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Distinct Bacterial and Fungal Communities Colonizing Waste Plastic Films Buried for More Than 20 Years in Four Landfill Sites in Korea

  • Joon-hui Chung (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Jehyeong Yeon (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Hoon Je Seong (Macrogen Inc.) ;
  • Si-Hyun An (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Da-Yeon Kim (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Younggun Yoon (College of Environmental and Bioresource Sciences, Jeonbuk National University) ;
  • Hang-Yeon Weon (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Jeong Jun Kim (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA)) ;
  • Jae-Hyung Ahn (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration (RDA))
  • Received : 2022.06.13
  • Accepted : 2022.11.10
  • Published : 2022.12.28

Abstract

Plastic pollution has been recognized as a serious environmental problem, and microbial degradation of plastics is a potential, environmentally friendly solution to this. Here, we analyzed and compared microbial communities on waste plastic films (WPFs) buried for long periods at four landfill sites with those in nearby soils to identify microbes with the potential to degrade plastics. Fourier-transform infrared spectroscopy spectra of these WPFs showed that most were polyethylene and had signs of oxidation, such as carbon-carbon double bonds, carbon-oxygen single bonds, or hydrogen-oxygen single bonds, but the presence of carbonyl groups was rare. The species richness and diversity of the bacterial and fungal communities on the films were generally lower than those in nearby soils. Principal coordinate analysis of the bacterial and fungal communities showed that their overall structures were determined by their geographical locations; however, the microbial communities on the films were generally different from those in the soils. For the pulled data from the four landfill sites, the relative abundances of Bradyrhizobiaceae, Pseudarthrobacter, Myxococcales, Sphingomonas, and Spartobacteria were higher on films than in soils at the bacterial genus level. At the species level, operational taxonomic units classified as Bradyrhizobiaceae and Pseudarthrobacter in bacteria and Mortierella in fungi were enriched on the films. PICRUSt analysis showed that the predicted functions related to amino acid and carbohydrate metabolism and xenobiotic degradation were more abundant on films than in soils. These results suggest that specific microbial groups were enriched on the WPFs and may be involved in plastic degradation.

Keywords

Acknowledgement

This work was supported by the National Institute of Agricultural Sciences, Rural Development Administration, Republic of Korea (Project No. PJ014974).

References

  1. MacLeod M, Arp HPH, Tekman MB, Jahnke A. 2021. The global threat from plastic pollution. Science 373: 61-65.  https://doi.org/10.1126/science.abg5433
  2. Yoshida S, Hiraga K, Takehana T, Taniguchi I, Yamaji H, Maeda Y, et al. 2016. A bacterium that degrades and assimilates poly(ethylene terephthalate). Science 351: 1196-1199.  https://doi.org/10.1126/science.aad6359
  3. Son HF, Cho IJ, Joo S, Seo H, Sagong H-Y, Choi SY, et al. 2019. Rational protein engineering of thermo-stable PETase from Ideonella sakaiensis for highly efficient PET degradation. ACS Catal. 9: 3519-3526.  https://doi.org/10.1021/acscatal.9b00568
  4. Tournier V, Topham CM, Gilles A, David B, Folgoas C, Moya-Leclair E, et al. 2020. An engineered PET depolymerase to break down and recycle plastic bottles. Nature 580: 216-219.  https://doi.org/10.1038/s41586-020-2149-4
  5. Geyer R, Jambeck JR, Law KL. 2017. Production, use, and fate of all plastics ever made. Sci. Adv. 3: e1700782. 
  6. Danso D, Chow J, Streit WR. 2019. Plastics: Environmental and biotechnological perspectives on microbial degradation. Appl. Environ. Microbiol. 85: e01095-01019. 
  7. Montazer Z, Habibi Najafi MB, Levin DB. 2020. Challenges with verifying microbial degradation of polyethylene. Polymers 12: 123. 
  8. Ghatge S, Yang Y, Ahn JH, Hur HG. 2020. Biodegradation of polyethylene: a brief review. Appl. Biol. Chem. 63: 27. 
  9. Otake Y, Kobayashi T, Asabe H, Murakami N, Ono K. 1995. Biodegradation of low-density polyethylene, polystyrene, polyvinyl chloride, and urea formaldehyde resin buried under soil for over 32 years. J. Appl. Polym. Sci. 56: 1789-1796.  https://doi.org/10.1002/app.1995.070561309
  10. Kim SK, Kim JS, Lee H, Lee HJ. 2021. Abundance and characteristics of microplastics in soils with different agricultural practices: Importance of sources with internal origin and environmental fate. J. Hazard. Mater. 403: 123997. 
  11. Steinmetz Z, Wollmann C, Schaefer M, Buchmann C, David J, Troger J, et al. 2016. Plastic mulching in agriculture. Trading short-term agronomic benefits for long-term soil degradation? Sci. Total Environ. 550: 690-705.  https://doi.org/10.1016/j.scitotenv.2016.01.153
  12. Briassoulis D, Hiskakis M, Babou E. 2013. Technical specifications for mechanical recycling of agricultural plastic waste. Waste Manag. 33: 1516-1530. 
  13. Yenice MK, Dogruparmak SC, Durmusoglu E, Ozbay B, Oz HO. 2011. Solid waste characterization of Kocaeli. Pol. J. Environ. Stud. 20: 479-484. 
  14. Zeng Y, Trauth KM, Peyton RL, Banerji SK. 2005. Characterization of solid waste disposed at Columbia Sanitary Landfill in Missouri. Waste Manag. Res. 23: 62-71.  https://doi.org/10.1177/0734242X05050995
  15. Gajendiran A, Krishnamoorthy S, Abraham J. 2016. Microbial degradation of low-density polyethylene (LDPE) by Aspergillus clavatus strain JASK1 isolated from landfill soil. 3 Biotech. 6: 52. 
  16. Pramila R, Ramesh KV. 2011. Biodegradation of low density polyethylene (LDPE) by fungi isolated from municipal landfill area. J. Microbiol. Biotechnol. Res. 1: e136. 
  17. Palmisano AC, Pettigrew CA. 1992. Biodegradability of plastics. BioScience 42: 680-685.  https://doi.org/10.2307/1312174
  18. Park SY, Kim CG. 2019. Biodegradation of micro-polyethylene particles by bacterial colonization of a mixed microbial consortium isolated from a landfill site. Chemosphere 222: 527-533.  https://doi.org/10.1016/j.chemosphere.2019.01.159
  19. Zettler ER, Mincer TJ, Amaral-Zettler LA. 2013. Life in the "plastisphere": Microbial communities on plastic marine debris. Environ. Sci. Technol. 47: 7137-7146.  https://doi.org/10.1021/es401288x
  20. Puglisi E, Romaniello F, Galletti S, Boccaleri E, Frache A, Cocconcelli P. 2019. Selective bacterial colonization processes on polyethylene waste samples in an abandoned landfill site. Sci. Rep-UK 9: 14138. 
  21. MacLean J, Mayanna S, Benning LG, Horn F, Bartholomaus A, Wiesner Y, et al. 2021. The terrestrial plastisphere: diversity and polymer-colonizing potential of plastic-associated microbial communities in soil. Microorganisms 9: 1876. 
  22. Wright RJ, Langille MGI, Walker TR. 2021. Food or just a free ride? A meta-analysis reveals the global diversity of the plastisphere. ISME J. 15: 789-806.  https://doi.org/10.1038/s41396-020-00814-9
  23. Wang C, Wang L, Ok YS, Tsang DCW, Hou D. 2022. Soil plastisphere: exploration methods, influencing factors, and ecological insights. J. Hazard. Mater. 430: 128503. 
  24. Sandt C, Waeytens J, Deniset-Besseau A, Nielsen-Leroux C, Rejasse A. 2021. Use and misuse of FTIR spectroscopy for studying the bio-oxidation of plastics. Spectrochim. Acta A. 258: 119841. 
  25. Herlemann DPR, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000km salinity gradient of the Baltic Sea. ISME J. 5: 1571. 
  26. White T, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, pp. 315-322. In Innis MA, Gelfand DH, Sninski JJ, White TJ (eds.), PCR-protocols a guide to methods and applications, Ed. Academic Press, San Diego 
  27. Illumina. 2013. 16S metagenomic sequencing library preparation protocol: Preparing 16S ribosomal RNA gene amplicons for the Illumina MiSeq system. Part no. 15044223 Rev. B. Journal. 
  28. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.  https://doi.org/10.1093/bioinformatics/btq461
  29. Schloss PD. 2009. A high-throughput DNA sequence aligner for microbial ecology studies. PloS One 4: e8230. 
  30. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. 2009. The ribosomal database project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37: D141-D145.  https://doi.org/10.1093/nar/gkn879
  31. Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22: 5271-5277.  https://doi.org/10.1111/mec.12481
  32. Pruesse E, Peplies J, Glockner FO. 2012. SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.  https://doi.org/10.1093/bioinformatics/bts252
  33. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. 2012. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41: D590-D596.  https://doi.org/10.1093/nar/gks1219
  34. Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26: 1641-1650.  https://doi.org/10.1093/molbev/msp077
  35. Hamady M, Lozupone C, Knight R. 2009. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4: 17-27.  https://doi.org/10.1038/ismej.2009.97
  36. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.  https://doi.org/10.1093/molbev/mst197
  37. Tipton L, Muller CL, Kurtz ZD, Huang L, Kleerup E, Morris A, et al. 2018. Fungi stabilize connectivity in the lung and skin microbial ecosystems. Microbiome 6: 12. 
  38. Kurtz ZD, Muller CL, Miraldi ER, Littman DR, Blaser MJ, Bonneau RA. 2015. Sparse and compositionally robust inference of microbial ecological networks. PLoS Computat. Biol. 11: e1004226. 
  39. Briatte F. 2021. ggnet: functions to plot networkswith ggplot2. 
  40. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31: 814-821.  https://doi.org/10.1038/nbt.2676
  41. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40: D109-114.  https://doi.org/10.1093/nar/gkr988
  42. RStudio Team. 2018. RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. URL http://www.r-studio.com/. Integrated development for R. Rstudio, Boston, MA. 
  43. Gulmine JV, Janissek PR, Heise HM, Akcelrud L. 2002. Polyethylene characterization by FTIR. Polym. Test. 21: 557-563.  https://doi.org/10.1016/S0142-9418(01)00124-6
  44. Chabira SF, Benhorma HA, Hiver JM, Godard O, Poncot M, Royaud I, et al. 2019. Impact of the structural changes on the fracture behavior of naturally weathered low-density polyethylene (LDPE) films. J. Macromol. Sci. B. 58: 400-424.  https://doi.org/10.1080/00222348.2019.1565126
  45. Guadagno L, Naddeo C, Vittoria V, Camino G, Cagnani C. 2001. Chemical and morphologial modifications of irradiated linear low density polyethylene (LLDPE). Polym. Degrad. Stabil. 72: 175-186.  https://doi.org/10.1016/S0141-3910(01)00024-6
  46. Gulmine JV, Janissek PR, Heise HM, Akcelrud L. 2003. Degradation profile of polyethylene after artificial accelerated weathering. Polym. Degrad. Stabil. 79: 385-397.  https://doi.org/10.1016/S0141-3910(02)00338-5
  47. Hamzah M, Khenfouch M, Rjeb A, Sayouri S, Houssaini DS, Darhouri M, et al. 2018. Surface chemistry changes and microstructure evaluation of low density nanocluster polyethylene under natural weathering: A spectroscopic investigation. J. Phys. Conf. Ser. 984: 012010. 
  48. Grause G, Chien MF, Inoue C. 2020. Changes during the weathering of polyolefins. Polym. Degrad. Stabil. 181: 109364. 
  49. Wang X, Cao A, Zhao G, Zhou C, Xu R. 2017. Microbial community structure and diversity in a municipal solid waste landfill. Waste Manag. 66: 79-87. 
  50. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2011. GenBank. Nucleic Acids Res. 39: D32-D37.  https://doi.org/10.1093/nar/gkq1079
  51. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, et al. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67: 1613-1617.  https://doi.org/10.1099/ijsem.0.001755
  52. Busse HJ. 2016. Review of the taxonomy of the genus Arthrobacter, emendation of the genus Arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen. nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov. and Pseudarthrobacter gen. nov., and emended description of Arthrobacter roseus. Int. J. Syst. Evol. Microbiol. 66: 9-37. https://doi.org/10.1099/ijsem.0.000702
  53. Jones D, Keddie RM. 2006. The Genus Arthrobacter, pp. 945-960. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds.), The Prokaryotes: Volume 3: Archaea. Bacteria: Firmicutes, Actinomycetes, Ed. Springer New York, New York, NY. 
  54. Guo X, Xie C, Wang L, Li Q, Wang Y. 2019. Biodegradation of persistent environmental pollutants by Arthrobacter sp. Environ. Sci. Pollut. Res. Int. 26: 8429-8443.  https://doi.org/10.1007/s11356-019-04358-0
  55. Kallimanis A, Kavakiotis K, Perisynakis A, Sproer C, Pukall R, Drainas C, et al. 2009. Arthrobacter phenanthrenivorans sp. nov., to accommodate the phenanthrene-degrading bacterium Arthrobacter sp. strain Sphe3. Int. J. Syst. Evol. Microbiol. 59: 275-279.  https://doi.org/10.1099/ijs.0.000984-0
  56. Abdulrasheed M, Zakaria NN, Ahmad Roslee AF, Shukor MY, Zulkharnain A, Napis S, et al. 2020. Biodegradation of diesel oil by cold-adapted bacterial strains of Arthrobacter spp. from Antarctica. Antarct. Sci. 32: 341-353.  https://doi.org/10.1017/S0954102020000206
  57. Fatima S, Zaman M, Hamid B, Bashir F, Baba ZA, Sheikh TA. 2022. Chapter 4 - Bioremediation of contaminated soils by bacterial biosurfactants, pp. 67-85. In Gupta PK, Yadav B, Himanshu SK (eds.), Advances in Remediation Techniques for Polluted Soils and Groundwater, Ed. Elsevier, Amsterdam, Netherlands. 
  58. Goel R, Zaidi MGH, Soni R, Lata K, Shouche YS. 2008. Implication of Arthrobacter and Enterobacter species for polycarbonate degradation. Int. Biodeter. Biodegr. 61: 167-172.  https://doi.org/10.1016/j.ibiod.2007.07.001
  59. Takehara I, Kato D-I, Takeo M, Negoro S. 2017. Draft genome sequence of the nylon oligomer-degrading bacterium Arthrobacter sp. Strain KI72. Genome Announc. 5: e00217-00217. 
  60. Albertsson AC, Erlandsson B, Hakkarainen M, Karlsson S. 1998. Molecular weight changes and polymeric matrix changes correlated with the formation of degradation products in biodegraded polyethylene. J. Environ. Polym. Degr. 6: 187-195.  https://doi.org/10.1023/A:1021873631162
  61. Han YN, Wei M, Han F, Fang C, Wang D, Zhong YJ, et al. 2020. Greater biofilm formation and increased biodegradation of polyethylene film by a microbial consortium of Arthrobacter sp. and Streptomyces sp. Microorganisms 8: 1979. 
  62. Yi M, Zhou S, Zhang L, Ding S. 2021. The effects of three different microplastics on enzyme activities and microbial communities in soil. Water Enivron. Res. 93: 24-32.  https://doi.org/10.1002/wer.1327
  63. Nowak B, Pajak J, Drozd-Bratkowicz M, Rymarz G. 2011. Microorganisms participating in the biodegradation of modified polyethylene films in different soils under laboratory conditions. Int. Biodeter. Biodegr. 65: 757-767.  https://doi.org/10.1016/j.ibiod.2011.04.007
  64. Hirai H, Takada H, Ogata Y, Yamashita R, Mizukawa K, Saha M, et al. 2011. Organic micropollutants in marine plastics debris from the open ocean and remote and urban beaches. Mar. Pollut. Bull. 62: 1683-1692.  https://doi.org/10.1016/j.marpolbul.2011.06.004
  65. Luo G, Jin T, Zhang H, Peng J, Zuo N, Huang Y, et al. 2022. Deciphering the diversity and functions of plastisphere bacterial communities in plastic-mulching croplands of subtropical China. J. Hazard. Mater. 422: 126865. 
  66. Okurowska K, Karunakaran E, Al-Farttoosy A, Couto N, Pandhal J. 2021. Adapting the algal microbiome for growth on domestic landfill leachate. Bioresour. Technol. 319: 124246. 
  67. Wang P, Song T, Bu J, Zhang Y, Liu J, Zhao J, et al. 2022. Does bacterial community succession within the polyethylene mulching film plastisphere drive biodegradation? Sci. Total Environ. 824: 153884. 
  68. Brinkmann N, Schneider D, Sahner J, Ballauff J, Edy N, Barus H, et al. 2019. Intensive tropical land use massively shifts soil fungal communities. Sci. Rep-UK 9: 3403. 
  69. Orgiazzi A, Lumini E, Nilsson RH, Girlanda M, Vizzini A, Bonfante P, et al. 2012. Unravelling soil fungal communities from different Mediterranean land-use backgrounds. PLoS One 7: e34847. 
  70. Lee JS, Nam B, Lee HB, J. CY. 2018. Molecular phylogeny and morphology reveal the underestimated diversity of Mortierella (Mortierellales) in Korea. Kor. J. Mycol. 46: 375-382. 
  71. De Tender C, Devriese LI, Haegeman A, Maes S, Vangeyte J, Cattrijsse A, et al. 2017. Temporal dynamics of bacterial and fungal colonization on plastic debris in the North Sea. Environ. Sci. Technol. 51: 7350-7360.  https://doi.org/10.1021/acs.est.7b00697
  72. Lacerda ALdF, Proietti MC, Secchi ER, Taylor JD. 2020. Diverse groups of fungi are associated with plastics in the surface waters of the Western South Atlantic and the Antarctic Peninsula. Mol. Ecol. 29: 1903-1918.  https://doi.org/10.1111/mec.15444
  73. Gao B, Yao H, Li Y, Zhu Y. 2021. Microplastic addition alters the microbial community structure and stimulates soil carbon dioxide emissions in vegetable-growing soil. Environ. Toxicol. Chem. 40: 352-365.  https://doi.org/10.1002/etc.4916
  74. Cowan AR, Costanzo CM, Benham R, Loveridge EJ, Moody SC. 2022. Fungal bioremediation of polyethylene: challenges and perspectives. J. Appl. Microbiol. 132: 78-89.  https://doi.org/10.1111/jam.15203
  75. Sanchez C. 2020. Fungal potential for the degradation of petroleum-based polymers: An overview of macro- and microplastics biodegradation. Biotechnol. Adv. 40: 107501. 
  76. Song L, Wang Y, Tang W, Lei Y. 2015. Bacterial community diversity in municipal waste landfill sites. Appl. Microbiol. Biotechnol. 99: 7745-7756.  https://doi.org/10.1007/s00253-015-6633-y
  77. Ye R, Xu S, Wang Q, Fu X, Dai H, Lu W. 2020. Fungal diversity and its mechanism of community shaping in the milieu of sanitary landfill. Front. Environ. Sci. Eng. 15: 77. 
  78. Amaral-Zettler LA, Zettler ER, Mincer TJ. 2020. Ecology of the plastisphere. Nat. Rev. Microbiol. 18: 139-151.  https://doi.org/10.1038/s41579-019-0308-0
  79. Viljakainen VR, Hug LA. 2021. New approaches for the characterization of plastic-associated microbial communities and the discovery of plastic-degrading microorganisms and enzymes. Comput. Struct. Biotechnol. J. 19: 6191-6200.  https://doi.org/10.1016/j.csbj.2021.11.023
  80. Lear G, Kingsbury JM, Franchini S, Gambarini V, Maday SDM, Wallbank JA, et al. 2021. Plastics and the microbiome: impacts and solutions. Environ. Microbiome. 16: 2. 
  81. Sulaiman S, Yamato S, Kanaya E, Kim J-J, Koga Y, Takano K, et al. 2012. Isolation of a novel cutinase homolog with polyethylene terephthalate-degrading activity from leaf-branch compost by using a metagenomic approach. Appl. Environ. Microbiol. 78: 1556-1562. https://doi.org/10.1128/AEM.06725-11