Abstract
Recent studies describe the role of specific isolated members of insect larval gut microbiota in plastic degradation. However, the effect of plastics on the entire gut microbial community composition and structure is yet unknown. To determine these roles, we studied two insect larvae – Tenebrio molitor degrades polystyrene (PS) and Plodia interpunctella degrades polyethylene (PE). We established two colonies of each species: control (fed oats) and test (fed either PS or PE). After dissecting the larvae to obtain their guts, we extracted, sequenced, and analyzed 16S rRNA through amplicon sequencing. In Plodia interpunctella fed only PE, we find significant increased relative abundance of microbial families Pseudomonaceae, Clostridiaceae and Caulobacteraceae - from 0.15% in the control to ~ 50% in the PE-fed group. In Tenebrio molitor fed only PS, degradation is not associated with significant changes in microbial abundance. We hypothesize that Tenebrio microbiome uses other mechanisms such as protein production and/or cross feeding, retaining the original gut microbial structure and composition during PS degradation. This study showcases the diverse mechanisms used by larval gut microbiota to achieve polyethylene and polystyrene degradation, indicating a variation in the effect of plastic degradation on the gut microbial community of larvae.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Plastics - the facts 2022 • plastics Europe. In: Plastics Europe. https://plasticseurope.org/knowledge-hub/plastics-the-facts-2022/. Accessed 5 Dec 2022
Geyer R, Jambeck JR, Law KL (2017) Production, uses, and fate of all plastics ever made. Sci Adv 3:5. https://doi.org/10.1126/sciadv.1700782
Shah AA, Hasan F, Hameed A, Ahmed S (2008) Biological degradation of plastics: a comprehensive review. Biotechnol Adv 26:246–265. https://doi.org/10.1016/j.biotechadv.2007.12.005
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
Nanda S, Sahu S, Abraham J (2010) Studies on the biodegradation of natural and synthetic polyethylene by Pseudomonas spp. JASEM, 14(2)
Lilja EE, Johnson DR (2016) Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates. ISME J (in Press 1–11. https://doi.org/10.1038/ismej.2015.243
Riudavets J, Salas I, Pons MJ (2007) Damage characteristics produced by insect pests in packaging film. J Stored Prod Res 43:564–570. https://doi.org/10.1016/j.jspr.2007.03.006
Brandon AM, Gao SH, Tian R et al (2018) Biodegradation of Polyethylene and Plastic Mixtures in Mealworms (Larvae of Tenebrio molitor) and Effects on the gut Microbiome. Environ Sci Technol 52:6526–6533. https://doi.org/10.1021/acs.est.8b02301
Yang Y, Yang J, Wu WM et al (2015) Biodegradation and Mineralization of Polystyrene by Plastic-Eating Mealworms: part 2. Role of gut microorganisms. Environ Sci Technol 49:12087–12093. https://doi.org/10.1021/acs.est.5b02663
Bombelli P, Howe CJ, Bertocchini F (2017) Polyethylene bio-degradation by caterpillars of the wax moth Galleria mellonella. Curr Biol 27:R292–R293. https://doi.org/10.1016/j.cub.2017.02.060
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 R Soc B Biol Sci 287:9–11. https://doi.org/10.1098/rspb.2020.0112
Yang J, Yang Y, Wu WM et al (2014) Evidence of polyethylene biodegradation by bacterial strains from the guts of plastic-eating waxworms. Environ Sci Technol 48:13776–13784. https://doi.org/10.1021/es504038a
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
Wang Z, Xin X, Shi X, Zhang Y (2020) A polystyrene-degrading Acinetobacter bacterium isolated from the larvae of Tribolium castaneum. Sci Total Environ 726:138564. https://doi.org/10.1016/j.scitotenv.2020.138564
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
Kannan M, Mubarakali D, Thiyonila B et al (2019) Insect gut as a bioresource for potential enzymes - an unexploited area for industrial biotechnology. Biocatal Agric Biotechnol 18:101010. https://doi.org/10.1016/j.bcab.2019.01.048
Urbanek AK, Rybak J, Wróbel M et al (2020) A comprehensive assessment of microbiome diversity in Tenebrio molitor fed with polystyrene waste. Environ Pollut 262. https://doi.org/10.1016/j.envpol.2020.114281
Wang S, Shi W, Huang Z et al (2022) Complete digestion/biodegradation of polystyrene microplastics by greater wax moth (Galleria mellonella) larvae: direct in vivo evidence, gut microbiota independence, and potential metabolic pathways. J Hazard Mater 423:127213. https://doi.org/10.1016/j.jhazmat.2021.127213
Pivato AF, Miranda GM, Prichula J et al (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
Wang Y, Zhang Y (2015) Investigation of gut-associated bacteria in Tenebrio molitor (Coleoptera: Tenebrionidae) larvae using culture-dependent and DGGE methods. Ann Entomol Soc Am 108:941–949. https://doi.org/10.1093/aesa/sav079
Bolyen E, Rideout JR, Dillon MR et al (2019) Author Correction: Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 (Nature Biotechnology, (2019), 37, 8, (852–857). Nat Biotechnol 37:1091. https://doi.org/10.1038/s41587-019-0252-6
Lappan R, Classon C, Kumar S et al (2019) Meta-taxonomic analysis of prokaryotic and eukaryotic gut flora in stool samples from visceral leishmaniasis cases and endemic controls in Bihar State India. PLoS Negl Trop Dis 13:1–28. https://doi.org/10.1371/journal.pntd.0007444
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) Dada2: high resolution sample inference from Illumina amplicon data. Encycl Med Immunol 13:581–583. https://doi.org/10.1038/nmeth.3869
McDonald D, Clemente JC, Kuczynski J et al (2012) The Biological Observation Matrix (BIOM) format or: how I learned to stop worrying and love the ome-ome. Gigascience 464:1–6. https://doi.org/10.1186/2047-217X-1-7
Johnson M, Zaretskaya I, Raytselis Y et al (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:5–9. https://doi.org/10.1093/nar/gkn201
NCBI Resource Coordinators (2018) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 46:D8–D13. https://doi.org/10.1093/nar/gkx1095
Bokulich NA, Kaehler BD, Rideout JR et al (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:1–17. https://doi.org/10.1186/s40168-018-0470-z
Pedregosa F, Varoquaux G, Gramfort A et al (2011) Scikit-learn: machine learning in Python. J Mach Learn Res 12:2825–2830
Kruskal WH, Wallis WA (1952) Use of Ranks in One-Criterion Variance Analysis author (Kruskal-Wallis Test). J Am Stat Assoc 47:583–621
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1046/j.1442-9993.2001.01070.x
Halko N, Martinsson P-G, Shkolnisky Y, Tygert M (2011) An Algorithm for the principal component analysis of large data sets. Soc Ind Appl Math 33:2580–2594
Vázquez-Baeza Y, Pirrung M, Gonzalez A, Knight R (2013) EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2:2–5. https://doi.org/10.1186/2047-217X-2-16
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Douglas GM, Maffei VJ, Zaneveld JR et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:669–688. https://doi.org/10.1038/s41587-020-0548-6
Brandon AM, Garcia AM, Khlystov NA et al (2021) Enhanced bioavailability and Microbial Biodegradation of Polystyrene in an Enrichment Derived from the gut microbiome of Tenebrio molitor (Mealworm Larvae). Environ Sci Technol 55:2027–2036. https://doi.org/10.1021/acs.est.0c04952
Nandiyanto ABD, Oktiani R, Ragadhita R (2019) How to read and interpret ftir spectroscope of organic material. Indones J Sci Technol 4:97–118. https://doi.org/10.17509/ijost.v4i1.15806
Ebciba C, Gnanamani A (2020) Detailed studies on microbial adhesion and degradation of polystyrene foam wastes (PSFW) for clean environment. Environ Sci Pollut Res 27:44257–44266. https://doi.org/10.1007/s11356-020-10272-7
Bhardwaj H, Gupta R, Tiwari A (2012) Microbial Population Associated With Plastic Degradation. Open Access Sci Reports 1–5. https://doi.org/10.4172/scientificreports.272
Belhaj A, Desnoues N, Elmerich C (2002) Alkane biodegradation in Pseudomonas aeruginosa strains isolated from a polluted zone: identification of alkB and alkb-related genes. Res Microbiol 153(6):339–344
Wright RJ, Gibson MI, Christie-Oleza JA (2018) Artificial selection of microbial communities to enhance degradation of recalcitrant polymers. bioRxiv 474742. https://doi.org/10.1101/474742
Yu Z, Ji Y, Bourg V et al (2020) Chitin- and cellulose-based sustainable barrier materials: a review. Emergent Mater 3:919–936. https://doi.org/10.1007/s42247-020-00147-5
Dang H, Lovell CR (2016) Microbial Surface colonization and Biofilm Development in Marine environments. Microbiol Mol Biol Rev 80:91–138
Yang SS, Wu WM (2020) Biodegradation of Plastics in Tenebrio Genus (Mealworms). In: Handbook of Environmental Chemistry. pp 385–422
van Passel MWJ, Kant R, Zoetendal EG et al (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS ONE 6. https://doi.org/10.1371/journal.pone.0016876
Basili M, Quero GM, Giovannelli D et al (2020) Major role of surrounding Environment in shaping Biofilm Community Composition on Marine Plastic debris. Front Mar Sci 7:1–12. https://doi.org/10.3389/fmars.2020.00262
Lin H, An Y, Hao F et al (2016) Correlations of Fecal Metabonomic and Microbiomic Changes Induced by High-fat Diet in the Pre-Obesity State. Sci Rep 6:1–14. https://doi.org/10.1038/srep21618
Danso D, Chow J, Streita WR (2019) Plastics: Environmental and biotechnological perspectives on microbial degradation. Appl Environ Microbiol 85:1–14. https://doi.org/10.1128/AEM.01095-19
Nguyen AT, Oglesby-Sherrouse AG (2016) Interactions between Pseudomonas aeruginosa and Staphylococcus aureus during co-cultivations and polymicrobial infections. Appl Microbiol Biotechnol 100(14):6141–6148
Zhong Z, Nong W, Xie Y, Hui JHL, Chu LM (2022) Long-term effect of plastic feeding on growth and transcriptomic response of mealworms (Tenebrio molitor L.). Chemosphere 287:132063. https://doi.org/10.1016/j.chemosphere.2021.132063
Acknowledgements
This research received funding from Grants-in-aid awards provided by the Graduate School as well as the student organization Association of Biologists, both at Texas Tech University, Lubbock, TX, USA. The authors would also like to acknowledge Center for Biotechnology and Genomics (CBG) at Texas Tech University and RTL Genomics for their timely sequencing and quick turnaround for all the samples. The authors further acknowledge Dr. Moamen Elmassry whose contributions to data analysis were instrumental to the progress of this research.
Funding
Partial financial support was received as Grants-in-aid awards from student organization Texas Tech University Association of Biologists and the Graduate School at Texas Tech University.
Author information
Authors and Affiliations
Contributions
Authors ASN and DLC conceived and designed the research study. ASN conducted all the experiments. ASN and EO contributed equally towards data analysis. ASN wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethical Statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Competing Interests
The authors have no competing interests to declare that are relevant to the content of this article.
Conflict of Interest
ASN declares that she has no conflict of interest. EO declares that she has no conflict of interest. DLC declares that she has no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Navlekar, A.S., Osuji, E. & Carr, D.L. Gut Microbial Communities in Mealworms and Indianmeal Moth Larvae Respond Differently to Plastic Degradation. J Polym Environ 31, 2434–2447 (2023). https://doi.org/10.1007/s10924-023-02773-6
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10924-023-02773-6