Sustainable Marine Structures

Knowledge and Opportunities from the Plastisphere: A Prelude for the Search of Plastic Degrading Bacteria on Coastal Environments

Luis Felipe Avilés-Ramírez

Faculty of Sciences, National Autonomous University of Mexico (UNAM), Yucatán, Mexico

Joanna M. Ortiz-Alcantara

Laboratory of Ecogenomic Studies, Faculty of Sciences, National Autonomous University of Mexico (UNAM), Yucatán, Mexico

Ma. Leticia Arena-Ortiz

Laboratory of Ecogenomic Studies, Faculty of Sciences, National Autonomous University of Mexico (UNAM), Yucatán, Mexico

DOI: https://doi.org/10.36956/sms.v3i2.432

---

Abstract

Plastic pollution has become an urgent issue, since its invasion to every ecosystem has led to multiple impacts on the environment and human populations. Certain microbial strains and genera had shown the ability to biodegrade plastic sources under laboratory conditions. In this minireview, we collect and analyze scientific papers and reports of this microbial activity as we contextualize this information on the global plastic pollution problem, to provide an updated state of the art of plastic biodegradation with microbial agents. Along with a broad understanding of the general process of plastic biodegradation hosted by microorganisms. The contributions of this minireview come from the identification of research gaps, as well as proposals for new approaches. One of the main proposals focuses on coastal environments and in particular coastal wetlands as a great microbiome source with potential for plastic biodegradation, whether reported or undiscovered. Our final proposal consists of the application of this knowledge into technologic tools and strategies that have a remarkable impact on the battle against the plastic pollution problem.

Keywords: Plastic biodegradation; Bacteria; Plastisphere; Bioremediation; Coastal environments

---

References

[1] Cristán-Frías, A., Ize-Lema, I. and Gavilán-García, A. (2003) La situación de los envases de plástico en México Gaceta Ecológica, núm. 69, octubre-diciembre, 2003, pp. 67-82. Secretaría de Medio Ambiente y Recursos Naturales, Distrito Federal, México.

[2] North, E.J. and Halden, R.U. (2013) Plastics and Environmental Health: The Road Ahead. Rev Environ Health 28: 1-8. DOI: http://dx.doi.org/10.1515/reveh-2012-0030.

[3] Rojo-Nieto, E. and Montoto, T. (2017) “Basuras marinas, plásticos y microplásticos: orígenes, impactos y consecuencias de una amenaza global” Ecologistas en Acción ISBN:978-84-946151-9-1.

[4] NOAA. (2018) Plastic Fact Sheet. URL https://marinedebris.noaa.gov/sites/default/files/2018_Plastics_Fact_Sheet.pdf.

[5] Barrett, J., Chase, Z., Zhang, J., Banaszak-Holl, M.M., Willis, K., Williams, A., Hardesty, B.D. and Wilcox, C. (2020) Microplastic pollution in deep-sea sediments from the Great Australian Bight. Front Mar Sci 7: 808. DOI: http://dx.doi.org/10.3389/fmars.2020.576170.

[6] Napper, I.E., Davies, B.F.R., Clifford, H., Elvin, S., Koldewey, H.J., Mayewski, P. A., Miner, K. R., Potocki M., Elmore, A.C., Gajurel, A.P., Thompson, R.C. (2020) Reaching New Heights in Plastic Pollution—Preliminary Findings of Microplastics on Mount Everest. One Earth 3:621-630. DOI: http://dx.doi.org/10.1016/j.oneear.2020.10.020.

[7] Ragusa A., Svelato A., Santacroce C., Catalano P., Notarstefano V., Carnevali O., Papa F., Rongioletti M. C.A., Baiocco F., Draghi S., D'Amore E., Rinaldo D., Matta M., and Giorgini E. (2020) Plasticenta: First evidence of microplastics in human placenta. Environ Int 146: 106274. DOI: http://dx.doi.org/10.1016/j.envint.2020.106274.

[8] ONU Ambiente (2018) El Estado de los Plásticos: Perspectiva del Día Mundial del Medio Ambiente 2018. URL https://www.unenvironment.org/es/resources/informe/el-estado-de-los-plasticos-perspectiva-del-dia-mundial-del-medio-ambiente-2018.

[9] INEGI, (2010) Bases de datos Promedio diario de residuos sólidos urbanos recolectados por municipio y delegación. Promedio diario de residuos sólidos urbanos recolectados según método de obtención del dato por entidad federativa URL https://www.inegi.org.mx/temas/residuos/default.html#Tabulados.

[10] SEMARNAT (2012) Informe de la Situación del Medio Ambiente en México, Capítulo 7. Residuos.URL http://biblioteca.semarnat.gob.mx/janium/Documentos/Ciga/Libros2013/CD001623.pdf.

[11] Van Sebille, E., England, M. H., and Froyland, G. (2012) Origin, dynamics and evolution of ocean garbage patches from observed surface drifters. Environ Res Lett 7: 044040.

[12] Rios, L.M., Jones, P.R., Moore, C., and Narayan, U.V. (2010) Quantitation of persistent organic pollutants adsorbed on plastic debris from the Northern Pacific Gyre’s “eastern garbage patch”. Journal of Environ Monit 12: 2226-2236.

[13] Derraik, J.G.B. (2002) The pollution of the marine environment by plastic debris: a review. Mar Pollut Bull 44:842-852.

[14] Van Cauwenberghe, L., & Janssen C.R. (2014) Microplastics in bivalves cultured for human consumption. Environmental Pollution, Volume 193, Pages 65-70, ISSN 0269-7491. https://doi.org/10.1016/j.envpol.2014.06.010.

[15] Bennett, D., Bellinger, D. C., Birnbaum, L. S., Hertz-Picciotto, I. et al. (2016) Project TENDR: Targeting Environmental Neuro-Developmental Risks the TENDR Consensus Statement. URL https://ehp.niehs.nih.gov/doi/full/10.1289/ehp358.

[16] Constanza, R., d'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O'Neill, R. V., Paruelo, J., Raskin, R. G., Sutton, P, Van-den, B. M. (1998) The value of the world's ecosystem services and natural capital. Ecol Econom 25: 3-15.

[17] Schwartz, M. W., Bringham, C., Hoeksema, J. D., Lyons, K. G., Mills, M.H. and van Mantgem, P.J. (2000) Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 122: 297 -305.

[18] de Groot, R. S., Wilson Matthew A. and Boumans Roelof M.J. (2002) A typology for the classification, description and valuation of ecosystem functions,goods and services. Ecol Econom 41: 393-408. DOI: http://dx.doi.org/10.1016/S0921-8009(02)00089-7.

[19] Barbier, E., Hacker, S., Kennedy, C., Koch, E., Stier, A., Silliman, B. (2011). The Value of Estuarine and Coastal Ecosystem Services. Ecological Monographs. 81. DOI: http://dx.doi.org/10.1890/10-1510.1.

[20] Liu, X., Ashforth E., Ren, B., Song, F., Dai, H., Liu, M., Wang, J., Xie, Q. and Zhang, L., (2010) Bioprospecting microbial natural product libraries from the marine environment for drug discovery. J Antibiot 63: 415-422. DOI: 10.1038/ja.2010.56.

[21] Maron, P. A., Ranjard, L., Mougel, C. and Lemanceau, P. (2007) Metaproteomics: A New Approach for Studying Functional Microbial Ecology. Microb Ecol 53: 486-493. https://doi.org/10.1007/s00248-006-9196-8.

[22] Obradors N. and Aguilar J. (1991) Efficient Biodegradation of High-Molecular-Weight Polyethylene Glycols by Pure Cultures of Pseudomonas stutzeri. Appl Environ Microbiol 57: 2383-2388.

[23] Pometto III, A. L., Lee, B., and Johnson, K. E. (1991) Production of an Extracellular Polyethylene-Degrading Enzyme(s) by Streptomyces Species. Appl Environ Microbiol 58:731-733.

[24] Muñoz-Inostroza, S.C. (2014) Degradación de polímeros de interés industrial utilizando una mezcla de Pseudomonas aeruginosa, Cladosporium sp y Alternaria sp. (Tesis para título profesional de Tecnólogo Médico) Universidad Santo Tomás Tecnología Médica.

[25] Abou-Zeid, D.M., Müller, R.J., Deckwer, W.D. (2001) Degradation of natural and synthetic polyesters under anaerobic conditions. J Biotechnol 86:113-126.

[26] Uribe, D., Giraldo, D., Gutiérrez and Merino, F. (2010) Biodegradation of low-density polyethylene by the action of a microbial consortium isolated from a landfill, Lima, Peru. Rev Peru Biol 17: 133 - 136.

[27] Kim, M.Y., Kim, C., Moon, J., Heo, J., Jung, S.P., and Kim, J.R. (2016) Polymer Film-Based Screening and Isolation of Polylactic Acid (PLA)-Degrading Microorganisms. J Microbiol Biotechnol 27: 342-349. DOI: http://dx.doi.org/10.4014/jmb.1610.10015.

[28] Akbar, S., Hasan, F., Nadhman, A., Khan, S., Shah, A.A. (2013) Production and Purification of Poly(3-hydroxybutyrate-co-3-hydroxyvalerate) Degrading Enzyme from Streptomyces sp. AF-111. J Polym Environ 21: 1109-1116. DOI: http://dx.doi.org/10.1007/s10924-013-0600-4.

[29] Shah, A.A., Hasan, F., Akhter, J.I., Hameed, A. and Ahmed, S. (2008) Degradation of polyurethane by novel bacterial consortium isolated from soil. Ann Microbiol 58: 381. DOI: http://dx.doi.org/10.1007/BF03175532

[30] Yoshida, S., Hiraga, K., Takehana, T., Yamaji, I., Hironao, Y., Maeda, Y., Toyohara, K., Miyamoto, K., Kimura, Y., and Oda, K. (2016) A bacterium that degrades and assimilates poly(ethylene terephthalate). Science 351: 1196-1199. DOI: http://dx.doi.org/10.1126/science.aad6359

[31] Gutiérrez-Pescador, J.G. (2013) Biodegradación de polietileno de baja densidad por consorcios microbianos. (Tesis de Licenciatura). Universidad Nacional Autónoma de México, México. Retrieved from https://repositorio.unam.mx/contenidos/404040.

[32] Nakajima-Kambe, T., Onuma, F., Kimpara, N., Nakahara, T., (1995) Isolation and characterization of a bacterium which utilizes polyester polyurethane as a sole carbon and nitrogen source. FEMS Microbiol Lett 129: 39-42. DOI: http://dx.doi.org/10.1111/j.1574-6968.1995.tb07554.x.

[33] Uchida, H., Nakajima-Kambe, T., Shigeno-Akutsu, Y., Nomura, N., Tokiwa, Y., Nakahara, T. (2000) Properties of a bacterium which degrades solid poly(tetramethylene succinate)-co-adipate, a biodegradable plastic. FEMS Microbiol Lett 189: 25-29.

[34] Abdullahi, M. and Saidu, B.T. (2013) Biodegradation of polythene and plastic using FADAMA soil amended with organic and inorganic fertilizer. Indian J Sci Res 4: 17-24.

[35] Hadad, D., Geresh, S. and Sivan, A. (2004) Biodegradation of polyethylene by the thermophilic bacterium Brevibacillus borstelensis. J Appl Microbiol 98: 1093-1100. DOI: http://dx.doi.org/10.1111/j.1365-2672.2005.02553.x.

[36] Orr, I. G., Hadar, Y., and Sivan, A. (2004) Colonization, biofilm formation and biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl Microbiol Biotechnol 65: 97-104. DOI: http://dx.doi.org/10.1007/s00253-004-1584-8.

[37] Danko, A.S., Luo, M., Bagwell, Christopher, E., Brigmon, R. L., and Freedman, D.L. (2004) Involvement of Linear Plasmids in Aerobic Biodegradation of Vinyl Chloride. Appl Environ Microbiol 70: 6092-6097. DOI: http://dx.doi.org/10.1128/AEM.70.10.6092-6097.2004.

[38] Howard, G.T. and Blake, R. C. (1998) Growth of Pseudomonas fluorescens on a polyester-polyurethane and the purification and characterization of a polyurethanase-protease enzyme. Int Biodeterior Biodegrad 42: 213-220.

[39] Kleeberg, I., Hetz, C., Kroppenstedt, R.M., Müller, R.J., and Deckwer, W.D. (1998) Biodegradation of Aliphatic-Aromatic Copolyesters by Thermomonospora fusca and Other Thermophilic Compost Isolates. Appl Environ Microbiol 64: 1731-1735.

[40] Elbanna, K., Lütke-Eversloh, T., Jendrossek, D., Luftmann, H., Steinbüchel, A. (2004) Studies on the biodegradability of polythioester copolymers and homopolymers by polyhydroxyalkanoate (PHA)-degrading bacteria and PHA depolymerases. Arch Microbiol 182: 212-225. DOI: http://dx.doi.org/10.1007/s00203-004-0715-z.

[41] Saad, J.O. (2017) Screening of Plastic Degrading Bacteria from Dumped Soil Area. IOSR J Environ Sci Toxicol Food Technol 11: 93-98. URL: https://www.researchgate.net/publication/317115202_Screening_Of_Plastic_Degrading_Bacteria_from_Dumped_Soil_Area.

[42] Abrusci, C., Pablos, J.L., Corrales, T., López-Marín, J., Marín, I., Catalina, F. (2011) Biodegradation of photo-degraded mulching films based on polyethylenes and stearates of calcium and iron as pro-oxidant additives. Int Biodeterior Biodegradation 65: 451e459. DOI: http://dx.doi.org/10.1016/j.ibiod.2010.10.012.

[43] Fontanella, S., Bonhomme, S., Koutny, M., Husarova, L., Brusson, J. M., Courdavault, J.P., Pitteri, S., Samuel, G., Pichon, G., Lemaire, J., Delort, A.M. (2010) Comparison of the biodegradability of various polyethylene films containing pro-oxidant additives. Polym Degrad Stab 95: 1011e1021. DOI: http://dx.doi.org/10.1016/j.polymdegradstab.2010.03.009.

[44] Sriyapai, P., Chansiri, K. and Sriyapai, T. (2018) Isolation and Characterization of Polyester-Based Plastics-Degrading Bacteria from Compost Soils. Microbiology 87: 290-300. DOI: http://dx.doi.org/10.1134/S0026261718020157.

[45] Teeraphatpornchai, T., Nakajima-Kambe, T., Shigeno-Akutsu, Y., Nakayama, M., Nomura, N., Nakahara, T., Uchiyama H. (2003) Isolation and characterization of a bacterium that degrades various polyester-based biodegradable plastics. Biotechnol Lett 25: 23-28.

[46] Satlewal, A., Soni, R., Zaidi, M., Shouche, Y., Goel, R. (2008) Comparative biodegradation of HDPE and LDPE using an indigenously developed microbial consortium. J Microbiol Biotechnol Mar 18: 477-82. PMID: 18388465.

[47] Kathirensan, K. (2003) Polythene and Plastics-degrading microbes from the mangrove soil. Rev Biol Trop 51: 629-634.

[48] Morohoshi, T., Ogata, K., Okura, T., and Sato, S. (2018) Molecular Characterization of the Bacterial Community in Biofilms for Degradation of Poly(3-Hydroxybutyrate-co-3-Hydroxyhexanoate) Films in Seawater. Microbes Environ 00: 000-000. DOI: http://dx.doi.org/10.1264/jsme2.ME17052.

[49] Sekiguchi, T., Sato, T., Enoki, M., Kanehiro, H., Uematsu, K., and Kato, C. (2010) Isolation and characterization of biodegradable plastic degrading bacteria from deep-sea environments. JAMSTEC Rep Res Dev 11: 33-41. DOI: http://dx.doi.org/10.5918/jamstecr.11.33.

[50] Suyama, T., Tokiwa, Y., Ouichanpagdee, P., Kanagawa, T., and Kamagata, Y. (1998) Phylogenetic Affiliation of Soil Bacteria That Degrade Aliphatic Polyesters Available Commercially as Biodegradable Plastics. Appl Environ Microbiol 64: 5008 - 5011. DOI: http://dx.doi.org/10.1128/AEM.64.12.5008-5011.1998.

[51] Adıgüzel, A.O. (2020) Production and characterization of thermo-, halo- and solvent-stable esterase from Bacillus mojavensis TH309. Biocatal Biotransformation 38: 210-226. DOI: http://dx.doi.org/10.1080/10242422.2020.1715370.

[52] Denaro, R., Aulenta, F., Crisafi, F., Di Pippo, F., Cruz-Viggi, C., Matturro, B., Tomei, P., Smedile, F., Martinelli, A., Di Lisio, V., Venezia, and C., Rossetti S. (2020) Marine hydrocarbon-degrading bacteria breakdown poly(ethylene terephthalate) (PET). Sci Total Environ 749: 141608. DOI: http://dx.doi.org/10.1016/j.scitotenv.2020.141608.

[53] Suzuki, M., Tachibana, Y., Oba, K., Takizawa, R., & Kasuya, K. (2018) Microbial degradation of poly(ε-caprolactone) in a coastal environment. Polym Degrad Stab 149: 1-8. DOI: http://dx.doi.org/10.1016/j.polymdegradstab.2018.01.017.

[54] Xu, X., Wang, S., Gao, F., Li, J., Zheng, L., Sun, C., He, C., Wang, Z., & Qu, L. (2019) Marine microplastic-associated bacterial community succession in response to geography, exposure time, and plastic type in China's coastal seawaters. Mar Pollut Bull 145: 278-286. DOI: http://dx.doi.org/10.1016/j.marpolbul.2019.05.036.

[55] Harrison, J.P., Schratzberger, M., Sapp, M. and Osborn, A.M. (2014) Rapid bacterial colonization of low-density polyethylene microplastics in coastal sediment microcosms. BMC Microbiology 14: 232.

[56] Auta, H. S., Emenike, C. U., Fauziah, S. H. (2017) Screening of Bacillus strains isolated from mangrove ecosystems in Peninsular Malaysia for microplastic degradation. Environ Pollut 231: 1552e1559. DOI: http://dx.doi.org/10.1016/j.envpol.2017.09.043.

[57] Shahnawaz, M., Sangale, M. K. and Ade, A.B. (2016) Rhizosphere of Avicennia marina (Forsk.) Vierh. as a landmark for polythene degrading bacteria. Environ Sci Pollut Res 23: 14621-14635. DOI: http://dx.doi.org/10.1007/s11356-016-6542-3.

[58] Madhusoodanan J. (2019) Do hosts and their microbes evolve as a unit? PNAS 116: 14391-14394. URL http://www.pnas.org/cgi/doi/10.1073/pnas.1908139116.

[59] Cassone, B. J., Grove, H. C., Elebute, O., Villanueva, S. M. P. and LeMoine, C. M. R. (2020) Role of the intestinal microbiome in low-density polyethylene degradation by caterpillar larvae of the greater wax moth, Galleria mellonella. Proc R Soc B 287: 20200112. DOI: http://dx.doi.org/10.1098/rspb.2020.0112.

[60] Peng, B.Y., Su, Y., Chen, Z., Chen, J., Zhou, X., Benbow, M. E., Criddle, C. S., Wu, W.M., and Zhang, Y. (2019) Biodegradation of Polystyrene by Dark (Tenebrio obscurus) and Yellow (Tenebrio molitor) Mealworms (Coleoptera: Tenebrionidae). Environ Sci Technol 53: 5256−5265. DOI: http://dx.doi.org/10.1021/acs.est.8b06963.

[61] Yang, L., Gao, J., Liu, Y., Zhuang, G., Peng, X., Wu, W.M., and Zhuang, X. (2021) Biodegradation of expanded polystyrene and low-density polyethylene foams in larvae of Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae): Broad versus limited extent depolymerization and microbe-dependence versus independence. Chemosphere 262: 127818. DOI: http://dx.doi.org/10.1016/j.chemosphere.2020.127818.

[62] Song, Y., Qiu, R., Hu, J., Li, X., Zhang, X., Chen, Y., Wu, W.M., and He, D. (2020) Biodegradation and disintegration of expanded polystyrene by land snails Achatina fulica. Sci Total Environ 746: 141289. DOI: http://dx.doi.org/10.1016/j.scitotenv.2020.141289.

[63] Woo, S., Song, I., and Cha, H. J. (2020) Fast and Facile Biodegradation of Polystyrene by the Gut Microbial Flora of Plesiophthalmus davidis Larvae. Appl Environ Microbiol 86: e01361-20. DOI: http://dx.doi.org/10.1128/AEM.01361-20.

[64] Huerta-Lwanga, E., Thapa, B., Yang, X., Gertsen, H., Salánki, T., Geissen, V., and Garbeva, P. (2017) Decay of low-density polyethylene by bacteria extracted from earthworm's guts: A potential for soil restoration. Sci Total Environ 624: 753-757.DOI: http://dx.doi.org/10.1016/j.scitotenv.2017.12.144.

[65] Lou, Y., Ekaterina, P., Yang, S. S., Lu, B., Liu, B., Ren, N., Corvini, P. F. X., and Xing, D.(2020) Biodegradation of Polyethylene and Polystyrene by Greater Wax Moth Larvae (Galleria mellonella L.) and the Effect of Co-diet Supplementation on the Core Gut Microbiome. Environ Sci Technol 54: 2821−2831. DOI: http://dx.doi.org/10.1021/acs.est.9b07044.

[66] Lucas, N., Bienaime, C., Belloy, C., Queneudec, M., Silvestre, F., Nava-Saucedo, J.E. (2008) Polymer biodegradation: Mechanisms and estimation techniques. Chemosphere 73: 429-442.

[67] Singh, B., and Sharma, N. (2008) Mechanistic implications of plastic degradation. Polym Degrad Stab 93: 561-584.DOI: http://dx.doi.org/10.1016/j.polymdegradstab.2007.11.008.

[68] Zettler, E. R., Mincer, T., Proskurowski, G., Amaral-Zettler, L. A. (2011) The "Plastisphere": A new and expanding habitat for marine protists. J Phycol 47: pS45-pS45.

[69] Müller, R. J. (2005) Biodegradability of Polymers: Regulations and Methods for Testing. Online, A. Steinbüchel (Ed.). DOI: http://dx.doi.org/10.1002/3527600035.bpola012.

[70] Glaser, J.A. (2019). Biological Degradation of Polymers in the Environment. In Plastics in the Environment. Gomiero, A. IntechOpen.DOI: http://dx.doi.org/10.5772/intechopen.85124.

[71] Savoldelli, J., Tomback, D., Savoldelli, H. (2017) Breaking down polystyrene through the application of a two-step thermal degradation and bacterial method to produce usable byproducts. Waste Management, Volume 60, ISSN 0956-053X.DOI: http://dx.doi.org/10.1016/j.wasman.2016.04.017

[72] Alshehrei, F. (2017) Biodegradation of Synthetic and Natural Plastic by Microorganisms. Appl Environ Microbiol 5: 8-19. https://www.researchgate.net/publication/317115202_Screening_Of_Plastic_Degrading_Bacteria_from_Dumped_Soil_Area.