The interaction between plastics and microorganisms in soil and their ecological effects
JU Zhi-cheng1,2, JIN De-cai1,2, DENG Ye1,2
1. Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; 2. School of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:The pollution of plastics and microplastics in the soil environment attracted lots of attentions in recent years. This paper reviewed the latest research progresses on the interaction between microorganisms and soil plastics. The main contents included, (i) the source and migration of soil plastics and their basic characteristics of long-term storage forms in the soil; (ii) the impacts of soil microorganism on plastics; (iii) the impacts of plastic pollution on soil microbiota, enzyme activities, animals and crop production, and the potential impact on the function of global terrestrial ecosystems. Finally, the future research directions on plastics and microplastics pollution were discussed, topics range from functional microorganisms, experimental design, plastisphere, large-scale and long-term studies on plastics and soil microorganisms. This review provided valuable references for understanding and solving plastic pollution in soil from a microbiological perspective.
鞠志成, 金德才, 邓晔. 土壤中塑料与微生物的相互作用及其生态效应[J]. 中国环境科学, 2021, 41(5): 2352-2361.
JU Zhi-cheng, JIN De-cai, DENG Ye. The interaction between plastics and microorganisms in soil and their ecological effects. CHINA ENVIRONMENTAL SCIENCECE, 2021, 41(5): 2352-2361.
Carpente E J, Anderson S J, Miklas H P, et al. Polystyrene spherules in coastal waters[J]. Science, 1972,178(4062):749-750.
[2]
Tokiwa Y, Suzuki T. Hydrolysis of polyesters by lipases[J]. Nature, 1977,270(5632):76-78.
[3]
Wright S L, Kelly F J. Plastic and human health:A micro issue?[J]. Environmental Science & Technology, 2017,51(12):6634-6647.
[4]
Huerta Lwanga E, Gertsen H, Gooren H, et al. Microplastics in the terrestrial ecosystem:Implications for lumbricus terrestris (Oligochaeta, Lumbricidae)[J]. Environmental Science & Technology, 2016,50(5):2685-2691.
[5]
Rillig M C. Microplastic in terrestrial ecosystems and the soil?[J]. Environmental Science & Technology, 2012,46(12):6453-6454.
[6]
Huerta Lwanga E, Mendoza Vega J, Ku Quej V, et al. Field evidence for transfer of plastic debris along a terrestrial food chain[J]. Scientific Reports, 2017,7(1):14071.
[7]
Abel D, Kloas W, Zarfl C, et al. Microplastics as an emerging threat to terrestrial ecosystems[J]. Global Change Biology, 2018,24(4):1405-1416.
[8]
Qi R, Jones D L, Li Z, et al. Behavior of microplastics and plastic film residues in the soil environment:A critical review[J]. Science of the Total Environment, 2020,703:134722.
[9]
Delgado-Baquerizo M, Grinyer J, Reich P B, et al. Relative importance of soil properties and microbial community for soil functionality:insights from a microbial swap experiment[J]. Functional Ecology, 2016,30(11):1862-1873.
[10]
Qian H, Zhang M, Liu G, et al. Effects of soil residual plastic film on soil microbial community structure and fertility[J]. Water Air & Soil Pollution, 2018,229(8):261.
[11]
de Souza Machado A A, Lau C W, Till J, et al. Impacts of microplastics on the soil biophysical environment[J]. Environmental Science & Technology, 2018,52(17):9656-9665.
[12]
朱永官,朱冬,许通,等.(微)塑料污染对土壤生态系统的影响:进展与思考[J]. 农业环境科学学报, 2019,38(11):1-6. Zhu Y G, Zhu D, Xu T, et al. Impacts of (micro) plastics on soil ecosystem:Progress and perspective[J]. Journal of Agro-Environment Science, 2019,38(1):1-6.
[13]
Kasirajan S, Ngouajio M. Polyethylene and biodegradable mulches for agricultural applications:a review[J]. Agronomy for Sustainable Development, 2013,33(2):443-443.
[14]
Nizzetto L, Bussi G, Futter M N, et al. A theoretical assessment of microplastic transport in river catchments and their retention by soils and river sediments[J]. Environmental Science-Processes & Impacts, 2016,18(8):1050-1059.
[15]
Blaesing M, Amelung W. Plastics in soil:Analytical methods and possible sources[J]. Science of the Total Environment, 2018,612:422-435.
[16]
Horton A A, Walton A, Spurgeon D J, et al. Microplastics in freshwater and terrestrial environments:Evaluating the current understanding to identify the knowledge gaps and future research priorities[J]. Science of the Total Environment, 2017,586:127-141.
[17]
Mintenig S M, Int-Veen I, Loeder M G J, et al. Identification of microplastic in effluents of waste water treatment plants using focal plane array-based micro-Fourier-transform infrared imaging[J]. Water Research, 2017,108:365-372.
[18]
Foitzik M J, Unrau H J, Gauterin F, et al. Investigation of ultra fine particulate matter emission of rubber tires[J]. Wear, 2018,394:87-95.
[19]
Dris R, Gasperi J, Saad M, et al. Synthetic fibers in atmospheric fallout:A source of microplastics in the environment?[J]. Marine Pollution Bulletin, 2016,104(1/2):290-293.
[20]
Thompson R C, Olsen Y, Mitchell R P, et al. Lost at sea:Where is all the plastic?[J]. Science, 2004,304(5672):838-838.
[21]
Gigault J, Ter Halle A, Baudrimont M, et al. Current opinion:What is a nanoplastic?[J]. Environmental Pollution, 2018,235:1030-1034.
[22]
Gaylor M O, Harvey E, Hale R C. Polybrominated diphenyl ether (PBDE) accumulation by earthworms (eisenia fetida) exposed to biosolids-, polyurethane foam microparticle-, and penta-BDE-amended soils[J]. Environmental Science & Technology, 2013, 47(23):13831-13839.
[23]
Rillig M C, Bonkowski M. Microplastic and soil protists:A call for research[J]. Environmental Pollution, 2018,241:1128-1131.
[24]
Ju H, Zhu D, Qiao M. Effects of polyethylene microplastics on the gut microbial community, reproduction and avoidance behaviors of the soil springtail, Folsomia candida[J]. Environmental Pollution, 2019, 247:890-897.
[25]
Rillig M C, Ziersch L, Hempel S. Microplastic transport in soil by earthworms[J]. Sci Rep, 2017,7(1):1362.
[26]
Rillig M C, De Souza Machado A A, Lehmann A, et al. Evolutionary implications of microplastics for soil biota[J]. Environ Chem, 2019,16(1):3-7.
[27]
Wimpenny J, Manz W, Szewzyk U. Heterogenety in biofilms[J]. Fems Microbiology Reviews, 2001,24(5):661-671.
[28]
Potera C. Microbes occupy, may be degrading plastic debris in oceans[J]. Microbe, 2013,8(11):438-439.
[29]
Harrison J P, Sapp M, Schratzberger M, et al. Interactions between microorganisms and marine microplastics:a call for research[J]. Marine Technology Society Journal, 2011,45(2):12-20.
[30]
Zettler E R, Mincer T J, Amaral-Zettler L A. Life in the ‘plastisphere’:microbial communities on plastic marine debris[J]. Environmental Science & Technology, 2013,47(13):7137-7146.
[31]
Amaral-Zettler L A, Zettler E R, Slikas B, et al. The biogeography of the Plastisphere:implications for policy[J]. Frontiers in Ecology and the Environment, 2015,13(10):541-546.
[32]
Zhang M, Zhao Y, Qin X, et al. Microplastics from mulching film is a distinct habitat for bacteria in farmland soil[J]. Science of the Total Environment, 2019,688:470-478.
[33]
Burger M, Woods R G, Mccarthy C, et al. Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator[J]. Microbiology-Sgm, 2000, 146:3149-3155.
[34]
Philippot L, Andersson S G E, Battin T J, et al. The ecological coherence of high bacterial taxonomic ranks[J]. Nature Reviews Microbiology, 2010,8(7):523-529.
[35]
Wright R J, Langille M G I, Walker TR. Food or just a free ride? A meta-analysis reveals the global diversity of the Plastisphere[J]. The ISME Journal, 2020,15(3):789-806.
[36]
Zhang H, Wang J, Zhou B, et al. Enhanced adsorption of oxytetracycline to weathered microplastic polystyrene:Kinetics, isotherms and influencing factors[J]. Environmental Pollution, 2018,243:1550-1557.
[37]
Andrady A L. Microplastics in the marine environment[J]. Marine Pollution Bulletin, 2011,62(8):1596-1605.
[38]
Shah A A, Hasan F, Hameed A, et al. Biological degradation of plastics:a comprehensive review[J]. Biotechnology Advances, 2008,26(3):246-265.
[39]
Guo X, Wang X, Zhou X, et al. Sorption of four hydrophobic organic compounds by three chemically distinct polymers:role of chemical and physical composition[J]. Environmental Science & Technology, 2012,46(13):7252-7259.
[40]
Mcgivney E, Cederholm L, Barth A, et al. Rapid physicochemical changes in microplastic induced by biofilm formation[J]. Frontiers in Bioengineering and Biotechnology, 2020,8:205.
[41]
Fierer N. Embracing the unknown:disentangling the complexities of the soil microbiome[J]. Nature Reviews Microbiology, 2017,15(10):579-590.
[42]
Kong X, Jin D, Jin S, et al. Responses of bacterial community to dibutyl phthalate pollution in a soil-vegetable ecosystem[J]. Journal of Hazardous Materials, 2018,353:142-150.
[43]
Ren X, Tang J, Liu X, et al. Effects of microplastics on greenhouse gas emissions and the microbial community in fertilized soil[J]. Environmental Pollution, 2020,256:113347.
[44]
Awet T T, Kohl Y, Meier F, et al. Effects of polystyrene nanoparticles on the microbiota and functional diversity of enzymes in soil[J]. Environmental Ences Europe, 2018,30(1):11.
[45]
Liu H, Yang X, Liu G, et al. Response of soil dissolved organic matter to microplastic addition in Chinese loess soil[J]. Chemosphere, 2017,185:907-917.
[46]
Zhang G S, Liu Y F. The distribution of microplastics in soil aggregate fractions in southwestern China[J]. Science of the Total Environment, 2018,642:12-20.
[47]
Xie H J, Shi Y J, Zhang J, et al. Degradation of phthalate esters (PAEs) in soil and the effects of PAEs on soil microcosm activity[J]. Journal of Chemical Technology & Biotechnology, 2010,85(8):1108-1116.
[48]
Kong X, Jin D, Tai X, et al. Bioremediation of dibutyl phthalate in a simulated agricultural ecosystem by Gordonia sp. strain QH-11 and the microbial ecological effects in soil[J]. Science of the Total Environment, 2019,667:691-700.
[49]
Huang Y, Zhao Y, Wang J, et al. LDPE microplastic films alter microbial community composition and enzymatic activities in soil[J]. Environmental Pollution, 2019,254:112983.
[50]
魏子艳,金德才,邓晔.环境微生物宏基因组学研究中的生物信息学方法[J]. 微生物学通报, 2015,42(5):890-901. Wei Z, Jin D, Deng Y. Bioinformatics tools and applications in the study of environmental microbial metagenomics[J]. Microbiology China, 2015,42(5):890-901.
[51]
Wang J, Lv S, Zhang M, et al. Effects of plastic film residues on occurrence of phthalates and microbial activity in soils[J]. Chemosphere, 2016,151:171-177.
[52]
Lehmann A, Zheng W, Rillig M C. Soil biota contributions to soil aggregation[J]. Nature Ecology & Evolution, 2017,1(12):1828.
[53]
Sebiomo A, Ogundero V W, Bankole S A. Effect of four herbicides on microbial population, soil organic matter and dehydrogenase activity[J]. African Journal of Biotechnology, 2010,10(31):770-778.
[54]
Muscolo A, Settineri G, Attina E. Early warning indicators of changes in soil ecosystem functioning[J]. Ecological Indicators, 2015,48:542-549.
[55]
Yang X, Bento C P M, Chen H, et al. Influence of microplastic addition on glyphosate decay and soil microbial activities in Chinese loess soil[J]. Environmental Pollution, 2018,242:338-347.
[56]
He Z, Deng Y, Van Nostrand J D, et al. GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity[J]. The ISME Journal, 2010,4(9):1167-1179.
[57]
Jin D, Bai Z, Chang D, et al. Biodegradation of di-n-butyl phthalate by an isolated Gordonia sp. strain QH-11:Genetic identification and degradation kinetics[J]. Journal of Hazardous Materials, 2012,221-222:80-85.
[58]
Jin D, Kong X, Cui B, et al. Biodegradation of di-n-butyl phthalate by a newly isolated halotolerant Sphingobium sp[J]. International Journal of Molecular Sciences, 2013,14(12):24046-24054.
[59]
Wang Z G, You Y M, Xu W H, et al. Dimethyl phthalate altered the microbial metabolic pathways in a Mollisol[J]. European Journal of Soil Science, 2018,69(3):439-449.
[60]
Deng Y, He Z, Xiong J, et al. Elevated carbon dioxide accelerates the spatial turnover of soil microbial communities[J]. Global Change Biology, 2016,22(2):957-964.
[61]
Van Elsas J D, Bailey M J. The ecology of transfer of mobile genetic elements[J]. Fems Microbiology Ecology, 2002,42(2):187-197.
[62]
Heuer H, Kopmann C, Binh C T T, et al. Spreading antibiotic resistance through spread manure:characteristics of a novel plasmid type with low%G plus C content[J]. Environmental Microbiology, 2009,11(4):937-949.
[63]
Heuer H, Smalla K. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months[J]. Environmental Microbiology, 2007,9(3):657-666.
[64]
Aminov RI. Horizontal gene exchange in environmental microbiota[J]. Frontiers in Microbiology, 2011,2:158.
[65]
Wu X, Pan J, Li M, et al. Selective enrichment of bacterial pathogens by microplastic biofilm[J]. Water Research, 2019,165:114979.
[66]
Arias Andres M, Kluemper U, Rojas Jimenez K, et al. Microplastic pollution increases gene exchange in aquatic ecosystems[J]. Environmental Pollution, 2018,237:253-261.
[67]
Wang Z, Wang C, You Y, et al. Response of Pseudomonas fluorescens to dimethyl phthalate[J]. Ecotoxicology and Environmental Safety, 2019,167:36-43.
[68]
Jin Y, Lu L, Tu W, et al. Impacts of polystyrene microplastic on the gut barrier, microbiota and metabolism of mice[J]. Science of the Total Environment, 2019,649:308-317.
[69]
Lei L, Wu S, Lu S, et al. Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans[J]. Science of the Total Environment, 2018, 619-620:1-8.
[70]
Wang J, Coffin S, Sun C, et al. Negligible effects of microplastics on animal fitness and HOC bioaccumulation in earthworm Eisenia fetida in soil[J]. Environmental Pollution, 2019,249:776-784.
[71]
Rodriguez Seijo A, Lourenco J, Rocha Santos TaP, et al. Histopathological and molecular effects of microplastics in Eisenia andrei Bouche[J]. Environmental Pollution, 2017,220:495-503.
[72]
Zhu D, Chen Q, An X, et al. Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition[J]. Soil Biology & Biochemistry, 2018,116:302-310.
[73]
Lili L, Mengting L, Yang S, et al. Polystyrene (nano) microplastics cause size-dependent neurotoxicity, oxidative damage and other adverse effects in Caenorhabditis elegans[J]. Environmental Science Nano, 2018,10:1039.
[74]
Zhu B, Fang Y, Zhu D, et al. Exposure to nanoplastics disturbs the gut microbiome in the soil oligochaete Enchytraeus crypticus[J]. Environmental Pollution, 2018,239:408-415.
[75]
Gao H, Yan C, Liu Q, et al. Effects of plastic mulching and plastic residue on agricultural production:A meta-analysis[J]. Science of the Total Environment, 2018,651:484-492.
[76]
Ding L, Zhang S, Wang X, et al. The occurrence and distribution characteristics of microplastics in the agricultural soils of Shaanxi Province, in north-western China[J]. Science of the Total Environment, 2020,720:137525.
[77]
Qi Y, Yang X, Mejia Pelaez A, et al. Macro-and micro-plastics in soil-plant system:Effects of plastic mulch film residues on wheat (Triticum aestivum) growth[J]. Science of the Total Environment, 2018,645:1048-1056.
[78]
Steinmetz Z, Wollmann C, Schaefer M, et al. Plastic mulching in agriculture. Trading short-term agronomic benefits for long-term soil degradation?[J]. Science of the Total Environment, 2016,550:690-705.
[79]
Sander M. Biodegradation of polymeric mulch films in agricultural soils:concepts, knowledge gaps, and future research directions[J]. Environmental Science & Technology. 2019,53(5):2304-2315.
[80]
Machado A, Lau C W, Kloas W, et al. Microplastics can change soil properties and affect plant performance[J]. Environmental Science & Technology, 2019,53(10):6044-6052.
[81]
Li L, Luo Y, Li R, et al. Effective uptake of submicrometre plastics by crop plants via a crack-entry mode[J]. Nature Sustainability, 2020,3:929-937.
[82]
Lozano Y M, Rillig M C. Effects of microplastic fibers and drought on plant communities[J]. Environmental Science & Technology. 2020,54(10):6166-6173.
[83]
Zota A R, Calafat A M, Woodruff T J. Temporal trends in phthalate exposures:findings from the national health and nutrition examination survey, 2001-2010[J]. Environmental Health Perspectives, 2014, 122(3):235-241.
[84]
Ramos L, Berenstein G, Hughes E A, et al. Polyethylene film incorporation into the horticultural soil of small periurban production units in Argentina[J]. Science of the Total Environment, 2015,523:74-81.
[85]
Sun M, Ye M, Jiao W, et al. Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid[J]. Journal of Hazardous Materials, 2018,345:131-139.
[86]
Rillig M C. Microplastic disguising as soil carbon storage[J]. Environmental Science & Technology, 2018,52(11):6079.
[87]
Kramm J, Voelker C, Wagner M. Superficial or substantial:why care about microplastics in the anthropocene?[J]. Environmental Science & Technology, 2018,52(6):3336-3337.