When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films

Agricultural plastic mulching films have been an environmental concern for decades. The effects of the interactions between the anthropogenic plastisphere and other soil biospheres, particularly that of earthworms, on the fate of plastics remain poorly understood. Here, we investigated the decomposi...

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Main Authors: Caide Huang, Liuwei Wang, Wei-Min Wu, Yvan Capowiez, Yuhui Qiao, Deyi Hou
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Environment International
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Online Access:http://www.sciencedirect.com/science/article/pii/S0160412025000601
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author Caide Huang
Liuwei Wang
Wei-Min Wu
Yvan Capowiez
Yuhui Qiao
Deyi Hou
author_facet Caide Huang
Liuwei Wang
Wei-Min Wu
Yvan Capowiez
Yuhui Qiao
Deyi Hou
author_sort Caide Huang
collection DOAJ
description Agricultural plastic mulching films have been an environmental concern for decades. The effects of the interactions between the anthropogenic plastisphere and other soil biospheres, particularly that of earthworms, on the fate of plastics remain poorly understood. Here, we investigated the decomposition of buried nonbiodegradable low-density polyethylene (LDPE) versus biodegradable PBTA/PLA copolymers in the presence of earthworms (Amynthas cortices) in dynamic microcosms. Earthworms significantly enhanced the biodegradation of plastic films in situ, as confirmed by mass reduction, surface modification, and changes in the molecular weights of films. Notably, the PBTA/PLA films exhibited a 1.41-fold increase in mass loss and a 5.69% reduction in the number-average molecular weight when incubated with earthworms. Earthworms influenced the microbial assembly within the plastisphere by increasing both bacterial and fungal biodiversity, as well as their network complexity. The time-decay patterns in the abundance of keystone degrader taxa, including the genera Noviherbaspirillum, Rhizobacter, and Mortierella, were mitigated by earthworms over the 60-day period. Additionally, earthworms preferentially consumed recalcitrant dissolved organic matter in LDPE and PBAT/PLA plastisphere soils, thereby increasing the bioavailability of components that serve as nutrient supplies for plastisphere microbiomes. Our findings demonstrate that earthworms enhance the decomposition of plastics in soils via cross-species interplay within the plastisphere and drilosphere, contributing not only to soil conditioning and biodiversity but also to plastic biodegradation in natural agroecosystems.
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spelling doaj-art-42344a7f45864f6abe7240f53983af0f2025-02-05T04:31:04ZengElsevierEnvironment International0160-41202025-02-01196109309When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic filmsCaide Huang0Liuwei Wang1Wei-Min Wu2Yvan Capowiez3Yuhui Qiao4Deyi Hou5School of Environment, Tsinghua University, Beijing 100084, ChinaSchool of Environment, Tsinghua University, Beijing 100084, ChinaDepartment of Civil and Environmental Engineering, William & Cloy Codiga Resource Recovery Center, Stanford University, Stanford, CA 94305-4020, United StatesINRAE, UMR EMMAH INRAE-Université d’Avignon, Site Agroparc, 84914, Avignon, Cedex 09, FranceCollege of Resources and Environmental Science, China Agricultural University, Beijing 100193, ChinaSchool of Environment, Tsinghua University, Beijing 100084, China; Corresponding author.Agricultural plastic mulching films have been an environmental concern for decades. The effects of the interactions between the anthropogenic plastisphere and other soil biospheres, particularly that of earthworms, on the fate of plastics remain poorly understood. Here, we investigated the decomposition of buried nonbiodegradable low-density polyethylene (LDPE) versus biodegradable PBTA/PLA copolymers in the presence of earthworms (Amynthas cortices) in dynamic microcosms. Earthworms significantly enhanced the biodegradation of plastic films in situ, as confirmed by mass reduction, surface modification, and changes in the molecular weights of films. Notably, the PBTA/PLA films exhibited a 1.41-fold increase in mass loss and a 5.69% reduction in the number-average molecular weight when incubated with earthworms. Earthworms influenced the microbial assembly within the plastisphere by increasing both bacterial and fungal biodiversity, as well as their network complexity. The time-decay patterns in the abundance of keystone degrader taxa, including the genera Noviherbaspirillum, Rhizobacter, and Mortierella, were mitigated by earthworms over the 60-day period. Additionally, earthworms preferentially consumed recalcitrant dissolved organic matter in LDPE and PBAT/PLA plastisphere soils, thereby increasing the bioavailability of components that serve as nutrient supplies for plastisphere microbiomes. Our findings demonstrate that earthworms enhance the decomposition of plastics in soils via cross-species interplay within the plastisphere and drilosphere, contributing not only to soil conditioning and biodiversity but also to plastic biodegradation in natural agroecosystems.http://www.sciencedirect.com/science/article/pii/S0160412025000601PlasticsAmynthas corticisBiodegradationPlastisphereDissolved organic matter
spellingShingle Caide Huang
Liuwei Wang
Wei-Min Wu
Yvan Capowiez
Yuhui Qiao
Deyi Hou
When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
Environment International
Plastics
Amynthas corticis
Biodegradation
Plastisphere
Dissolved organic matter
title When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
title_full When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
title_fullStr When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
title_full_unstemmed When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
title_short When plastisphere and drilosphere meet: Earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
title_sort when plastisphere and drilosphere meet earthworms facilitate microbiome and nutrient turnover to accelerate biodegradation of agricultural plastic films
topic Plastics
Amynthas corticis
Biodegradation
Plastisphere
Dissolved organic matter
url http://www.sciencedirect.com/science/article/pii/S0160412025000601
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