Abstract
Polyethylene has considered as non-degradable for decades, and their degradation through marine bacteria has rarely studied. However, LDPE found a significant source of pollution in the marine environment. In the present study, four bacterial strains capable of biodegradation of LDPE were isolated from the marine environment. These bacterial isolates H-237, H-255, H-256 and H-265 were revealed close similarity with Cobetia sp., Halomonas sp., Exigobacterium sp. and Alcanivorax sp., respectively based on 16S rRNA gene sequencing method. These bacterial isolates were individually incubated for 90 days supplied with LDPE films as a carbon source using the Bushnell-Haas medium. During the biodegradation assay, bacterial isolates were formed the viable biofilm on the LDPE surface, which decreased the thermal stability of the films. At the end of the incubation study, a maximum weight loss of 1.72% of LDPE film was observed by the bacterial isolate H-255. The bacterial attachment on the film changed the physical structure (surface erosion, roughness and degradation) which were confirmed by field emission scanning electron microscopy and atomic force microscopy. The changes in the chemical structure of the LDPE film were analyzed by Attenuated total reflection Fourier-transform infrared spectroscopy (ATR-FTIR). This ATR-FTIR showed the shifting of peaks of C–H stretch and C=C bond stretching and the new peaks formation of C–O and –C=C– bonds in comparison to control LDPE film. Further, biodegradation of LDPE film was also confirmed by remineralization of carbon and enzymatic activities. This study revealed that the active biodegradation of LDPE film by marine bacteria and these bacteria could reduce plastic pollution in the marine environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akutsu Y, Nakajima-Kambe T, Nomura N, Nakahara T (1998) Purification and properties of a polyester polyurethane-degrading enzyme from Comamonas acidovorans TB-35. Appl Environ Microbiol 64:62–67. https://doi.org/10.1128/AEM.64.1.62-67.1998
Albertsson AC, Karlsson S (1990) The influence of biotic and abiotic environments on the degradation of polyethylene. Prog Polym Sci 15:177–192. https://doi.org/10.1016/0079-6700(90)90027-X
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic Press, New York
Amidei R (1997) Marine bacteria: a better cleaner-upper? Calif Agric 51:47–48. https://doi.org/10.3733/ca.v051n04p47
Azam F (1998) Microbial control of oceanic carbon flux: the plot thickens. Science 280(5364):694–696
Balasubramanian V, Natarajan K, Hemambika B, Ramesh N, Sumathi CS, Kottaimuthu R, Kannan VR (2010) High-density polyethylene (HDPE)-degrading potential bacteria from marine ecosystem of Gulf of Mannar, India. Lett Appl Microbiol 51: 205–211. https://doi.org/10.1111/j.1472-765X.2010.02883.x
Banerjee UC, Chisti Y, Moo-Young M (1993) Spectrophotometric determination of mycelial biomass. Biotechnol Tech 7: 313–316. https://doi.org/10.1007/BF00150905
Bonhomme S, Cuer A, Delort AM, Lemaire J, Sancelme M, Scott G (2003) Environmental biodegradation of polyethylene. Polym Degrad Stab 81:441–452. https://doi.org/10.1016/S0141-3910(03)00129-0
Bueno-Ferrer C, Garrigos MC, Jimenez A (2010) Characterization and thermal stability of poly(vinyl chloride) plasticized with epoxidized soybean oil for food packaging. Polym Degrad Stabil 95:2207–2212. https://doi.org/10.1016/j.polymdegradstab.2010.01.027
Castellani F, Esposito A, Stanzione V, Altieri R (2016) Measuring the biodegradability of plastic polymers in olive-mill waste compost with an experimental apparatus. Adv Mater Sci Eng 3(3):64. https://doi.org/10.1155/2016/6909283
Chavant P, Martinie B, Meylheuc T, Bellon-Fontaine MN, Hebraud M (2002) Listeria monocytogenes LO28: Surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl Environ Microbiol 68:728–737. https://doi.org/10.1128/aem.68.2.728-737.2002
Chung WK, King GM (2001) Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen nov sp nov and Cycloclasticus spirillensus sp nov. Appl Environ Microbiol 67:5585–5592. https://doi.org/10.1128/AEM.67.12.5585-5592.2001
Copinet A, Bertrand C, Govindin S, Coma V, Couturier Y (2004) Effects of ultraviolet light (315 nm), temperature and relative humidity on the degradation of polylactic acid plastic films. Chemosphere 55:763–773. https://doi.org/10.1016/j.chemosphere.2003.11.038
Devi RS, Kannan VR, Nivas D, Kannan K, Chandru S, Antony AR (2015) Biodegradation of HDPE by Aspergillus spp. from marine ecosystem of Gulf of Mannar. India Mar Pollut Bull 96:32–40. https://doi.org/10.1016/j.marpolbul.2015.05.050
Esmaeili A, Pourbabaee AA, Alikhani HA, Shabani F, Kumar L (2014) Colonization and biodegradation of photo-oxidized low-density polyethylene (LDPE) by new strains of Aspergillus sp. and Lysinibacillus sp. Bioremediat J 18:213–226. https://doi.org/10.1080/10889868.2014.917269
Fukuzaki H, Yoshida M, Asano M, Kumakura M (1989) Synthesis of copoly (D, L-lactic acid) with relatively low molecular weight and in vitro degradation. Eur Polym J 25:1019–1026. https://doi.org/10.1016/0142-9612(91)90014-2
Gajendiran A, Krishnamoorthy S, Abraham J (2016) Microbial degradation of low-density polyethylene (LDPE) by Aspergillus clavatus strain JASK1 isolated from landfill soil. Biotech 6:52. https://doi.org/10.1007/s13205-016-0394-x
Galkiewicz JP, Kellogg CA (2008) Cross-kingdom amplification using bacteria-specific primers: complications for studies of coral microbial ecology. Appl Environ Microbiol 74:7828–7831. https://doi.org/10.1128/AEM.01303-08
Gouin T, Avalos J, Brunning I, Brzuska K, de Graaf J, Kaumanns J (2015) Use of micro-plastic beads in cosmetic products in Europe and their estimated emissions to the North Sea environment. SOFW-J 141:40–46
Grochowalski AR, Cooper DG, Nicell JA (2007) Effect of surfactants on plasticizer biodegradation by Bacillus subtilis ATCC 6633. Biodegrad 18:283–293. https://doi.org/10.1007/s10532-006-9062-x
Gu JD (2003) Microbiological deterioration and degradation of synthetic polymeric materials: recent research advances. Int Biodeterior Biodegr 52:69–91. https://doi.org/10.1016/S0964-8305(02)00177-4
Hadad D, Geresh S, Sivan A (2005) Biodegradation of polyethylene by the thermophilic bacterium Brevibacillus borstelensis. J Appl Microbiol 98:1093–1100. https://doi.org/10.1111/j.1365-2672.2005.02553.x
Harshvardhan K, Jha B (2013) Biodegradation of low-density polyethylene by marine bacteria from pelagic waters, Arabian Sea, India. Mar Pollut Bull 77:100–106. https://doi.org/10.1016/j.marpolbul.2013.10.025
Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen nov sp. nov. Appl Environ Microbiol 65:251–259
Hopewell J, Dvorak R, Kosior E (2009) Plastics recycling: challenges and opportunities. Philos Trans R Soc Lond B Biol Sci 364:2115–2126. https://doi.org/10.1098/rstb.2008.0311
Ibiene AA, Stanley HO, Immanuel OM (2013) Biodegradation of polyethylene by Bacillus sp. indigenous to the Niger delta mangrove swamp. Niger J Biotechnol 26:68–78
Iiyoshi Y, Tsutsumi Y, Nishida T (1998) Polyethylene degradation by lignin-degrading fungi and manganese peroxidase. J Wood Sci 44:222–229. https://doi.org/10.1007/BF0052196
ISO 14855 (2005). Determination of the ultimate aerobic biodegradability and disintegration of plastic materials under controlled composting conditions-method by analysis of evolved carbon dioxide-Part 1: General Method.
Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryman M, Andrady A, Narayan R, Law KL (2015) Plastic waste inputs from land into the ocean. Sci 347(6223):768–771. https://doi.org/10.1126/science.1260352
Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enzyme Res. https://doi.org/10.4061/2011/805187
Kathiresan K (2003) Polythene and plastics-degrading microbes from the mangrove soil. Rev Biol Trop 51:629–634
Kay MJ, McCabe RW, Morton LHG (1993) Chemical and physical changes occurring in polyester polyurethane during biodegradation. Int Biodeter Biodegr 31:209–225. https://doi.org/10.1016/0964-8305(93)90006-N
Kumar D, Kumar L, Nagar S, Raina C, Parshad R, Gupta VK (2012) Screening, isolation, and production of lipase/esterase producing Bacillus sp. strain DVL2 and its potential evaluation in esterification and resolution reactions. Arch App Sci Res 4:1763–1770
Kumari A, Chaudhary DR, Jha B (2019) Destabilization of polyethylene and polyvinylchloride structure by marine bacterial strain. Environ Sci Pollut Res 26:1507–1516. https://doi.org/10.1007/s11356-018-3465-1
Latha K, Lalithakumari D (2001) Transfer and expression of a hydrocarbon-degrading plasmid pHCL from Pseudomonas putida to marine bacteria. World J Microbiol Biotechnol 17:523–528. https://doi.org/10.1023/A:1011917408368
Leejarkpai T, Suwanmanee U, Rudeekit Y, Mungcharoen T (2011) Biodegradable kinetics of plastics under controlled composting conditions. Waste Manage 31:1153–1161. https://doi.org/10.1016/j.wasman.2010.12.011
Maeda H, Yamagata Y, Abe K, Hasegawa F, Machida M, Ishioka R, Gomi K, Nakajima T (2005) Purification and characterization of a biodegradable plastic-degrading enzyme from Aspergillus oryzae. Appl Microbiol Biotechnol 67:778–788. https://doi.org/10.1007/s00253-004-1853-6
Maquelin K, Kirschner C, Choo-Smith LP, van den Braak N, Endtz HP, Naumann D, Puppels GJ (2002) Identification of medically relevant microorganisms by vibrational spectroscopy. J Microbiol Meth 51:255–271. https://doi.org/10.1016/S0167-7012(02)00127-6
Na-Phatthalung W, Musikavong C, Suttinun O (2019) Degradation of N-nitrosodimethylamine and its amine precursors by cumene-induced Rhodococcus sp. strain L4. Biodegrad 30:375–388. https://doi.org/10.1007/s10532-019-09876-9
Ojha N, Pradhan N, Singh S, Barla A, Shrivastava A, Khatua P, Rai V, Bose S (2017) Evaluation of HDPE and LDPE degradation by fungus, implemented by statistical optimization. Sci Rep 7:39515. https://doi.org/10.1038/srep39515
Orr IG, Hadar Y, Sivan A (2004) Colonization, biofilm formation and biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl Microbiol Biotechnol 65:97–104. https://doi.org/10.1007/s00253-004-1584-8
Osman H, Zakaria MH (2012) Effects of durian seed flour on processing torque, tensile, thermal and biodegradation properties of polypropylene and high density polyethylene composites. Polymer Plast Technol Engg 51:243–250. https://doi.org/10.1080/03602559.2011.625379
Papinutti L, Martínez MJ (2006) Production and characterization of laccase and manganese peroxidase from the ligninolytic fungus Fomes sclerodermeus. J Chem Tech Biotech 81:1064–1070. https://doi.org/10.1002/jctb.1537
Pathak VM (2017) Review on the current status of polymer degradation: a microbial approach. Bioresour Bioprocess 4:15. https://doi.org/10.1186/s40643-017-0145-9
Pradeep S, Faseela P, Josh MKS, Balachandran S, Sudha Devi R, Benjamin S (2013) Fungal biodegradation of phthalate plasticizer in situ. Biodegrad 24:257–267. https://doi.org/10.1007/s10532-012-9584-3
Pramila R, Ramesh KV (2015) Potential biodegradation of low density polyethylene (LDPE) by Acinetobacter baumannii. J Bacteriol Res 7:24–28. https://doi.org/10.5897/JBR2015.0152
Raghul SS, Bhat SG, Chandrasekaran M, Francis V, Thachil ET (2014) Biodegradation of polyvinyl alcohol-low linear density polyethylene-blended plastic film by consortium of marine benthic Vibrios. Int J Environ Sci Technol 11:1827–1834. https://doi.org/10.1007/s13762-013-0335-8
Rejmanova P, Kopecek J, Pohl J, Baudys M, Kostka V (1983) Polymers containing enzymatically degradable bonds 8 degradation of oligopeptide sequences in N-(2-hydroxypropyl) methacrylamide copolymers by bovine spleen cathepsin B. Die Macromol Chem 184:2009–2020. https://doi.org/10.1002/macp.1983.021841006
Ren L, Men L, Zhang Z, Guan F, Tian J, Wang B, Wang J, Zhang Y, Zhang W (2019) Biodegradation of polyethylene by Enterobacter sp D1 from the guts of wax moth Galleria mellonella. Int J Environ Res Public Health 16:1941. https://doi.org/10.3390/ijerph16111941
Sadocco P, Nocerino S, Dubini-Paglia E, Seves A, Elegir G (1997) Characterization of a poly (3-hydroxybutyrate) depolymerase from aureobacterium saperdae: active site and kinetics of hydrolysis studies. J Environ Polym Degrad 5:57. https://doi.org/10.1007/BF02763569
Sanin SZ, Sanin FD, Bryers JD (2003) Effect of starvation on the adhesive properties of xenobiotic degrading bacteria. Process Biochem 38:909–914. https://doi.org/10.1016/S0032-9592(02)00173-5
Santo M, Weitsman R, Sivan A (2013) The role of the copper-binding enzyme laccase in the biodegradation of polyethylene by the actinomycete Rhodococcus ruber. Int Biodeter Biodegr 84:204–210. https://doi.org/10.1016/j.ibiod.2012.03.001
Scheirs J, Kaminsky W (2006) Feedstock recycling and pyrolysis of waste plastics. Wiley, Chichester
Sekhar VC, Nampoothiri KM, Mohan AJ, Nair NR, Bhaskar T, Pandey A (2016) Microbial degradation of high impact polystyrene (HIPS), an e-Plastic with decabromodiphenyl oxide and antimony trioxide. J Hazard Mater 318:347–354. https://doi.org/10.1016/j.jhazmat.2016.07.008
Shah AA, Hasan F, Hameed A, Ahmed S (2007) Isolation and characterization of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) degrading bacteria and purification of PHBV depolymerase from newly isolated Bacillus sp. AF3. Int Biodeterior Biodegr 60:109–115. https://doi.org/10.1016/j.ibiod.2007.01.004
Shah Z, Krumholz L, Aktas DF, Hasan F, Khattak M, Shah AA (2013) Degradation of polyester polyurethane by a newly isolated soil bacterium, Bacillus subtilis strain MZA-75. Biodegrad 24:865–877. https://doi.org/10.1007/s10532-013-9634-5
Shahnawaz M, Sangale MK, Ade AB (2016) Rhizosphere of Avicennia marina (Forsk.) Vierh. as a landmark for polythene degrading bacteria. Environ Sci Pollut Res 23:14621–14635. https://doi.org/10.1007/s11356-016-6542-3
Singh B, Sharma N (2008) Mechanistic implications of plastic degradation. Polym Degrad Stab 93:561–584. https://doi.org/10.1016/j.polymdegradstab.2007.11.008
Sivan A (2011) New perspectives in plastic biodegradation. Curr Opin Biotechnol 22:422–426. https://doi.org/10.1016/j.copbio.2011.01.013
Sivan A, Szanto M, Pavlov V (2006) Biofilm development of the polyethylene-degrading bacterium Rhodococcus ruber. Appl Microbiol Biotechnol 72:346–352. https://doi.org/10.1007/s00253-005-0259-4
Sowmya HV, Ramalingappa KM, Thippeswamy B (2014) Biodegradation of polyethylene by Bacillus cereus. Adv Poly Sci Tech 4:28–32
Starnecker A, Menner M (1996) Assessment of biodegradability of plastics under simulated composting conditions in a laboratory test system. Int Biodeterior Biodegr 37:85–92. https://doi.org/10.1016/0964-8305(95)00089-5
Sudhakar M, Doble M, Murthy PS, Venkatesan R (2008) Marine microbe-mediated biodegradation of low- and high-density polyethylenes. Int Biodeterior Biodegrad 61:203–213. https://doi.org/10.1016/j.ibiod.2007.07.011
Swift G (1998) Requirements for biodegradable water-soluble polymers. Polym Degrad Stab 59:19–24. https://doi.org/10.1016/S0141-3910(97)00162-6
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
Yamada-Onodera K, Mukumoto H, Katsuyaya Y, Saiganji A, Tani Y (2001) Degradation of polyethylene by a fungus, Penicillium simplicissimum YK. Polym Degrad Stab 72:323–327. https://doi.org/10.1016/S0141-3910(01)00027-1
Zheng Y, Yanful EK, Bassi AS (2005) A review of plastic waste biodegradation. Crit Rev Biotechnol 25:243–250. https://doi.org/10.1080/07388550500346359
Acknowledgements
CSIR-CSMCRI Communication No.: 047/2019. The financial support received BARTI as BANRF fellowship to S.D.K. greatly acknowledged. Council of Scientific and Industrial Research (CSIR), New Delhi is also thankfully acknowledged for financial support (CSC0120-Waste to Wealth). Help received from Mr. Chintan B. Gajera is greatfully acknowldeged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Khandare, S.D., Chaudhary, D.R. & Jha, B. Marine bacterial biodegradation of low-density polyethylene (LDPE) plastic. Biodegradation 32, 127–143 (2021). https://doi.org/10.1007/s10532-021-09927-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-021-09927-0