lipids, and lipid bodies of living and
ligninolytic enzymes are common, their production is decaying plants. Indeed, many of the microorganisms
highly regulated and variously induced by depletion of reported to break down biodegradable polymers (e.g.,
nitrogen, carbon, and sulfur; by abundant oxygen, and by Ghosh et al. 2013; Bhardwaj et al. 2012; Kim and Rhee
the presence of Mn+2, appropriate temperature, light and 2003; Shah et al. 2008) are plant pathogens and sapro-
pH, and other factors (e.g., Faison and Kirk 1985; phytes. For example, the degradative abilities of the sap-
Kubicek et al. 2010; Brown et al. 2014). Catabolite re- rophyte Aspergillus oryzae are exploited during the fer-
pression and other regulation of ligninocellulytic enzyme mentation of soybeans into sake, soy sauce, and miso; this
production is a hurdle for the breakdown of fungus also is able to degrade PBS and PBSA (Maeda
ligninocellulosic materials in biofuel production and bio- et al. 2005). PCL is degraded by a cutinase produced by
remediation. These limitations logically extend to oxida- the plant pathogen Fusarium (Nishida and Tokiwa 1994;
tion of biodegradable plastic mulches. Nevertheless, the Murphy et al. 1996). The most efficient PLA-
molecular signal transduction underlying these regulatory depolymerizing enzyme reported to date is a cutinase-
processes is well studied in relevant model fungi (Brown like enzyme isolated from the yeast Cryptococcus. This
et al. 2014), permitting hope of biotechnological enzyme was able to degrade high-molecular-weight PLA
solutions. with 500 times better efficiency than the common PLA-
3. Hydrolysis by secreted esterases and proteases. With the degrading standard, proteinase K, and it also
exception of starch-based products, potentially biodegrad- depolymerized PBS and PCL efficiently (Masaki et al.
able mulches that are used commercially are polyesters. 2005). Outstanding among microorganisms that secrete
Fundamental to biodegradability is the lower energy of plastic-degrading hydrolases are fungi within the family
Appl Microbiol Biotechnol

Trichocomaceae, which includes the genera Aspergillus tricarboxylic acid cycle intermediates (Hartman et al. 1972;
and Penicillium. Aspergillus not only secretes numerous Hartman and Keen 1973, 1974). Thus, colonization and/or
hydrolases (Mellon et al. 2007), but its individual en- CO2 generation of plastic surfaces by oligotrophic microor-
zymes also can accept several substrates (e.g., Maeda ganisms does not necessarily equate with biodegradation.
et al. 2005). Penicillium sp. strain 14-3 degraded multiple Fungi secrete organic acids (e.g., citric, malic, fumaric, and
polymers, including poly(ethylene adipate) (PEA), poly(- oxalic acids) in copious amounts, given the correct conditions
ethylene succinate) (PES), PBS, and poly(butylene (Magnuson and Lasure 2004). Visually apparent degradation
adipate) (PBA) (Tokiwa and Suzuki 1974). A lipase iso- of plastic surfaces may be due to acid weathering rather than
lated from this strain degraded poly(propylactone) and to enzymatic breakdown, with fungal growth resulting from
PCL, but not PHB (Tokiwa and Suzuki 1977a, b). Purified utilization of non-plastic carbon sources. On the other hand,
lipases from fungi within the genera Penicillium, oligotrophs may act as keystone species in microbial commu-
Rhizopus, and Candida can hydrolyze PEA and PCL nities which may, as a whole, eventually accomplish bona fide
(Tokiwa and Suzuki 1977a, b). PLA is hydrolyzed not biodegradable plastic mulch degradation.
only by cutinases and lipases, but also by a variety of The majority of fungal colonizers of soil-buried biodegrad-
proteases (comprehensively reviewed by Kawai 2010; able plastic mulches in a recent survey fell into the family
Tokiwa and Calabia 2006). PLA was degraded by the Trichocomaceae (Moore-Kucera et al. 2014), known for its
actinomycete Amycolatopsis in vitro (Pranamuda and ubiquity (Alexopoulos et al. 1996), oligotrophy, and broad
Tokiwa 1999); later, proteinaceous materials were shown metabolic capacity. Penicillium and Aspergillus (members of
to be potent inducers of PLA-degrading activities by the Trichocomaceae) are prominent among fungi reported to
Amycolatopsis and the fungus, Tritirachium album be isolated as degraders of both biodegradable and conven-
(Jarerat et al. 2004, 2006). Silk also is degraded by these tional polymers (e.g., Cook et al. 1981; reviewed by Ghosh
fungi, and silk fibroin contains a high level of the amino et al. 2013 and Bhardwaj et al. 2012; Kim and Rhee 2003;
acids alanine and glycine. Peptides composed of these Shah et al. 2008). Individual members of the Trichocomaceae
amino acids induced PLA degradation (Jarerat et al. also can degrade multiple polymer types, including those not
2004), presumably because the structure of L-alanine re- generally considered biodegradable, like PE (El-Shafei et al.
sembles that of L -lactic acid (Jarerat et al. 2004; 1998; Yamada-Onodera et al. 2001; Ojeda et al. 2009) and
Pranamuda et al. 2001). An inducer of enzyme activity PVC (Mogil’nitskii et al. 1987). Considering their enzymatic
or expression is not always structurally related to the profligacy (e.g., Mellon et al. 2007; Alexopoulos et al. 1996)
enzyme’s substrate: A cutinase-like enzyme isolated from and promiscuity (Maeda et al. 2005; Tokiwa and Suzuki
a phyllosphere yeast was highly induced by xylose 1977a, b), one might well imagine that the Trichocomaceae
(Watanabe et al. 2014). could solve many plastic waste problems. However, aban-
doned, intact LDPE plastic shopping bags and
Trichocomaceae are both ubiquitous across myriad environ-
The broad enzymatic spectra of oligotrophs may predispose ments worldwide, illustrating that environmental and biolog-
them as plastic colonizers and/or degraders ical factors drive actual enzyme activity and efficiency for
polymer degradation in situ.
Parkinson et al. (1989) tested the ability of several fungal
species to grow on silica gel (medium lacking the polysaccha-
ride solidfying agent, agar) in the absence of added C and N
sources. Among fungi able to grow in these oligotrophic Potential ecotoxicity and other effects of biodegradable
conditions were Aspergillus, Fusarium, Mucor, and mulch films on agroecosystem sustainability
Penicillium spp., all of which also are genera reported to
colonize and/or decompose biodegradable plastics (Moore- Potential for accumulation of biodegradable plastic mulch
Kucera et al. 2014; Ghosh et al. 2013; Bhardwaj et al. 2012; fragments in soil
Kim and Rhee 2003; Shah et al. 2008). Oligotrophic fungi
have a broad range of enzymatic capabilities (e.g., Wainwright The largest single market for agricultural plastics is China, and
et al. 1993; Mellon et al. 2007) and can glean nutrients from recently, concerns have been raised about the accumulation of
nutrient-poor sources, i.e., dust, trace contaminants of water, recalcitrant plastic in soils there. In one location, accumulation
reagents, or glassware, and organic volatiles in the air (e.g., of more than 300 kg polyolefins/ha were measured in soils
Fontanille et al. 2012; Isola et al. 2013; reviewed by Prenafet- where agricultural plastics were used in cotton production for
Boldú et al. 2006; Hirsch 1986; Wainwright et al. 1991; more than 20 years (Sun 2014). Continued use of biodegrad-
Wainwright et al. 1993). In addition, some oligotrophic fungi able mulch films that pass the ISO 17088 (2012) and ASTM
have been shown to fix CO2 via anaplerotic reactions into D6400-12 (2012) composting standard, theoretically, would
Appl Microbiol Biotechnol

permit the accumulation of (1) plastic fragments smaller than


2.0 mm, (2) 10 % of organic carbon left after 180 days, (3) up
to 5 % original weight of untested organic constituents (at up
to 1 % for each component), and (4) up to 49 % of the
concentration of regulated metals allowed for sludges,
fertilizers, and composts. A similar situation would occur
under ASTM WK29802 (2014) currently being considered
for aerobically biodegradable plastics in a soil environment,
that is, persistence of 10 % of the plastic mass after 24 months,
for each constituent present in the material at a concentration
of more than 1 %. Assuming such, the authors calculate that, if
any portion of the remaining 10 % represents recalcitrant
polymers, metals, or untested components, they will accumu-
late with repeated applications in the soil in a manner that can
be estimated by the following relationship: Fig. 4 Theoretical effect of persistent plastic fraction (f=volume fraction
of a plastic mulch film remaining at the end of 1 year in soil) and time
volume fraction volume of residual plastic since first film application on the number of equivalent single films
¼  1000
of plastic in soil ðpptÞ tilled volume of soil remaining in soil (left axis) and on the volume fraction of residual,
persistent plastic accumulated in soil in parts per thousand (ppt, right
n⋅ f ⋅h1 p⋅ ⋅α⋅ axis). It is assumed that a new film is applied each year with the same
¼  1000 persistent plastic n, the depth of plowed soil is 150 mm, and 50 % of the
hs
total soil surface is covered in a plastic mulch having thickness of
0.024 mm (0.00095 in.)

Here, f represents the volume fraction of a plastic mulch 50 % of the area of the field (α=0.5). The persisting plastic
fraction in the soil, given these assumptions, is shown on the
film (or other contaminant) remaining at the end of 1 year in
soil. A key assumption in this model is that no further decay right axis in Fig. 4 as a function of f and time. It is important to
occurs. Thus, at the end of year 1, f of a film remains and is note that the relationship above is a theoretical one. Over repeat-
ed cropping cycles, the persisting fraction accumulates in the
plowed into the field, but another film is applied, so that at the
end of year 2, 2f film volumes remain in the soil. Therefore, at soil, where its aggregate effects on soil quality and ecosystem
the end of year n, n·f film volumes persist; this quantity is health have not been addressed systematically by researchers.
shown on the left axis in Fig. 4 as a function of f and time. A
value of f=1 would be typical of polyethylene, but f would Potential for synthetic toxins to enter terrestrial food web
drop dramatically the better the degradation characteristics of adsorbed to biodegradable plastic mulch fragments
the mulch film. Little or no starch would remain after 1 year,
so, for starch, f=0. Few studies have addressed the effect of biodegradable plastic
If the number of film volumes persisting is calculated, then on terrestrial ecosystems (Rudnik 2008). Pesticides and plastic
the fraction of soil volume occupied by persisting plastic can mulches are commonly used together, and there is a potential
be determined also, provided assumptions about soil tillage for certain pesticide residues to accumulate on fragments of
depth and mulch coverage are made. At any given time, the biodegradable mulch in soils, which may have unintended
total volume of persisting plastic is Vp =(n·f)·(h1p ·Ap), where consequences. The herbicides atrazine and metachlor
the thickness of one sheet of plastic film is h1p (p refers to adsorbed tightly to LDPE (Topp and Smith 1992). PE also
“plastic”), and the total area of the plastic film is Ap. Assuming efficiently adsorbed the insecticide permethrin (Sharom and
that eventually this plastic is tilled into a given working area Solomon 1981). In marine systems, plastic waste (mainly PE,
(As) and working depth (hs) of soil, the volume of soil into and polypropylene or PP) acts as a solid-phase extraction
which the persisting plastic is dispersed is Vs =hs ×As. The medium, concentrating toxins, notably, lipophilic legacy pol-
fraction of the soil volume occupied by the residual, persisting lutants whose chemical and biological degradation is slow,
plastic is the ratio of Vp/Vs. In the equation shown above, the such as 1,1,1-trichloro-2,2-bis(ρ-chlorophenyl)ethane (DDT)
volume fraction is expressed in parts per thousand (ppt), and and its breakdown products, as well as polychlorinated biphe-
the ratio Ap/As is defined as the fraction of tilled area initially nyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), or-
covered by the mulch film, α. ganochlorine pesticides, and aliphatic hydrocarbons (e.g.,
In practice, soil typically is tilled to a depth of about Mato et al. 2001; Rios et al. 2007, 2010; Pascall et al. 2005;
150 mm (6 in.), the plastic mulches have a thickness of about Teuten et al. 2009; Zarfl and Matthies 2010; Hirai et al. 2011).
0.024 mm (0.00095 in.), and the films are applied over about The properties of biodegradable plastic mulch fragments in
Appl Microbiol Biotechnol

soil are not identical to PE or PP in aqueous environments, so larvae (e.g.; Zeng et al. 2006, 2013; Döll et al. 2013; Caballero
the rate and kinetics of toxin adsorption would be expected to Ortiz et al. 2013; Trienens and Rohlfs 2011; Rohlfs et al.
differ. To our knowledge, these rates remain untested. How- 2007), it is logical to hypothesize that small fragments of
ever, the marine situation warrants a careful look at the inter- plastics in soil ecosystems, which may carry adsorbed myco-
action between plastics and pesticides in agricultural soils. toxins, could be toxic in the soil food web.

Potential for mycotoxins to concentrate on biodegradable


plastic mulch fragments
Is in-soil biodegradation an achievable goal?
Among fungi frequently reported to degrade biodegradable
plastics are Aspergillus, Fusarium, and Penicillium (reviewed Lourens Baas Becking famously stated “Everything is every-
by Ghosh et al. 2013; Bhardwaj et al. 2012; Kim and Rhee where, but the environment selects” (Baas Becking 1934).
2003; Shah et al. 2008). Some species of these fungi produce a This maxim might be used to predict that introduction of
number of potent toxins (e.g., aflatoxin, fumonisins, biodegradable plastics into soil would encourage the enlarge-
tricothecenes, cyclopiazonic acid, zearalenone, and ochratox- ment of populations of fungi and bacteria capable of
in) (Desjardins 2006; Schuman and D’Arcy 2006; Yu et al. degrading them. However, in a recent study (Moore-Kucera
2008; Schmale and Munkvold 2014). Moore-Kucera et al. et al. 2014), such plastics buried in soil for 6 months did not
(2014) isolated both Aspergillus and Fusarium from biode- have a statistically discernible effect upon the microbial com-
gradable plastic mulch containing Mater-Bi (Novamont, No- munity structure. Rather, the sites themselves, three environ-
vara, Italy). Others (Bergenholtz and Nielson 2002; Kim et al. mentally distinct locations in the U.S. that varied in crop
2000) also found that Aspergillus flavus is a proficient colo- history, edaphic factors, and environmental parameters, were
nizer of biodegradable plastic materials containing Mater-Bi. the main predictors of microbial community structure. Addi-
In fact, this attraction has been exploited by using Mater-Bi to tionally, in situ soil degradation of plastic biodegradable
distribute inoculum of the biocontrol strain A. flavus NRRL mulches was slow, in contrast to visually near-complete deg-
30797 (Accinelli et al. 2009) and to “bait” A. flavus from soil radation of a cellulosic mulch paper (Moore-Kucera et al.
for quantification purposes (Accinelli et al. 2012). A. flavus 2014; Li et al. 2014).
produces aflatoxin, a potent mycotoxin reported to bind A frequently posed potential solution to slow degradation
strongly to PE and other plastics (Scoppa and Marafante is the addition of crude or purified enzyme solutions. Another
1971). Accumulation of mycotoxin-producing fungi on bio- potential solution is to amend soils with plastic-degrading
degradable plastic mulches could lead to adsorption and ac- microorganisms. That strategy has inspired searches for native
cumulation of secreted mycotoxins onto the plastics. For soil microorganisms that break down biodegradable plastic
future studies involving biodegradable plastic mulches, mea- mulches (e.g., Moore-Kucera et al. 2014; Kasuya et al. 2009;
surement of mycotoxin accumulation should be considered. Abe et al. 2010). However, as discussed above, for the en-
zymes and/or microorganisms to be active, the soil environ-
Potential for ingestion of biodegradable plastic mulch ment must be amenable to microbial growth and to enzyme
fragments by animals production. Addition of enzymes produced by fermentation
(e.g., ligninolytic oxidases as in Khiyami et al. 2006) may
The ultimate destination for biodegradable plastic mulches is represent a viable strategy for expediting polymer breakdown
the soil, whether they are directly tilled in, or first exposed to in situ. Or, plastic-degrading bacteria or fungal spores could
composting conditions and then applied as an amendment. be encapsulated within an agricultural film. Wu (2008) report-
Although passage of plastics through the digestive tracts of ed immobilization of PLA-degrading Bacillus in a plastic film,
macro-organisms has been reported to facilitate plastic break- as well as its subsequent escape (indicating PLA breakdown).
down (Tsao et al. 1993; Whitney et al. 1993; Müller et al. However, these strategies would likely be cost-prohibitive on
2012; Wood and Zimmer 2014), it is unknown what effects the scale required for the agricultural industry. An alternate
ingesting plastic will have on terrestrial dwelling organisms. If way to consider the biodegradation of plastic mulches is from
plastic fragments have adsorbed pesticides, these may desorb a standpoint of agricultural practices. As described above,
upon ingestion. For example, insects that were fed toxin- oxidases tend to be produced by ligninocellulytic organisms
contaminated plastic fragments accumulated the toxins in their under conditions of nutrient limitation. Thus, the addition of
own tissues (Gaylor et al. 2012). Toxins in adipose tissues of high-lignin, high C:N organic matter (e.g., corn stubble and
birds were found to correlate positively with the amount of wheat straw) to soil might stimulate the production of these
ingested plastic (Ryan et al. 1988; Yamashita et al. 2011). enzymes and aid plastic breakdown. Similarly, the incorpora-
Furthermore, since Aspergillus secondary metabolites are tox- tion of any plant material into soil or compost is likely to
ic to birds, fish, and mammals (Yu et al. 2008) as well as insect introduce epiphytes, plant pathogens, and saprophytes whose
Appl Microbiol Biotechnol

cutinases and lipases may cleave structurally similar compo- ecosystem services to cropping systems in addition to decom-
nents of biodegradable plastic mulches. position. For example, endophytic and mycorrhizal fungi
It is important to note that soil and compost are not the only boost plant productivity, and certain plant-associated fungi
potential end-of-life options for biodegradable plastic and bacteria help plants fend off pathogenic microbes. While
mulches. PHB and PHBV, as well as PCL, have been used a recent study (Moore-Kucera et al. 2014) did not find any
successfully as solid substrates and electron donors for bacte- differences in the microbial population structure on a broad
rial denitrification of wastewater (reviewed by Hiraishi and scale, fine-scale analyses of the effect of mulch film accumu-
Khan 2003), as has PLA (Takahashi et al. 2011). Germane to lation on both microbial population structure and on the
the toxin accumulation concerns raised above, Yoshida et al. biochemistry that underlies plant–microbe associations should
(2013) showed that a biodegradable, starch-based plastic pro- be studied.
vided the necessary electron donor, H2, for microbial reduc- Overall, the concept of biodegradable plastic mulch films
tive dechlorination of a polychlorinated polyaromatic hydro- represents an exciting option for sustainable agriculture. How-
carbon. The first studies are particularly relevant to agricul- ever, this review outlines need for collaborations between
ture, where animal husbandry produces copious wastewater, polymer engineers and microbiologists, agricultural scientists,
and the second study suggests that, even if agricultural mulch toxicologists, and soil ecologists. Finally, bona fide, useful
fragments accumulate toxins as discussed above, they may scientific analysis will require knowledge of all parties about
also facilitate breakdown of those toxins. the (currently proprietary) components of commercially rele-
vant agricultural mulch films.

Conclusions Acknowledgments This review resulted from work funded by a grant


from the United States Department of Agriculture, National Institute of
The sustainability of agricultural practices over the long term Food and Agriculture, Specialty Crops Research Initiative, Standard
Research and Extension Project Grant Award No. 2009-02484.
requires not only agricultural, but also economic and ecolog-
ical benefits. From the point of view of plant productivity and Conflict of interest The authors declare that they have no conflict of
disease management, plastic mulches remain a critical tool for interest.
weed suppression, soil moisture retention, and soil tempera-
ture control. Commercially available plastic mulches contain-
ing biodegradable components have been shown to perform References
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