Vermicomposting Enhances Microbial Detoxification of Sewage Sludge, Enabling Potential Application of the Treated Product in Agroecosystems
Source abstract
Abstract
Vermicomposting offers an eco-friendly solution to managing the sewage sludge generated in wastewater treatment plants. The objective of this study was to investigate the microbial community composition, structure and functionality during the vermicomposting of sewage sludge. We analyzed samples of sewage sludge, earthworm casts and vermicompost by applying high-throughput sequencing 16S and ITS rRNA. Most of the bacterial (95%) and fungal taxa (99%) were eliminated and subsequently replaced by other microbial taxa originating from earthworms. Further changes resulted in a vermicompost with a more diverse bacterial (but not fungal) community. In addition, the earthworm activity led to an increase in bacterial and a decrease in fungal alpha diversity, resulting in greater differences in beta diversity between sewage sludge, casts and vermicompost. We also found that bacterial pathways associated with amino acid and plant hormone biosynthesis and antibiotic synthesis were enriched. Vermicomposting successfully eliminated most of the 10 human bacterial pathogens found in the sewage sludge. Simultaneously, parasitic and pathogenic fungal taxa were removed. Overall, vermicompost derived from sewage sludge is safer for disposal on land than raw sludge, particularly regarding their respective microbial compositions. This indicates that it could potentially be used as a soil organic amendment and fertilizer.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: Composting and Vermicomposting Techniques · Soil Carbon and Nitrogen Dynamics · Anaerobic Digestion and Biogas Production
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Grupo de Ecoloxía Animal (GEA), Universidade de Vigo, E-36310 Vigo, Spain
Funding
Spanish Ministerio de Ciencia e Innovación · Xunta de Galicia · MCIN/AEI and European Union Next Generation_EU
References (62)
Show source-provided references
1. Ecotoxicological aspects and environmental implications of the use of water and sewage treatment sludges10.1007/s13762-023-05338-1 ↗
2. Domínguez, J., Aira, M., Crandall, K.A., and Pérez-Losada, M. (2021). Earthworms drastically change fungal and bacterial communities during vermicomposting of sewage sludge. Sci. Rep., 11.10.1038/s41598-021-95099-z ↗
3. Concentration of the main persistent organic pollutants in sewage sludge in relation to wastewater treatment plant parameters and sludge stabilisation10.1016/j.envpol.2023.122060 ↗
4. Structural Diversity of Organic Contaminants in Sewage Sludge: A Comparison of Sewage Fingerprints from Germany and China10.1007/s43832-021-00004-4 ↗
5. Kumar, S. (2012). Vermicomposting: Composting with earthworms to recycle organic wastes. Management of Organic Waste, InTech.10.5772/1382 ↗
6. A Comprehensive Review of the Fate of Pathogens during Vermicomposting of Organic Wastes10.2134/jeq2017.07.0265 ↗
7. Pathogen Reduction in Septic Tank Sludge through Vermicomposting Using Eisenia Fetida10.1016/j.biortech.2009.12.001 ↗
8. Persistence of Escherichia Coli in Batch and Continuous Vermicomposting Systems10.1016/j.wasman.2016.07.033 ↗
9. Exploring the effects of earthworms on bacterial profiles during vermicomposting process of sewage sludge and cattle dung with high-throughput sequencing10.1007/s11356-018-1520-6 ↗
10. Earthworms restructure the distribution of extracellular antibiotics resistance genes of sludge by modifying the structure of extracellular polymeric substances during vermicomposting10.1016/j.jhazmat.2023.131315 ↗
11. Zhu, L., Wu, Z., Chen, J., and Huang, K. (2024). Removal of Antibiotic Resistance Genes in Sewage Sludge Vermicomposting. Occurrence and Behavior of Emerging Contaminants in Organic Wastes and Their Control Strategies, Elsevier.10.1016/B978-0-443-13585-9.00007-0 ↗
12. Bioaccumulation of heavy metals during composting and vermicomposting processes of sewage sludge
13. Influence of earthworms on the behaviour of organic micropollutants in sewage sludge10.1016/j.jclepro.2023.137869 ↗
14. The use of vermicompost in organic farming: Overview, effects on soil and economics10.1002/jsfa.6849 ↗
15. Potential of Vermicompost for Sustainable Crop Production and Soil Health Improvement in Different Cropping Systems10.20546/ijcmas.2018.710.116 ↗
16. Investigating organic molecules responsible of auxin-like activity of humic acid fraction extracted from vermicompost10.1016/j.scitotenv.2016.03.212 ↗
17. Valorization of fecal sludge stabilization via vermicomposting in microcosm enriched substrates using organic soils for vermicompost production10.1016/j.heliyon.2021.e06422 ↗
18. Vuković, A., Velki, M., Ečimović, S., Vuković, R., Štolfa Čamagajevac, I., and Lončarić, Z. (2021). Vermicomposting—Facts, Benefits and Knowledge Gaps. Agronomy, 11.10.3390/agronomy11101952 ↗
19. How do earthworms affect the pathway of sludge bio-stabilization via vermicomposting?10.1016/j.scitotenv.2024.170411 ↗
20. Metabarcoding Analysis of the Bacterial Succession during Vermicomposting of Municipal Solid Waste Employing the Earthworm Eisenia fetida10.1016/j.scitotenv.2020.144389 ↗
21. Elimination of Antibiotic-Resistant Bacteria and Resistance Genes by Earthworms during Vermifiltration Treatment of Excess Sludge10.1007/s11356-023-31287-w ↗
22. Zhang, H., Li, J., Zhang, Y., and Huang, K. (2020). Quality of Vermicompost and Microbial Community Diversity Affected by the Contrasting Temperature during Vermicomposting of Dewatered Sludge. Int. J. Environ. Res. Public Health, 17.10.3390/ijerph17051748 ↗
23. Pilot-scale vermicomposting of sewage sludge mixed with mature vermicompost using earthworm reactor of frame composite structure10.1016/j.scitotenv.2020.144217 ↗
24. Vermicomposting Preferably Alters Fungal Communities in Wasted Activated Sludge and Promotes the Production of Plant Growth-Promoting Biostimulants in the Vermicompost10.1016/j.cej.2024.153232 ↗
25. DADA2: High-Resolution Sample Inference from Illumina Amplicon Data10.1038/nmeth.3869 ↗
26. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis10.1038/ismej.2017.119 ↗
27. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools10.1093/nar/gks1219 ↗
28. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy10.1128/AEM.00062-07 ↗
29. Updating the 97% Identity Threshold for 16S Ribosomal RNA OTUs10.1093/bioinformatics/bty113 ↗
30. Bartlett, A., Padfield, D., Lear, L., Bendall, R., and Vos, M. (2022). A Comprehensive List of Bacterial Pathogens Infecting Humans. Microbiology, 168.10.1099/mic.0.001269 ↗
31. McMurdie, P.J., and Holmes, S. (2013). Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE, 8.10.1371/journal.pone.0061217 ↗
32. Welcome to the Tidyverse10.21105/joss.01686 ↗
33. Neuwirth, E. (2024, March 18). R Color Brewer: Color Brewer Palettes 2022. Available online: https://cran.r-project.org/web/packages/RColorBrewer/RColorBrewer.pdf.
34. Pedersen, T.L. (2024, March 18). Patchwork: The Composer of Plots 2024. Available online: https://cran.r-project.org/web/packages/patchwork/patchwork.pdf.
35. Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Solymos, P., Stevens, M.H.H., and Szoecs, E. (2024, March 18). Vegan: Community Ecology Package 2022. Available online: https://www.researchgate.net/publication/360782912_vegan_community_ecology_package_version_26-2_April_2022.
36. Dendextend: An R package for visualizing, adjusting and comparing trees of hierarchical clustering10.1093/bioinformatics/btv428 ↗
37. Complex heatmap visualization10.1002/imt2.43 ↗
38. (2024, March 18). R Core Team R: A Language and Environment for Statistical Computing 2023. Available online: https://www.R-project.org/.
39. Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15.10.1186/s13059-014-0550-8 ↗
40. Conservation evaluation and phylogenetic diversity10.1016/0006-3207(92)91201-3 ↗
41. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities10.1128/AEM.01996-06 ↗
42. Douglas, G.M., Maffei, V.J., Zaneveld, J., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C., and Langille, M.G.I. (2019). PICRUSt2: An improved and extensible approach for metagenome inference. BioRxiv.10.1101/672295 ↗
43. Rosado, D., Lores, M., Ramos-Tapia, I., Crandall, K.A., Pérez-Losada, M., and Domínguez, J. (2022). Integrated Fertilization with Bagasse Vermicompost Changes the Microbiome of Mencía Must and Wine. Fermentation, 8.10.3390/fermentation8080357 ↗
44. Grapevine treatment with bagasse vermicompost changes the microbiome of Albariño must and wine and improves wine quality10.20870/oeno-one.2022.56.3.5560 ↗
45. Douglas, G.M., Kim, S., Langille, M.G.I., and Shapiro, B.J. (2023). Efficient computation of contributional diversity metrics from microbiome data with FuncDiv. Bioinformatics, 39.10.1093/bioinformatics/btac809 ↗
46. Tenenbaum, D. (2024, June 03). KEGGREST: Client-Side REST Access to the Kyoto Encyclopedia of Genes and Genomes (KEGG). R Package Version 1.44.0. Available online: https://bioconductor.org/packages/release/bioc/html/KEGGREST.html.
47. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild10.1016/j.funeco.2015.06.006 ↗
48. Bacterial succession and functional diversity during vermicomposting of the white grape marc Vitis vinifera v10.1038/s41598-019-43907-y ↗
49. Gómez Brandón, M., Aira, M., Kolbe, A.R., de Andrade, N., Pérez-Losada, M., and Domínguez, J. (2019). Rapid Bacterial Community Changes during Vermicomposting of Grape Marc Derived from Red Winemaking. Microorganisms, 7.10.3390/microorganisms7100473 ↗
50. Gómez-Brandón, M., Aira, M., Santana, N., Pérez-Losada, M., and Domínguez, J. (2020). Temporal Dynamics of Bacterial Communities in a Pilot-Scale Vermireactor Fed with Distilled Grape Marc. Microorganisms, 8.10.3390/microorganisms8050642 ↗
51. Domínguez, J., Aira, M., Kolbe, A.R., Gómez-Brandón, M., and Pérez-Losada, M. (2019). Changes in the composition and function of bacterial communities during vermicomposting may explain beneficial properties of vermicompost. Sci. Rep., 9.10.1038/s41598-019-46018-w ↗
52. Rosado, D., Pérez-Losada, M., Aira, M., and Domínguez, J. (2021). Bacterial Succession during Vermicomposting of Silver Wattle (Acacia dealbata Link). Microorganisms, 10.10.3390/microorganisms10010065 ↗
53. Yang, J., Huang, K., Peng, L., Li, J., and Liu, A. (2021). Fate of Functional Bacterial and Eukaryotic Community Regulated by Earthworms during Vermicomposting of Dewatered Sludge, Studies Based on the 16S rDNA and 18S rDNA Sequencing of Active Cells. Int. J. Environ. Res. Public Health, 18.10.3390/ijerph18189713 ↗
54. Using FAME profiles for the characterization of animal wastes and vermicomposts10.1016/j.soilbio.2006.05.001 ↗
55. (2024, August 29). Commission Decision (EU) 2022/1244 of 13 July 2022 Establishing the EU Ecolabel Criteria for Growing Media and Soil Improvers (Notified under Document C(2022) 4758) (Text with EEA Relevance), Available online: https://www.isprambiente.gov.it/it/attivita/certificazioni/files/ecolabel/criteri/ammendanti/eur-lex-32022d1244-en-eur-lex.pdf.
56. (2024, August 29). Directive (EU) 2015/2366 of the European Parliament and of the Council of 25 November 2015 on Payment Services in the Internal Market, Amending Directives 2002/65/EC, 2009/110/EC and 2013/36/EU and Regulation (EU) No 1093/2010, and Repealing Directive 2007/64/EC (Text with EEA Relevance). Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32015L2366.
57. Gut digestion of earthworms significantly attenuates cell-free and -associated antibiotic resistance genes in excess activated sludge by affecting bacterial profiles10.1016/j.scitotenv.2019.07.177 ↗
58. Huang, K., Xia, H., Zhang, Y., Li, J., Cui, G., Li, F., Bai, W., Jiang, Y., and Wu, N. (2020). Elimination of antibiotic resistance genes and human pathogenic bacteria by earthworms during vermicomposting of dewatered sludge by metagenomic analysis. Bioresour. Technol., 297.10.1016/j.biortech.2019.122451 ↗
59. A Novel Strategy for Eliminating Antibiotic Resistance Genes during Fertilization of Dewatered Sludge by Earthworms: Vermicomposting Practice Using Chinese Herbal Residues Derived from Lianhua Qingwen as a Bulking Material10.1016/j.jenvman.2023.119444 ↗
60. Effects of earthworms on the fate of tetracycline and fluoroquinolone resistance genes of sewage sludge during vermicomposting10.1016/j.biortech.2018.03.021 ↗
61. Effects of tetracycline residuals on humification, microbial profile and antibiotic resistance genes during vermicomposting of dewatered sludge10.1016/j.envpol.2019.06.048 ↗
62. Functional characteristics and influence factors of microbial community in sewage sludge composting with inorganic bulking agent10.1016/j.biortech.2017.10.034 ↗