such as middens, casts and the burrow system (Fig. 4). The high nutrient content of
these structures boosts microbial proliferation. Moreover, the presence of cutaneous
mucus (burrow linings and middens) and gastrointestinal mucus (casts and middens)
also provide a C-labile source for microfauna and mesofauna foraging. Many studies
have examined the organic carbon dynamic and microbial community structure of
earthworm casts [139, 140], burrow linings [72, 139] and middens [54, 55, 68]. All
them conclude that these biostructures are hotspots of organic matter decomposition,
displaying higher microbial and enzymatic activities respect to undisturbed soil
[70, 71, 141]. Therefore, it can be assumed that earthworm biostructures are also
microenvironments for API biodegradation. However, because of the organic matter
content of biostructures, API may also be immobilised by binding to organic ligands,
thus reducing their bioavailability and transport in soil [47, 142, 143]. Extracellular
enzymes or exoenzymes represent also a pivotal mechanism of API inactivation.
Enzymes such as phenol oxidases (laccases) and peroxidases (manganese peroxidase
and lignin peroxidase) are actively involved in the oxidative metabolism of organic
contaminants including APIs [144, 145]. For example, laccase from the white-rot
fungi (lignin degraders) Trametes versicolor removed 100%, 95% and 85% of
diclofenac, trimethoprim and carbamazepine, respectively, from aqueous enzymatic
preparations [146]. Similarly, peroxidases from multiple biological sources are also
able to degrade (>80%) many APIs such as triclosan, carbamazepine, naproxen and
antibiotics [145]. Many other white-rot fungi species degrade anticancer drugs via
oxidative reactions catalysed by laccases and peroxidases [147]. These enzymes are
produced and excreted to the environment by soil microorganisms [148], and the
presence of lignocellulosic-rich organic matter induces their production [149]. Furthermore, laccase activity requires molecular oxygen, so earthworm burrowing
activity should facilitate laccase-mediated degradation of organic pollutants [150]
because of soil aeration increase. Therefore, API dissipation by these exoenzymes
should be a potential biodegradation process, particularly in earthworm
biostructures.
Earthworm gut-associated inactivating processes involve gut microbiota and the
enzymes secreted by the earthworm gut epithelium (Fig. 4). Many digestive enzymes
have been measured in the gastrointestinal content of earthworms such as lipases,
esterases, chitinases and cellulases [151–153]. Furthermore, laccase activity has also
been found in the gastrointestinal content of epigeic and endogeic earthworms,
although its activity level is low respect to other digestive enzymes [154], an
expected finding if one considers that the earthworm alimentary canal is anoxic
[155] and laccases require molecular oxygen. However, laccase activity has been
measured in the casts of some earthworm species [141], suggesting that microbialmediated oxidative metabolism occurs in these biostructures. Carboxylesterases are
other group of enzymes with potential to metabolise pharmaceuticals and illicit
drugs containing the ester bond such as capecitabine, cilazapril, clopidogrel, cocaine,
dabigatran etexilate, enalapril, heroin, imidapril, irinotecan, meperidine, methylphenidate, olmesartan, orlistat, oseltamivir, quinapril, ramipril, temocapril and
trandolapril [156]. Some of these compounds are detected in reclaimed wastewater,
surface water and groundwater [157, 158]. Interestingly, carboxylesterase activity
358
J. C. Sanchez-Hernandez
these structures boosts microbial proliferation. Moreover, the presence of cutaneous
mucus (burrow linings and middens) and gastrointestinal mucus (casts and middens)
also provide a C-labile source for microfauna and mesofauna foraging. Many studies
have examined the organic carbon dynamic and microbial community structure of
earthworm casts [139, 140], burrow linings [72, 139] and middens [54, 55, 68]. All
them conclude that these biostructures are hotspots of organic matter decomposition,
displaying higher microbial and enzymatic activities respect to undisturbed soil
[70, 71, 141]. Therefore, it can be assumed that earthworm biostructures are also
microenvironments for API biodegradation. However, because of the organic matter
content of biostructures, API may also be immobilised by binding to organic ligands,
thus reducing their bioavailability and transport in soil [47, 142, 143]. Extracellular
enzymes or exoenzymes represent also a pivotal mechanism of API inactivation.
Enzymes such as phenol oxidases (laccases) and peroxidases (manganese peroxidase
and lignin peroxidase) are actively involved in the oxidative metabolism of organic
contaminants including APIs [144, 145]. For example, laccase from the white-rot
fungi (lignin degraders) Trametes versicolor removed 100%, 95% and 85% of
diclofenac, trimethoprim and carbamazepine, respectively, from aqueous enzymatic
preparations [146]. Similarly, peroxidases from multiple biological sources are also
able to degrade (>80%) many APIs such as triclosan, carbamazepine, naproxen and
antibiotics [145]. Many other white-rot fungi species degrade anticancer drugs via
oxidative reactions catalysed by laccases and peroxidases [147]. These enzymes are
produced and excreted to the environment by soil microorganisms [148], and the
presence of lignocellulosic-rich organic matter induces their production [149]. Furthermore, laccase activity requires molecular oxygen, so earthworm burrowing
activity should facilitate laccase-mediated degradation of organic pollutants [150]
because of soil aeration increase. Therefore, API dissipation by these exoenzymes
should be a potential biodegradation process, particularly in earthworm
biostructures.
Earthworm gut-associated inactivating processes involve gut microbiota and the
enzymes secreted by the earthworm gut epithelium (Fig. 4). Many digestive enzymes
have been measured in the gastrointestinal content of earthworms such as lipases,
esterases, chitinases and cellulases [151–153]. Furthermore, laccase activity has also
been found in the gastrointestinal content of epigeic and endogeic earthworms,
although its activity level is low respect to other digestive enzymes [154], an
expected finding if one considers that the earthworm alimentary canal is anoxic
[155] and laccases require molecular oxygen. However, laccase activity has been
measured in the casts of some earthworm species [141], suggesting that microbialmediated oxidative metabolism occurs in these biostructures. Carboxylesterases are
other group of enzymes with potential to metabolise pharmaceuticals and illicit
drugs containing the ester bond such as capecitabine, cilazapril, clopidogrel, cocaine,
dabigatran etexilate, enalapril, heroin, imidapril, irinotecan, meperidine, methylphenidate, olmesartan, orlistat, oseltamivir, quinapril, ramipril, temocapril and
trandolapril [156]. Some of these compounds are detected in reclaimed wastewater,
surface water and groundwater [157, 158]. Interestingly, carboxylesterase activity
358
J. C. Sanchez-Hernandez