Research article

Discovery of Nylon 11 ingestion by mealworm (Tenebrio molitor) larvae and detection of monomer-degrading bacteria in gut microbiota

  • Received: 28 September 2022 Revised: 18 November 2022 Accepted: 15 December 2022 Published: 26 December 2022
  • Nylon 11, which can be found in many commercial products, is a synthetic plastic that has previously been considered non-biodegradable. Increasing nylon 11 and other plastics in landfills and in the environment pose an environmental concern. Recent studies on plastic biodegradation revealed that initial mechanical fragmentations increase the rate of degradation. In this study, we discovered that the larvae of mealworm (Tenebrio molitor) can masticate nylon 11 film at the rate of 0.25 ± 0.07 mg per fifty larvae per day. The body mass of larvae did not differ from that of starvation control while feeding on nylon 11. Comparison of gut microbiota in nylon-fed and starving larvae showed a shift in composition. There was a significant variation in community composition among the nylon 11-fed experimental groups, suggesting that many organisms are capable of metabolizing nylon 11 fragments and/or possess a growth advantage in a nylon-fed gut environment. We also discovered that a significant fraction of gut microbiome of control larvae is capable of metabolizing nylon 11 monomer (11-aminoundecanoic acid) even in the absence of prior exposure to nylon 11. This is the first study demonstrating ingestion of nylon polymers by invertebrates, and our results suggest the potential of mealworm larvae for nylon 11 biodegradation applications.

    Citation: Amelia Leicht, Jocelyn Gatz-Schrupp, Hisako Masuda. Discovery of Nylon 11 ingestion by mealworm (Tenebrio molitor) larvae and detection of monomer-degrading bacteria in gut microbiota[J]. AIMS Microbiology, 2022, 8(4): 612-623. doi: 10.3934/microbiol.2022039

    Related Papers:

  • Nylon 11, which can be found in many commercial products, is a synthetic plastic that has previously been considered non-biodegradable. Increasing nylon 11 and other plastics in landfills and in the environment pose an environmental concern. Recent studies on plastic biodegradation revealed that initial mechanical fragmentations increase the rate of degradation. In this study, we discovered that the larvae of mealworm (Tenebrio molitor) can masticate nylon 11 film at the rate of 0.25 ± 0.07 mg per fifty larvae per day. The body mass of larvae did not differ from that of starvation control while feeding on nylon 11. Comparison of gut microbiota in nylon-fed and starving larvae showed a shift in composition. There was a significant variation in community composition among the nylon 11-fed experimental groups, suggesting that many organisms are capable of metabolizing nylon 11 fragments and/or possess a growth advantage in a nylon-fed gut environment. We also discovered that a significant fraction of gut microbiome of control larvae is capable of metabolizing nylon 11 monomer (11-aminoundecanoic acid) even in the absence of prior exposure to nylon 11. This is the first study demonstrating ingestion of nylon polymers by invertebrates, and our results suggest the potential of mealworm larvae for nylon 11 biodegradation applications.



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    Acknowledgments



    The work was funded by the Grants-in-Aid from IUK Office of Academic Affairs. Authors also acknowledge the support from the IUK School of Sciences. We thank Dr. Peter Tupa for proofreading of the manuscript.

    Conflict of interest



    The authors declare no conflict of interest.

    Author contributions



    Amelia Leicht, Jocelyn Elpers: Methodology, Investigation, Writing – review. Hisako Masuda: Conceptualization, Methodology, Software, Data curation, Writing – Original draft preparation, Visualization, Investigation, Supervision.

    [1] Arkema. Rilsan® polyamide 11 resins, 2022. Available from: https://hpp.arkema.com/en/product-families/rilsan-polyamide-11-resins/.
    [2] Naughton FC (1974) Production, chemistry, and commercial applications of various chemicals from castor oil. JAOCS 51: 65-71. https://doi.org/10.1007/BF00000015
    [3] Tokiwa Y, Calabia BP, Ugwu CU, et al. (2009) Biodegradability of plastics. Int J Mol Sci 10: 3722-3742. https://doi.org/10.3390/ijms10093722
    [4] Cui X, Li W, Yan D (2005) Investigation of Odd-Odd Nylons Based on Undecanedioic Acid. 2: Crystal Structures. Polym Eng Sci 45: 1673-1679. https://doi.org/10.1002/pen.20378
    [5] Češarek U, Pahovnik D, Žagar E (2020) Chemical recycling of aliphatic polyamides by microwave-assisted hydrolysis for efficient monomer recovery. ACS Sustainable Chem Eng 8: 16274-16282. https://doi.org/10.1021/acssuschemeng.0c05706
    [6] Ali SS, Elsamahy T, Koutra E, et al. (2021) Degradation of conventional plastic wastes in the environment: A review on current status of knowledge and future perspectives of disposal. Sci Total Environ 771: 144719. https://doi.org/10.1016/j.scitotenv.2020.144719
    [7] Shah AA, Hasan F, Hameed A, et al. (2008) Biological degradation of plastics: a comprehensive review. Biotechnol Adv 26: 246-265. https://doi.org/10.1016/j.biotechadv.2007.12.005
    [8] Matjašič T, Simčič T, Medvešček N, et al. (2021) Critical evaluation of biodegradation studies on synthetic plastics through a systematic literature review. Sci Total Environ 752: 141959. https://doi.org/10.1016/j.scitotenv.2020.141959
    [9] Ali SS, Elsamahy T, Al-Tohamy R, et al. (2021) Plastic wastes biodegradation: Mechanisms, challenges and future prospects. Sci Total Environ 780: 146590. https://doi.org/10.1016/j.scitotenv.2021.146590
    [10] Jiang S, Su T, Zhao J, et al. (2021) Biodegradation of polystyrene by tenebrio molitor, galleria mellonella, and zophobas atratus larvae and comparison of their degradation effects. Polymers 13: 3539. https://doi.org/10.3390/polym13203539
    [11] Song Y, Qiu R, Hu J, et al. (2020) Biodegradation and disintegration of expanded polystyrene by land snails Achatina fulica. Sci Total Environ 746: 141289. https://doi.org/10.1016/j.scitotenv.2020.141289
    [12] Sun J, Prabhu A, Aroney STN, et al. (2022) Insights into plastic biodegradation: community composition and functional capabilities of the superworm (Zophobas morio) microbiome in styrofoam feeding trials. Microbial Genomics 8: 000842. https://doi.org/10.1099/mgen.0.000842
    [13] Peng BY, Su Y, Chen Z, et al. (2019) Biodegradation of polystyrene by dark (Tenebrio obscurus) and yellow (Tenebrio molitor) mealworms (Coleoptera: Tenebrionidae). Environ Sci Technol 53: 5256-5265. https://doi.org/10.1021/acs.est.8b06963
    [14] Peng BY, Li Y, Fan R, et al. (2020) Biodegradation of low-density polyethylene and polystyrene in superworms, larvae of Zophobas atratus (Coleoptera: Tenebrionidae): Broad and limited extent depolymerization. Environ Pollut 266: 115206. https://doi.org/10.1016/j.envpol.2020.115206
    [15] Yang Y, Wang J, Xia M (2020) Biodegradation and mineralization of polystyrene by plastic-eating superworms Zophobas atratus. Sci Total Environ 708: 135233. https://doi.org/10.1016/j.scitotenv.2019.135233
    [16] Lou Y, Li Y, Lu B, et al. (2021) Response of the yellow mealworm (Tenebrio molitor) gut microbiome to diet shifts during polystyrene and polyethylene biodegradation. J Hazard Mater 416: 126222. https://doi.org/10.1016/j.jhazmat.2021.126222
    [17] Parenti CC, Binelli A, Caccia S, et al. (2020) Ingestion and effects of polystyrene nanoparticles in the silkworm Bombyx mori. Chemosphere 257: 127203. https://doi.org/10.1016/j.chemosphere.2020.127203
    [18] Woo S, Song I, Cha HJ (2020) Fast and facile biodegradation of polystyrene by the gut microbial flora of plesiophthalmus davidis larvae. Appl Environ Microbiol 86: e01361-e01320. https://doi.org/10.1128/AEM.01361-20
    [19] Cassone BJ, Grove HC, Elebute O, et al. (2020) Role of the intestinal microbiome in low-density polyethylene degradation by caterpillar larvae of the greater wax moth, Galleria mellonella. Proc Biol Sci 287: 20200112. https://doi.org/10.1098/rspb.2020.0112
    [20] Kinoshita S, Kageyama S, Iba K, et al. (1975) Utilization of a cyclic dimer and linear oligomers of ϵ-aminocaproic acid by achrornobacter guttatus KI 72. Agric Biol Chem 39: 1219-1223. https://doi.org/10.1080/00021369.1975.10861757
    [21] Tomita K, Ikeda N, Ueno A (2003) Isolation and characterization of a thermophilic bacterium, Geobacillus thermocatenulatus, degrading nylon 12 and nylon 66. Biotechnol Lett 25: 1743-1746. https://doi.org/10.1023/A:1026091711130
    [22] Negoro S (2000) Biodegradation of nylon oligomers. Appl Microbiol Biotechnol 54: 461-466. https://doi.org/10.1007/s002530000434
    [23] Negoro S, Kato K, Fujiyama K, et al. (1994) The nylon oligomer biodegradation system of Flavobacterium and Pseudomonas. Biodegradation 5: 185-194. https://doi.org/10.1007/BF00696459
    [24] Paredes N, Rodriguez-Galán A, Puiggalí J (1996) Synthesis and structural study of a new biodegradable copolymer of nylon-11 and l-alanine. Polymer 37: 4175-4181. https://doi.org/10.1016/0032-3861(96)00245-5
    [25] Kuo P-C, Sahu D, Yu HH (2006) Properties and biodegradability of chitosan/nylon 11 blending films. Polym Degrad Stabil 91: 3097-3102. https://doi.org/10.1016/j.polymdegradstab.2006.07.025
    [26] Gatz-Schrupp J, Deckard P, Hufford B, et al. (2020) Isolation and genomic analysis of 11-aminoundecanoic acid-degrading bacterium Pseudomonas sp. JG-B from nylon 11 enrichment culture. J Genomics 8: 16-20. https://doi.org/10.7150/jgen.42095
    [27] Hareland WA, Crawford RL, Chapman PJ, et al. (1975) Metabolic function and properties of 4-hydroxyphenylacetic acid 1-hydroxylase from Pseudomonas acidovorans. J Bacteriol 121: 272-285. https://doi.org/10.1128/jb.121.1.272-285.1975
    [28] Whitmire JM, Merrell D (2012) Successful culture techniques for helicobacter species: general culture techniques for helicobacter pylori. Method Mol Biol 921: 17-27. https://doi.org/10.1007/978-1-62703-005-2_4
    [29] Albanese D, Fontana P, De Filippo C, et al. (2015) MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Scientific Reports 5: 9743. https://doi.org/10.1038/srep09743
    [30] Wang Q, Garrity GM, Tiedje JM, et al. (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267. https://doi.org/10.1128/AEM.00062-07
    [31] McMurdie PJ, Holmes S (2013) Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PloS One 8: e61217. https://doi.org/10.1371/journal.pone.0061217
    [32] Oksanen J, Blanchet FG, Friendly M, et al. vegan: Community Ecology Package. R package version 2.5–6., 2019. Available from: https://CRAN.R-project.org/package=vegan.
    [33] Pagès H, Aboyoun P, Gentleman R, et al. (2019) Biostrings: Efficient manipulation of biological strings. R package version 2: 10.18129.
    [34] Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21: 1-20. https://doi.org/10.18637/jss.v021.i12
    [35] Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526-528. https://doi.org/10.1093/bioinformatics/bty633
    [36] Wickham H, Seidel D Scales: scale functions for visualization. R package version 1.1. 1 (2020).
    [37] Kembel SW, Cowan PD, Helmus MR, et al. (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464. https://doi.org/10.1093/bioinformatics/btq166
    [38] Kassambara A Ggpubr: “ggplot2” based publication ready plots (2020).
    [39] Auguie B, Antonov A (2017) GridExtra: miscellaneous functions for "Grid" graphics. R package version 2.3. Computer software . Available from: https://CRAN R-project org/package= gridExtra.
    [40] Wickham H Ggplot2: Elegant Graphics for Data Analysis, 2016. Available from: https://cran.r-project.org/web/packages/ggplot2/index.html.
    [41] Vincent QV Ggbiplot: A ggplot2 based biplot. R package version 0.55., 2011. Available from: http://github.com/vqv/ggbiplot.
    [42] Mor R, Sivan A (2008) Biofilm formation and partial biodegradation of polystyrene by the actinomycete Rhodococcus ruber: biodegradation of polystyrene. Biodegradation 19: 851-858. https://doi.org/10.1007/s10532-008-9188-0
    [43] Yoshida S, Hiraga K, Takehana T, et al. (2016) A bacterium that degrades and assimilates poly(ethylene terephthalate). Science 351: 1196-1199. https://doi.org/10.1126/science.aad6359
    [44] Suyama T, Tokiwa Y, Ouichanpagdee P, et al. (1998) Phylogenetic affiliation of soil bacteria that degrade aliphatic polyesters available commercially as biodegradable plastics. Appl Environ Microbiol 64: 5008-5011. https://doi.org/10.1128/AEM.64.12.5008-5011.1998
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