PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

 

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ISSN 1511-3701

Home / Regular Issue / JTAS Vol. 46 (2) May. 2023 / JTAS-2578-2022

 

Biodegradation of Expanded and Extruded Polystyrene with Different Diets by Using Zophobas atratus Larvae (Coleoptera: Tenebrionidae)

Jun Hoe Tay, Norhayu Asib, Nor Azwady Abd Aziz and Geok Hun Tan

Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 2, May 2023

DOI: https://doi.org/10.47836/pjtas.46.2.06

Keywords: Biodegradation, expanded polystyrene, extruded polystyrene, superworms, supplements, Zophobas atratus

Published on: 16 May 2023

Polystyrene waste pollutes the environment and poses a significant health risk to humans, animals, and marine ecology. This study aims to evaluate the effectiveness of degradation on expanded (EPS) and extruded (XPS) polystyrene with different diets using superworms (Zophobas atratus larvae) obtained in Malaysia. The growth and development of the larvae after consumption of EPS and XPS and the gut microbial community changes in response to high polystyrene consumption diets were also identified. The oatmeal, wheat bran, and cornmeal were used as supplement diets and showed significantly enhanced EPS and XPS consumption and degradation compared to sole diet treatment. Gel permeation chromatography was carried out using egested frass of Z.atratus larvae to characterize depolymerization of EPS and XPS, indicating a significant reduction in the average molecular weight and average molecular weight. The highest reduction occurred in the presence of oatmeal. Proton nuclear magnetic resonance and Fourier transform infrared spectroscopy analyses indicated functional group changes and chemical modification occurred with depolymerization and partial oxidation of EPS and XPS. The larvae length increased, while the number of instars and duration of larvae became shorter with the addition of supplement diets. Oatmeal is predominantly effective among other supplements in assisting Z.atratus larvae with EPS and XPS degradation. The results of this study support the ubiquity of polystyrene biodegradation in Z.atratus and the next-generation sequencing studies. Kluyvera sp., Klebsiella sp., and Enterobacter sp. were found to be strongly associated with degrading EPS and XPS polystyrene with oatmeal as a supplemental diet.

  • Brandon, A. M., Gao, S. H., Tian, R., Ning, D., Yang, S. S., Zhou, J., Wu, W. M., & Criddle, C. S. (2018). Biodegradation of polyethylene and plastic mixtures in mealworms (larvae of Tenebrio molitor) and effects on the gut microbiome. Environmental Science and Technology, 52(11), 6526-6533. https://doi.org/10.1021/acs.est.8b02301

  • Chojnacka, K., Mikula, K., Izydorczyk, G., Skrzypczak, D., Witek-Krowiak, A., Gersz, A., Moustakas., K., & Korczyński, M. (2021). Innovative high digestibility protein feed materials reducing environmental impact through improved nitrogen-use efficiency in sustainable agriculture. Journal of Environmental Management, 291, 112693. https://doi.org/10.1016/j.jenvman.2021.112693

  • Emaleku, S. A., Omueti O. O., & Emaleku, G. O. (2018). Talinum triangulare whole wheat meal fortified with soy flour consumed with Talinum triangulare (gbure) soup glycemic index and the test human subjects’ lipid profiles. Diabetes and Metabolic Syndrome: Clinical Research and Reviews, 12(6), 831-837. https://doi.org/10.1016/j.dsx.2017.08.007

  • Esperk, T., Tammaru, T., & Nylin, S. (2007). Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology, 100(3), 627-645. https://doi.org/10.1603/0022-0493(2007)100[627:ivinol]2.0.co;2

  • Farmer III, J. J. (2015). Kluyvera. In Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Inc. and Bergey’s Manual Trust. https://doi.org/10.1002/9781118960608.gbm01151

  • Fu, K. H., Yeung, C. H., Hung, S. C., & To, C. Y. (2020). Two wrongs could make a right: Food waste compost accelerated polystyrene consumption of Tenebrio molitor. Journal of Emerging Investigators, 3, 1-7.

  • Gao, H. L., Li, H. T., Zhang, L., & Hao, M. J. (2010). Effects of Tenebrio molitor L. larva decomposing polystyrene foam. Advanced Materials Research, 113-116, 1972-1975. https://doi.org/10.4028/www.scientific.net/AMR.113-116.1972

  • Georgakopoulos, A. (2003). Study of low rank Greek coals using FTIR spectroscopy. Energy Sources, 25(10), 995–1005. https://doi.org/10.1080/00908310390232442

  • Hendrichs, J., Pereira, R. & Vreysen, M. J. (Eds.) (2021). Area-wide integrated pest management: Development and field application. CRC Press. https://doi.org/10.1201/9781003169239

  • Herman, V., Takacs, H., Duclairoir, F., Renault, O., Tortai, J. H., & Viala, B. (2015). Core double–shell cobalt/graphene/polystyrene magnetic nanocomposites synthesized by in situ sonochemical polymerization. RSC Advances, 5(63), 51371-51381. https://doi.org/10.1039/C5RA06847A

  • Hu, L., Xia, M., Lin, X., Xu, C., Li, W, Wang, J., Zeng, R., & Song, Y. (2018). Earthworm gut bacteria increase silicon bioavailability and acquisition by maize. Soil Biology and Biochemistry, 125, 215-221. https://doi.org/10.1016/j.soilbio.2018.07.015

  • Jang, S., & Kikuchi, Y. (2020). Impact of the insect gut microbiota on ecology, evolution, and industry. Current Opinion in Insect Science, 41, 33-39. https://doi.org/10.1016/j.cois.2020.06.004

  • Jiang, S., Su, T., Zhao, J., & Wang, Z. (2021). Biodegradation of polystyrene by Tenebrio molitor, Galleria mellonella, and Zophobas atratus larvae and comparison of their degradation effects. Polymers, 13(20), 3539. https://doi.org/10.3390/polym13203539

  • Kaleka, A. S., Kaur, N., & Bali, G. P. (2019). Larval development and molting. In H. Mikkola (Ed.), Edible insects. IntechOpen. https://doi.org/10.5772/intechopen.85530

  • Khoo, K. S., Ho, L. Y., Lim, H. R., Leong, H. Y., & Chew, K. W. (2021). Plastic waste associated with the COVID-19 pandemic: Crisis or opportunity?. Journal of Hazardous Materials, 417, 126108. https://doi.org/10.1016/j.jhazmat.2021.126108

  • Kim, S. Y., Kim, H. G., Song, S. H., & Kim, N. J. (2015). Developmental characteristics of Zophobas atratus (Coleoptera: Tenebrionidae) larvae in different instars. International Journal of Industrial Entomology, 30(2), 45-49. https://doi.org/10.7852/ijie.2015.30.2.45

  • Kissin, Y. V. (1995). Molecular weight distributions of linear polymers: Detailed analysis from GPC data. Journal of Polymer Science Part A: Polymer Chemistry, 33(2), 227-237. https://doi.org/10.1002/pola.1995.080330205

  • Kristek, A., Schär, M. Y., Soycan, G., Alsharif, S., Kuhnle, G. G. C., Walton, G., & Spencer, J. P. E. (2018). The gut microbiota and cardiovascular health benefits: A focus on wholegrain oats. Nutrition Bulletin, 43(4), 358-373. https://doi.org/10.1111/nbu.12354

  • Kundungal, H., Synshiang, K., & Devipriya, S. P. (2021). Biodegradation of polystyrene wastes by a newly reported honey bee pest Uloma sp. larvae: An insight to the ability of polystyrene-fed larvae to complete its life cycle. Environmental Challenges, 4, 100083. https://doi.org/10.1016/j.envc.2021.100083

  • Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C. (2017). Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLOS Biology, 15(4), e2000862. https://doi.org/10.1371/journal.pbio.2000862

  • Lin, H. H., & Liu, H. H. (2021). FTIR analysis of biodegradation of polystyrene by intestinal bacteria isolated from Zophobas morio and Tenebrio molitor. Proceedings of Engineering and Technology Innovation, 17, 50-57. https://doi.org/10.46604/peti.2021.5450

  • Liu, X. (2021). 1H NMR spectra and interpretation (Part I). https://batch.libretexts.org/print/url=https://chem.libretexts.org/Bookshelves/Organic_Chemistry/Organic_Chemistry_I_(Liu)/06%3A_Structural_Identification_of_Organic_Compounds-_IR_and_NMR_Spectroscopy/6.06%3A_H_NMR_Spectra_and_Interpretation_(Part_I).pdf

  • Lopes, F. M., Batista, K. A., Batista, G. L., Mitidieri, S., Bataus, L. A. M., & Fernandes, K. F. (2010). Biodegradation of epoxyconazole and piraclostrobin fungicides by Klebsiella sp. from soil. World Journal of Microbiology and Biotechnology, 26(7), 1155-1161. https://doi.org/10.1007/s11274-009-0283-0

  • Lou, Y., Ekaterina, P., Yang, S., Lu, B., Liu, B.-F., Ren, N., Corvini, P., & 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. Environmental Science and Technology, 54(5), 2821-2831. https://doi.org/10.1021/acs.est.9b07044

  • Lou, Y., Li, Y., Lu, B., Liu, Q., Yang, S. S., Liu, B., Ren, N., Wu, W. M., & Xing, D. (2021). Response of the yellow mealworm (Tenebrio molitor) gut microbiome to diet shifts during polystyrene and polyethylene biodegradation. Journal of Hazardous Materials, 416, 126222. https://doi.org/10.1016/j.jhazmat.2021.126222

  • Machona, O., Chidzwondo, F., & Mangoyi, R. (2022). Tenebrio molitor: Possible source of polystyrene-degrading bacteria. BMC Biotechnology, 22, 2. https://doi.org/10.1186/s12896-021-00733-3

  • Maintinguer, S. I., Lazaro, C. Z., Pachiega, R., Varesche, M. B. A., Sequinel, R., & de Oliveira, J. E. (2017). Hydrogen bioproduction with Enterobacter sp. isolated from brewery wastewater. International Journal of Hydrogen Energy, 42(1), 152-160. https://doi.org/10.1016/j.ijhydene.2016.11.104

  • Matyja, K., Rybak, J., Hanus-Lorenz, B., Wróbel, M., & Rutkowski, R. (2020). Effects of polystyrene diet on Tenebrio molitor larval growth, development and survival: Dynamic Energy Budget (DEB) model analysis. Environmental Pollution, 264, 114740. https://doi.org/10.1016/j.envpol.2020.114740

  • McHargue, J. S. (1920). The cause of deterioration and spoiling of corn and corn meal. Industrial and Engineering Chemistry, 12(3), 257-262. https://doi.org/10.1021/ie50123a019

  • Mlček, J., Adámek, M., Adámková, A., Matyáš, J., Bučková, M., Mrázková, M., Vicha, R., Vychodil, R., Knížková, I., & Volek, Z. (2021). Feed parameters influencing the breeding of mealworms (Tenebrio molitor). Sustainability, 13(23), 12992. https://doi.org/10.3390/su132312992

  • Mohanan, N., Montazer, Z., Sharma, P. K., & Levin, D. B. (2020). Microbial and enzymatic degradation of synthetic plastics. Frontiers in Microbiology, 11, 580709. https://doi.org/10.3389/fmicb.2020.580709

  • Morales-Ramos, J. A., Rojas, M. G., Shapiro-Ilan, D. I., & Tedders, W. L. (2010). Developmental plasticity in Tenebrio molitor (Coleoptera: Tenebrionidae): Analysis of instar variation in number and development time under different diets. Journal of Entomological Science, 45(2), 75-90. https://doi.org/10.18474/0749-8004-45.2.75

  • Onwulata, C. I., Phillips, J. G., Tunick, M. H., Qi, P. X., & Cooke, P. H. (2010). Texturized dairy proteins. Journal of Food Science, 75(2), E100–E109. https://doi.org/10.1111/j.1750-3841.2009.01473.x

  • Oonincx, D. G., van Broekhoven, S., van Huis, A., & van Loon, J. J. A. (2019). Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PLOS One, 14(10), e0222043. https://doi.org/10.1371/journal.pone.0222043

  • Ortiz, J. C., Ruiz, A. T., Morales-Ramos, J. A., Thomas, M., Rojas, M. G., Tomberlin, J. K., Yi, L., Han, R., Giroud, L., & Jullien, R. L. (2016). Insect mass production technologies. In Insects as sustainable food ingredients: Production, processing and food application (pp. 153-201). Academic Press. https://doi.org/10.1016/B978-0-12-802856-8.00006-5

  • Peña-Pascagaza, P. M., López-Ramírez, N. A., & Ballen-Segura, M. A. (2020). Tenebrio molitor and its gut bacteria growth in polystyrene (PS) presence as the sole source carbon. Universitas Scientiarum, 25(1), 37–53. https://doi.org/10.11144/javeriana.sc25-1.tmai

  • Peng, B.-Y., Li, Y., Fan, R., Chen, Z., Chen., J., Brandon, A. M., Criddle, C. C., Zhang, Y., & Wu, W.-M. (2020). Biodegradation of low-density polyethylene and polystyrene in superworms, larvae of Zophobas atratus (Coleoptera: Tenebrionidae): Broad and limited extent depolymerization. Environmental Pollution, 266(Part 1), 115206. https://doi.org/10.1016/j.envpol.2020.115206

  • Peng, B.-Y., Su, Y., Chen, Z., Chen, J., Zhou, X., Benbow, M. E., Criddle, C. C., Wu, W.-M., & Zhang, Y. (2019). Biodegradation of polystyrene by dark (Tenebrio obscurus) and yellow (Tenebrio molitor) mealworms (Coleoptera: Tenebrionidae). Environmental Science and Technology, 53(9), 5256-5265. https://doi.org/10.1021/acs.est.8b06963

  • Peng, B.-Y., Sun, Y., Wu, Z., Chen, J., Shen, Z., Zhou, X., Wu, W.-M., & Zhang, Y. (2022). Biodegradation of polystyrene and low-density polyethylene by Zophobas atratus larvae: Fragmentation into microplastics, gut microbiota shift, and microbial functional enzymes. Journal of Cleaner Production, 367, 132987. https://doi.org/10.1016/j.jclepro.2022.132987

  • Pivato, A. F., Miranda, G. M., Prichula, J., Lima, J. E. A., Ligabue, R. A., Seixas, A., & Trentin, D. S. (2022). Hydrocarbon-based plastics: Progress and perspectives on consumption and biodegradation by insect larvae. Chemosphere, 293, 133600. https://doi.org/10.1016/j.chemosphere.2022.133600

  • Rasane, P., Jha, A., Sabikhi, L., Kumar, A., & Unnikrishnan, V. S. (2015). Nutritional advantages of oats and opportunities for its processing as value added foods - A review. Journal of Food Science and Technology, 52, 662–675. https://doi.org/10.1007/s13197-013-1072-1

  • Rho, M. S., & Lee, K. P. (2022). Behavioural and physiological regulation of protein and carbohydrates in mealworm larvae: A geometric analysis. Journal of Insect Physiology, 136, 104329. https://doi.org/10.1016/j.jinsphys.2021.104329

  • Ribeiro, N., Abelho, M., & Costa, R. (2018). A review of the scientific literature for optimal conditions for mass rearing Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science, 53(4), 434-454. https://doi.org/10.18474/jes17-67.1

  • Rumbos, C. I., & Athanassiou, C. G. (2021). The superworm, Zophobas morio (Coleoptera: Tenebrionidae): A ‘Sleeping Giant’ in nutrient sources. Entomological Society of America, 21(2), 13. https://doi.org/10.1093/jisesa/ieab014

  • Ruschioni, S., Loreto, N., Foligni, R., Mannozzi, C., Raffaelli, N., Zamporlini, F., Pasquini, M., Roncolini, A., Cardinali, F., Osimani, A., Aquilanti, L., Isidoro, N., Riolo, P., & Mozzon, M. (2020). Addition of olive pomace to feeding substrate affects growth performance and nutritional value of mealworm (Tenebrio molitor L.) larvae. Foods, 9(3), 317. https://doi.org/10.3390/foods9030317

  • Saygin, H., & Baysal, A. (2021). Insights into the degradation behavior of submicroplastics by Klebsiella pneumoniae. Journal of Polymers and the Environment, 29(3), 958-966. https://doi.org/10.1007/s10924-020-01929-y

  • Sekhar, V. C., Nampoothiri, K. M., Mohan, A. J., Nimisha, R. N., Thallada, B., & Pandey, A. (2016). Microbial degradation of high impact polystyrene (HIPS), an e-plastic with decabromodiphenyl oxide and antimony trioxide. Journal of Hazardous Materials, 318, 347-354. https://doi.org/10.1016/j.jhazmat.2016.07.008

  • Shanmugam, V., Das, O., Neisiany, R. E., Babu, K., Singh, S., Hedenqvist, M. S., Berto, F., & Ramakrishna, S. (2020). Polymer recycling in additive manufacturing: An opportunity for the circular economy. Materials Circular Economy, 2, 11. https://doi.org/10.1007/s42824-020-00012-0

  • Singh, B., Mal, G., Gautam, S. K., & Mukesh, M. (2019). Insect gut - A treasure of microbes and microbial enzymes. In Advances in Animal Biotechnology (pp. 51-58). Springer. https://doi.org/10.1007/978-3-030-21309-1_5

  • Sun, J., Prabhu, A., Aroney, S., & Rinke, C. (2022). Insights into plastic biodegradation: Community composition and functional capabilities of the superworm (Zophobas morio) microbiome in styrofoam feeding trials. https://www.biorxiv.org/content/10.1101/2022.05.16.492041v1.full

  • Thushari, G. G. N., & Senevirathna, J. D. M. (2020). Plastic pollution in the marine environment. Heliyon, 6(8), e04709. https://doi.org/10.1016/j.heliyon.2020.e04709

  • Turner, A. (2020). Foamed polystyrene in the marine environment: Sources, additives, transport, behavior, and impacts. Environmental Science and Technology, 54(17), 10411-10420. https://doi.org/10.1021/acs.est.0c03221

  • Umamaheswari, S., & Murali, M. (2013). FTIR spectroscopic study of fungal degradation of poly (ethylene terephthalate) and polystyrene foam. Chemical Engineering, 64, 19159-19164.

  • Urbanek, A. K., Rybak, J., Wróbel, M., Leluk, K., & Mirończuk, A. M. (2020). A comprehensive assessment of microbiome diversity in Tenebrio molitor fed with polystyrene waste. Environmental Pollution, 262, 114281. https://doi.org/10.1016/j.envpol.2020.114281

  • Yang, J., Yang, Y., Wu, W. M., Zhao, J., & Jiang, L. (2014). Evidence of polyethylene biodegradation by bacterial strains from the guts of plastic-eating waxworms. Environmental Science and Technology, 48(23), 13776–13784. https://doi.org/10.1021/es504038a

  • Yang, L., Gao, J., Liu, Y., Zhuang, G., Peng, X., Wu, W. M., & 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. https://doi.org/10.1016/j.chemosphere.2020.127818

  • Yang, S.-S., & Wu, W.-M. (2020). Biodegradation of plastics in Tenebrio genus (mealworms). In D. He & Y. Luo (Eds.), Microplastics in terrestrial environments: The handbook of environmental chemistry (Vol. 95, pp. 385-422). Springer. https://doi.org/10.1007/698_2020_457

  • Yang, S.-S., Brandon, A. M., Flanagan, J. C. A., Yang, J., Ning, D., Cai, S.-Y., Fan, H.-Q., Wang, Z.-Y., Ren, J., Eric, B., Ren, N.-Q., Waymouth, R. M., Zhou, J., Criddle, C. S., & Wu, W.-M. (2018). Biodegradation of polystyrene wastes in yellow mealworms (larvae of Tenebrio molitor Linnaeus): Factors affecting biodegradation rates and the ability of polystyrene-fed larvae to complete their life cycle. Chemosphere, 191, 979-989. https://doi.org/10.1016/j.chemosphere.2017.10.117

  • Yang, S.-S., Ding, M.-Q., He, L., Zhang, C.-H., Li, Q.-X., Xing, D.-F., Cao, G.-L., Zhao, L., Ding, J., Ren, N.-Q., & Wu, W.-M. (2021). Biodegradation of polypropylene by yellow mealworms (Tenebrio molitor) and superworms (Zophobas atratus) via gut-microbe-dependent depolymerization. Science of The Total Environment, 756, 144087. https://doi.org/10.1016/j.scitotenv.2020.144087

  • Yang, S.-S., Wu, W.-M., Brandon, A. M., Fan, H.-Q., Receveur, J. P., Li, Y., Wang, Z.-Y., Fan, R., McClellan, R., Gao, S.-H., Ning., D., Philips, D. H., Peng, B.-Y., Wang, H., Cai, S.-Y., Li, P., Cai, W.-W., Ding, L.-Y., Yang, J., … Criddle, C. S. (2018). Ubiquity of polystyrene digestion and biodegradation within yellow mealworms, larvae of Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae). Chemosphere, 212, 262-271. https://doi.org/10.1016/j.chemosphere.2018.08.078

  • Yang, Y., Wang, J., & Xia, M. (2020). Biodegradation and mineralization of polystyrene by plastic-eating superworms Zophobas atratus. Science of the Total Environment, 708, 135233. https://doi.org/10.1016/j.scitotenv.2019.135233

  • Yang, Y., Yang, J., Wu, W.-M., Zhao, J., Song, Y., Gao, L., Yang, R., & Jiang, L. (2015). Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 2. Role of gut microorganisms. Environmental Science Technology, 49(20), 12087-12093. https://doi.org/10.1021/acs.est.5b02663

  • Zhou, D., Chen, J., Wu, J., Yang, J., & Wang, H. (2021). Biodegradation and catalytic-chemical degradation strategies to mitigate microplastic pollution. Sustainable Materials and Technologies, 28, e00251. https://doi.org/10.1016/j.susmat.2021.e00251

  • Zhou, J. Z., Mary, A. B., & James, M. T. (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2), 316-322. https://doi.org/10.1128/aem.62.2.316-322.1996

  • Brandon, A. M., Gao, S. H., Tian, R., Ning, D., Yang, S. S., Zhou, J., Wu, W. M., & Criddle, C. S. (2018). Biodegradation of polyethylene and plastic mixtures in mealworms (larvae of Tenebrio molitor) and effects on the gut microbiome. Environmental Science and Technology, 52(11), 6526-6533. https://doi.org/10.1021/acs.est.8b02301

  • Chojnacka, K., Mikula, K., Izydorczyk, G., Skrzypczak, D., Witek-Krowiak, A., Gersz, A., Moustakas., K., & Korczyński, M. (2021). Innovative high digestibility protein feed materials reducing environmental impact through improved nitrogen-use efficiency in sustainable agriculture. Journal of Environmental Management, 291, 112693. https://doi.org/10.1016/j.jenvman.2021.112693

  • Emaleku, S. A., Omueti O. O., & Emaleku, G. O. (2018). Talinum triangulare whole wheat meal fortified with soy flour consumed with Talinum triangulare (gbure) soup glycemic index and the test human subjects’ lipid profiles. Diabetes and Metabolic Syndrome: Clinical Research and Reviews, 12(6), 831-837. https://doi.org/10.1016/j.dsx.2017.08.007

  • Esperk, T., Tammaru, T., & Nylin, S. (2007). Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology, 100(3), 627-645. https://doi.org/10.1603/0022-0493(2007)100[627:ivinol]2.0.co;2

  • Farmer III, J. J. (2015). Kluyvera. In Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Inc. and Bergey’s Manual Trust. https://doi.org/10.1002/9781118960608.gbm01151

  • Fu, K. H., Yeung, C. H., Hung, S. C., & To, C. Y. (2020). Two wrongs could make a right: Food waste compost accelerated polystyrene consumption of Tenebrio molitor. Journal of Emerging Investigators, 3, 1-7.

  • Gao, H. L., Li, H. T., Zhang, L., & Hao, M. J. (2010). Effects of Tenebrio molitor L. larva decomposing polystyrene foam. Advanced Materials Research, 113-116, 1972-1975. https://doi.org/10.4028/www.scientific.net/AMR.113-116.1972

  • Georgakopoulos, A. (2003). Study of low rank Greek coals using FTIR spectroscopy. Energy Sources, 25(10), 995–1005. https://doi.org/10.1080/00908310390232442

  • Hendrichs, J., Pereira, R. & Vreysen, M. J. (Eds.) (2021). Area-wide integrated pest management: Development and field application. CRC Press. https://doi.org/10.1201/9781003169239

  • Herman, V., Takacs, H., Duclairoir, F., Renault, O., Tortai, J. H., & Viala, B. (2015). Core double–shell cobalt/graphene/polystyrene magnetic nanocomposites synthesized by in situ sonochemical polymerization. RSC Advances, 5(63), 51371-51381. https://doi.org/10.1039/C5RA06847A

  • Hu, L., Xia, M., Lin, X., Xu, C., Li, W, Wang, J., Zeng, R., & Song, Y. (2018). Earthworm gut bacteria increase silicon bioavailability and acquisition by maize. Soil Biology and Biochemistry, 125, 215-221. https://doi.org/10.1016/j.soilbio.2018.07.015

  • Jang, S., & Kikuchi, Y. (2020). Impact of the insect gut microbiota on ecology, evolution, and industry. Current Opinion in Insect Science, 41, 33-39. https://doi.org/10.1016/j.cois.2020.06.004

  • Jiang, S., Su, T., Zhao, J., & Wang, Z. (2021). Biodegradation of polystyrene by Tenebrio molitor, Galleria mellonella, and Zophobas atratus larvae and comparison of their degradation effects. Polymers, 13(20), 3539. https://doi.org/10.3390/polym13203539

  • Kaleka, A. S., Kaur, N., & Bali, G. P. (2019). Larval development and molting. In H. Mikkola (Ed.), Edible insects. IntechOpen. https://doi.org/10.5772/intechopen.85530

  • Khoo, K. S., Ho, L. Y., Lim, H. R., Leong, H. Y., & Chew, K. W. (2021). Plastic waste associated with the COVID-19 pandemic: Crisis or opportunity?. Journal of Hazardous Materials, 417, 126108. https://doi.org/10.1016/j.jhazmat.2021.126108

  • Kim, S. Y., Kim, H. G., Song, S. H., & Kim, N. J. (2015). Developmental characteristics of Zophobas atratus (Coleoptera: Tenebrionidae) larvae in different instars. International Journal of Industrial Entomology, 30(2), 45-49. https://doi.org/10.7852/ijie.2015.30.2.45

  • Kissin, Y. V. (1995). Molecular weight distributions of linear polymers: Detailed analysis from GPC data. Journal of Polymer Science Part A: Polymer Chemistry, 33(2), 227-237. https://doi.org/10.1002/pola.1995.080330205

  • Kristek, A., Schär, M. Y., Soycan, G., Alsharif, S., Kuhnle, G. G. C., Walton, G., & Spencer, J. P. E. (2018). The gut microbiota and cardiovascular health benefits: A focus on wholegrain oats. Nutrition Bulletin, 43(4), 358-373. https://doi.org/10.1111/nbu.12354

  • Kundungal, H., Synshiang, K., & Devipriya, S. P. (2021). Biodegradation of polystyrene wastes by a newly reported honey bee pest Uloma sp. larvae: An insight to the ability of polystyrene-fed larvae to complete its life cycle. Environmental Challenges, 4, 100083. https://doi.org/10.1016/j.envc.2021.100083

  • Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A. P., Fioreze, G. T., Anjos, M., Baltazar, C., Elias, A. P., Itskov, P. M., Piper, M. D. W., & Ribeiro, C. (2017). Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLOS Biology, 15(4), e2000862. https://doi.org/10.1371/journal.pbio.2000862

  • Lin, H. H., & Liu, H. H. (2021). FTIR analysis of biodegradation of polystyrene by intestinal bacteria isolated from Zophobas morio and Tenebrio molitor. Proceedings of Engineering and Technology Innovation, 17, 50-57. https://doi.org/10.46604/peti.2021.5450

  • Liu, X. (2021). 1H NMR spectra and interpretation (Part I). https://batch.libretexts.org/print/url=https://chem.libretexts.org/Bookshelves/Organic_Chemistry/Organic_Chemistry_I_(Liu)/06%3A_Structural_Identification_of_Organic_Compounds-_IR_and_NMR_Spectroscopy/6.06%3A_H_NMR_Spectra_and_Interpretation_(Part_I).pdf

  • Lopes, F. M., Batista, K. A., Batista, G. L., Mitidieri, S., Bataus, L. A. M., & Fernandes, K. F. (2010). Biodegradation of epoxyconazole and piraclostrobin fungicides by Klebsiella sp. from soil. World Journal of Microbiology and Biotechnology, 26(7), 1155-1161. https://doi.org/10.1007/s11274-009-0283-0

  • Lou, Y., Ekaterina, P., Yang, S., Lu, B., Liu, B.-F., Ren, N., Corvini, P., & 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. Environmental Science and Technology, 54(5), 2821-2831. https://doi.org/10.1021/acs.est.9b07044

  • Lou, Y., Li, Y., Lu, B., Liu, Q., Yang, S. S., Liu, B., Ren, N., Wu, W. M., & Xing, D. (2021). Response of the yellow mealworm (Tenebrio molitor) gut microbiome to diet shifts during polystyrene and polyethylene biodegradation. Journal of Hazardous Materials, 416, 126222. https://doi.org/10.1016/j.jhazmat.2021.126222

  • Machona, O., Chidzwondo, F., & Mangoyi, R. (2022). Tenebrio molitor: Possible source of polystyrene-degrading bacteria. BMC Biotechnology, 22, 2. https://doi.org/10.1186/s12896-021-00733-3

  • Maintinguer, S. I., Lazaro, C. Z., Pachiega, R., Varesche, M. B. A., Sequinel, R., & de Oliveira, J. E. (2017). Hydrogen bioproduction with Enterobacter sp. isolated from brewery wastewater. International Journal of Hydrogen Energy, 42(1), 152-160. https://doi.org/10.1016/j.ijhydene.2016.11.104

  • Matyja, K., Rybak, J., Hanus-Lorenz, B., Wróbel, M., & Rutkowski, R. (2020). Effects of polystyrene diet on Tenebrio molitor larval growth, development and survival: Dynamic Energy Budget (DEB) model analysis. Environmental Pollution, 264, 114740. https://doi.org/10.1016/j.envpol.2020.114740

  • McHargue, J. S. (1920). The cause of deterioration and spoiling of corn and corn meal. Industrial and Engineering Chemistry, 12(3), 257-262. https://doi.org/10.1021/ie50123a019

  • Mlček, J., Adámek, M., Adámková, A., Matyáš, J., Bučková, M., Mrázková, M., Vicha, R., Vychodil, R., Knížková, I., & Volek, Z. (2021). Feed parameters influencing the breeding of mealworms (Tenebrio molitor). Sustainability, 13(23), 12992. https://doi.org/10.3390/su132312992

  • Mohanan, N., Montazer, Z., Sharma, P. K., & Levin, D. B. (2020). Microbial and enzymatic degradation of synthetic plastics. Frontiers in Microbiology, 11, 580709. https://doi.org/10.3389/fmicb.2020.580709

  • Morales-Ramos, J. A., Rojas, M. G., Shapiro-Ilan, D. I., & Tedders, W. L. (2010). Developmental plasticity in Tenebrio molitor (Coleoptera: Tenebrionidae): Analysis of instar variation in number and development time under different diets. Journal of Entomological Science, 45(2), 75-90. https://doi.org/10.18474/0749-8004-45.2.75

  • Onwulata, C. I., Phillips, J. G., Tunick, M. H., Qi, P. X., & Cooke, P. H. (2010). Texturized dairy proteins. Journal of Food Science, 75(2), E100–E109. https://doi.org/10.1111/j.1750-3841.2009.01473.x

  • Oonincx, D. G., van Broekhoven, S., van Huis, A., & van Loon, J. J. A. (2019). Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PLOS One, 14(10), e0222043. https://doi.org/10.1371/journal.pone.0222043

  • Ortiz, J. C., Ruiz, A. T., Morales-Ramos, J. A., Thomas, M., Rojas, M. G., Tomberlin, J. K., Yi, L., Han, R., Giroud, L., & Jullien, R. L. (2016). Insect mass production technologies. In Insects as sustainable food ingredients: Production, processing and food application (pp. 153-201). Academic Press. https://doi.org/10.1016/B978-0-12-802856-8.00006-5

  • Peña-Pascagaza, P. M., López-Ramírez, N. A., & Ballen-Segura, M. A. (2020). Tenebrio molitor and its gut bacteria growth in polystyrene (PS) presence as the sole source carbon. Universitas Scientiarum, 25(1), 37–53. https://doi.org/10.11144/javeriana.sc25-1.tmai

  • Peng, B.-Y., Li, Y., Fan, R., Chen, Z., Chen., J., Brandon, A. M., Criddle, C. C., Zhang, Y., & Wu, W.-M. (2020). Biodegradation of low-density polyethylene and polystyrene in superworms, larvae of Zophobas atratus (Coleoptera: Tenebrionidae): Broad and limited extent depolymerization. Environmental Pollution, 266(Part 1), 115206. https://doi.org/10.1016/j.envpol.2020.115206

  • Peng, B.-Y., Su, Y., Chen, Z., Chen, J., Zhou, X., Benbow, M. E., Criddle, C. C., Wu, W.-M., & Zhang, Y. (2019). Biodegradation of polystyrene by dark (Tenebrio obscurus) and yellow (Tenebrio molitor) mealworms (Coleoptera: Tenebrionidae). Environmental Science and Technology, 53(9), 5256-5265. https://doi.org/10.1021/acs.est.8b06963

  • Peng, B.-Y., Sun, Y., Wu, Z., Chen, J., Shen, Z., Zhou, X., Wu, W.-M., & Zhang, Y. (2022). Biodegradation of polystyrene and low-density polyethylene by Zophobas atratus larvae: Fragmentation into microplastics, gut microbiota shift, and microbial functional enzymes. Journal of Cleaner Production, 367, 132987. https://doi.org/10.1016/j.jclepro.2022.132987

  • Pivato, A. F., Miranda, G. M., Prichula, J., Lima, J. E. A., Ligabue, R. A., Seixas, A., & Trentin, D. S. (2022). Hydrocarbon-based plastics: Progress and perspectives on consumption and biodegradation by insect larvae. Chemosphere, 293, 133600. https://doi.org/10.1016/j.chemosphere.2022.133600

  • Rasane, P., Jha, A., Sabikhi, L., Kumar, A., & Unnikrishnan, V. S. (2015). Nutritional advantages of oats and opportunities for its processing as value added foods - A review. Journal of Food Science and Technology, 52, 662–675. https://doi.org/10.1007/s13197-013-1072-1

  • Rho, M. S., & Lee, K. P. (2022). Behavioural and physiological regulation of protein and carbohydrates in mealworm larvae: A geometric analysis. Journal of Insect Physiology, 136, 104329. https://doi.org/10.1016/j.jinsphys.2021.104329

  • Ribeiro, N., Abelho, M., & Costa, R. (2018). A review of the scientific literature for optimal conditions for mass rearing Tenebrio molitor (Coleoptera: Tenebrionidae). Journal of Entomological Science, 53(4), 434-454. https://doi.org/10.18474/jes17-67.1

  • Rumbos, C. I., & Athanassiou, C. G. (2021). The superworm, Zophobas morio (Coleoptera: Tenebrionidae): A ‘Sleeping Giant’ in nutrient sources. Entomological Society of America, 21(2), 13. https://doi.org/10.1093/jisesa/ieab014

  • Ruschioni, S., Loreto, N., Foligni, R., Mannozzi, C., Raffaelli, N., Zamporlini, F., Pasquini, M., Roncolini, A., Cardinali, F., Osimani, A., Aquilanti, L., Isidoro, N., Riolo, P., & Mozzon, M. (2020). Addition of olive pomace to feeding substrate affects growth performance and nutritional value of mealworm (Tenebrio molitor L.) larvae. Foods, 9(3), 317. https://doi.org/10.3390/foods9030317

  • Saygin, H., & Baysal, A. (2021). Insights into the degradation behavior of submicroplastics by Klebsiella pneumoniae. Journal of Polymers and the Environment, 29(3), 958-966. https://doi.org/10.1007/s10924-020-01929-y

  • Sekhar, V. C., Nampoothiri, K. M., Mohan, A. J., Nimisha, R. N., Thallada, B., & Pandey, A. (2016). Microbial degradation of high impact polystyrene (HIPS), an e-plastic with decabromodiphenyl oxide and antimony trioxide. Journal of Hazardous Materials, 318, 347-354. https://doi.org/10.1016/j.jhazmat.2016.07.008

  • Shanmugam, V., Das, O., Neisiany, R. E., Babu, K., Singh, S., Hedenqvist, M. S., Berto, F., & Ramakrishna, S. (2020). Polymer recycling in additive manufacturing: An opportunity for the circular economy. Materials Circular Economy, 2, 11. https://doi.org/10.1007/s42824-020-00012-0

  • Singh, B., Mal, G., Gautam, S. K., & Mukesh, M. (2019). Insect gut - A treasure of microbes and microbial enzymes. In Advances in Animal Biotechnology (pp. 51-58). Springer. https://doi.org/10.1007/978-3-030-21309-1_5

  • Sun, J., Prabhu, A., Aroney, S., & Rinke, C. (2022). Insights into plastic biodegradation: Community composition and functional capabilities of the superworm (Zophobas morio) microbiome in styrofoam feeding trials. https://www.biorxiv.org/content/10.1101/2022.05.16.492041v1.full

  • Thushari, G. G. N., & Senevirathna, J. D. M. (2020). Plastic pollution in the marine environment. Heliyon, 6(8), e04709. https://doi.org/10.1016/j.heliyon.2020.e04709

  • Turner, A. (2020). Foamed polystyrene in the marine environment: Sources, additives, transport, behavior, and impacts. Environmental Science and Technology, 54(17), 10411-10420. https://doi.org/10.1021/acs.est.0c03221

  • Umamaheswari, S., & Murali, M. (2013). FTIR spectroscopic study of fungal degradation of poly (ethylene terephthalate) and polystyrene foam. Chemical Engineering, 64, 19159-19164.

  • Urbanek, A. K., Rybak, J., Wróbel, M., Leluk, K., & Mirończuk, A. M. (2020). A comprehensive assessment of microbiome diversity in Tenebrio molitor fed with polystyrene waste. Environmental Pollution, 262, 114281. https://doi.org/10.1016/j.envpol.2020.114281

  • Yang, J., Yang, Y., Wu, W. M., Zhao, J., & Jiang, L. (2014). Evidence of polyethylene biodegradation by bacterial strains from the guts of plastic-eating waxworms. Environmental Science and Technology, 48(23), 13776–13784. https://doi.org/10.1021/es504038a

  • Yang, L., Gao, J., Liu, Y., Zhuang, G., Peng, X., Wu, W. M., & 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. https://doi.org/10.1016/j.chemosphere.2020.127818

  • Yang, S.-S., & Wu, W.-M. (2020). Biodegradation of plastics in Tenebrio genus (mealworms). In D. He & Y. Luo (Eds.), Microplastics in terrestrial environments: The handbook of environmental chemistry (Vol. 95, pp. 385-422). Springer. https://doi.org/10.1007/698_2020_457

  • Yang, S.-S., Brandon, A. M., Flanagan, J. C. A., Yang, J., Ning, D., Cai, S.-Y., Fan, H.-Q., Wang, Z.-Y., Ren, J., Eric, B., Ren, N.-Q., Waymouth, R. M., Zhou, J., Criddle, C. S., & Wu, W.-M. (2018). Biodegradation of polystyrene wastes in yellow mealworms (larvae of Tenebrio molitor Linnaeus): Factors affecting biodegradation rates and the ability of polystyrene-fed larvae to complete their life cycle. Chemosphere, 191, 979-989. https://doi.org/10.1016/j.chemosphere.2017.10.117

  • Yang, S.-S., Ding, M.-Q., He, L., Zhang, C.-H., Li, Q.-X., Xing, D.-F., Cao, G.-L., Zhao, L., Ding, J., Ren, N.-Q., & Wu, W.-M. (2021). Biodegradation of polypropylene by yellow mealworms (Tenebrio molitor) and superworms (Zophobas atratus) via gut-microbe-dependent depolymerization. Science of The Total Environment, 756, 144087. https://doi.org/10.1016/j.scitotenv.2020.144087

  • Yang, S.-S., Wu, W.-M., Brandon, A. M., Fan, H.-Q., Receveur, J. P., Li, Y., Wang, Z.-Y., Fan, R., McClellan, R., Gao, S.-H., Ning., D., Philips, D. H., Peng, B.-Y., Wang, H., Cai, S.-Y., Li, P., Cai, W.-W., Ding, L.-Y., Yang, J., … Criddle, C. S. (2018). Ubiquity of polystyrene digestion and biodegradation within yellow mealworms, larvae of Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae). Chemosphere, 212, 262-271. https://doi.org/10.1016/j.chemosphere.2018.08.078

  • Yang, Y., Wang, J., & Xia, M. (2020). Biodegradation and mineralization of polystyrene by plastic-eating superworms Zophobas atratus. Science of the Total Environment, 708, 135233. https://doi.org/10.1016/j.scitotenv.2019.135233

  • Yang, Y., Yang, J., Wu, W.-M., Zhao, J., Song, Y., Gao, L., Yang, R., & Jiang, L. (2015). Biodegradation and mineralization of polystyrene by plastic-eating mealworms: Part 2. Role of gut microorganisms. Environmental Science Technology, 49(20), 12087-12093. https://doi.org/10.1021/acs.est.5b02663

  • Zhou, D., Chen, J., Wu, J., Yang, J., & Wang, H. (2021). Biodegradation and catalytic-chemical degradation strategies to mitigate microplastic pollution. Sustainable Materials and Technologies, 28, e00251. https://doi.org/10.1016/j.susmat.2021.e00251

  • Zhou, J. Z., Mary, A. B., & James, M. T. (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2), 316-322. https://doi.org/10.1128/aem.62.2.316-322.1996

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