in

Green manure-induced shifts in nematode communities associated with soil bacterial and fungal biomes


Abstract

Green manures are widely used to enhance soil health and suppress plant-parasitic nematodes, and their effects on the broader soil food web have been studied. Beyond direct suppression, the role of green manures in supporting and sustaining soil food webs has attracted increasing attention. In this study, we evaluated the use of DNA sequencing to identify various nematode genera and their microbial associates in a field trial using oat (Avena sativa) and hairy vetch (Vicia villosa) as green manures. Nematode index analysis revealed that the oat treatment promoted a structured nematode community. Furthermore, the nematode community structure observed in the oat treatment was linked to specific bacterial and fungal genera. Several beneficial fungi were identified, indicating that oats, used as a green manure, actively enhanced the microbiome. Our results showed that enriching the micro-food web through organic fertilizers can help in the detection of beneficial microorganisms, with the nematode index serving as a potential indicator.

Data availability

Sequence data that support the findings of this study have been deposited in the National Center for Biotechnology Information with the BioSample IDs: SAMN48745011, SAMN48745012, and SAMN48745013.

Code availability

Not applicable.

Materials availability

Not applicable.

References

  1. Fageria, N. K. Green manuring in crop production. J. Plant. Nutr. 30 (5), 691–719. https://doi.org/10.1080/01904160701289529 (2007).

    Google Scholar 

  2. Kumar, K. & Goh, K. M. Crop residues and management practices: effects on soil quality, soil nitrogen dynamics, crop yield, and nitrogen recovery. Adv. Agron. 68, 197–319. https://doi.org/10.1016/S0065-2113(08)60846-9 (1999).

    Google Scholar 

  3. Ndiaye, E. L., Sandeno, J. M., McGrath, D. & Dick, R. P. Integrative biological indicators for detecting change in soil quality. Amer J. Altern. Agricul. 15 (1), 26–36 (2000). https://www.jstor.org/stable/44503132

    Google Scholar 

  4. Schutter, M. E. & Dick, R. P. Microbial community profiles and activities among aggregates of winter fallow and cover-cropped soil. Soil. Sci. Soc. Am. J. 66 (1), 142–153. https://doi.org/10.2136/sssaj2002.1420 (2002).

    Google Scholar 

  5. Wang, K. H., Sipes, B. S. & Schmitt, D. P. Crotalaria as a cover crop for nematode management: a review. Nematropica 35–58. (2002).

  6. McSorley, R. Host suitability of potential cover crops for root-knot nematodes. J. Nematol. 31 (4S), 619 (1999).

    Google Scholar 

  7. Djian-Caporalino, C. et al. Evaluating sorghums as green manure against root-knot nematodes. Crop Prot. 122, 142–150. https://doi.org/10.1016/j.cropro.2019.05.002 (2019).

    Google Scholar 

  8. Dutta, T. K., Khan, M. R. & Phani, V. Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: current status and future prospects. Curr. Plant. Biol. 17, 17–32. https://doi.org/10.1016/j.cpb.2019.02.001 (2019).

    Google Scholar 

  9. Lord, J. S., Lazzeri, L., Atkinson, H. J. & Urwin, P. E. Biofumigation for control of pale potato cyst nematodes: activity of brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. J. Agricul Food Chem. 59 (14), 7882–7890. https://doi.org/10.1021/jf200925k (2011).

    Google Scholar 

  10. Sánchez-Moreno, S., Cano, M., López-Pérez, A. & Benayas, J. M. R. Microfaunal soil food webs in mediterranean semi-arid agroecosystems. Does organic management improve soil health? Appl. Soil. Ecol. 125, 138–147. https://doi.org/10.1016/j.apsoil.2017.12.020 (2018).

    Google Scholar 

  11. Li, Y. et al. Organic management practices enhance soil food web biomass and complexity under greenhouse conditions. Appl. Soil. Ecol. 167, 104010. https://doi.org/10.1016/j.apsoil.2021.104010 (2021).

    Google Scholar 

  12. Milkereit, J. et al. Interactions between nitrogen availability, bacterial communities, and nematode indicators of soil food web function in response to organic amendments. Appl. Soil. Ecol. 157, 103767. https://doi.org/10.1016/j.apsoil.2020.103767 (2021).

    Google Scholar 

  13. Bongers, T. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19. https://doi.org/10.1007/BF00324627 (1990).

    Google Scholar 

  14. Ferris, H., Bongers, T. & de Goede, R. G. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl. Soil. Ecol. 18 (1), 13–29. https://doi.org/10.1016/S0929-1393(01)00152-4 (2001).

    Google Scholar 

  15. Yang, B. et al. Impact of land use type and organic farming on the abundance, diversity, community composition and functional properties of soil nematode communities in vegetable farming. Agricul Ecosys Environ. 318, 107488. https://doi.org/10.1016/j.agee.2021.107488 (2021).

    Google Scholar 

  16. Matoute, A. et al. Meat-borne-parasite: A nanopore-based meta-barcoding work-flow for parasitic microbiodiversity assessment in the wild fauna of French Guiana. Curr. Issues Mol. Biol. 46 (5), 3810–3821. https://doi.org/10.3390/cimb46050237 (2024).

    Google Scholar 

  17. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 (D1), D590–D596. https://doi.org/10.1093/nar/gks1219 (2013).

    Google Scholar 

  18. Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584. (2016). https://doi.org/10.7717/peerj.2584 (2016).

  19. Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61 (1), 1–10. https://doi.org/10.1016/0006-3207(92)91201-3 (1992).

    Google Scholar 

  20. Gardes, M. & Bruns, T. D. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol. 2 (2), 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x (1993).

    Google Scholar 

  21. White, T. J., Bruns, T., Lee, S. J. W. T. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: Guide Methods Appl. 18 (1), 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1 (1990).

    Google Scholar 

  22. Bolyen, E. et al. Reproducible, interactive, scalable and extensible Microbiome data science using QIIME 2. Nat. Biotech. 37 (8), 852–857. https://doi.org/10.1038/s41587-019-0252-6 (2019).

    Google Scholar 

  23. Abarenkov, K. et al. The UNITE database for molecular identification and taxonomic communication of fungi and other eukaryotes: sequences, taxa and classifications reconsidered. Nucleic Acids Res. 5 (D1), D791–D797. https://doi.org/10.1093/nar/gkad1039 (2024).

    Google Scholar 

  24. Sapkota, R. & Nicolaisen, M. High-throughput sequencing of nematode communities from total soil DNA extractions. BMC Ecol. 15, 1–8. https://doi.org/10.1186/s12898-014-0034-4 (2015).

    Google Scholar 

  25. Porazinska, D. L. et al. Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol. Ecol. Resource. 9 (6), 1439–1450. https://doi.org/10.1111/j.1755-0998.2009.02611.x (2009).

    Google Scholar 

  26. Baker, H. V. et al. A new taxonomic database for analysis of nematode community data. Phytobiomes J. 7 (3), 385–391. https://doi.org/10.1094/PBIOMES-07-22-0042-R (2023).

    Google Scholar 

  27. González, I. & Déjean, S. C. C. A. Canonical Correlation Analysis. R package version 1.2.2, (2023). https://CRAN.R-project.org/package=CCA

  28. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-, 2016).

  29. DeJong, T. M. A comparison of three diversity indices based on their components of richness and evenness. Oikos 222–227. https://doi.org/10.2307/3543712 (1975).

  30. Zhou, X. G. & Everts, K. L. Suppression of fusarium wilt of watermelon enhanced by hairy Vetch green manure and partial cultivar resistance. Plant. Health Progress. 7 (1), 23. https://doi.org/10.1094/PHP-2006-0405-01-RS (2006). (2006).

    Google Scholar 

  31. Martin, T. & Sprunger, C. D. Soil food web structure and function in annual row-crop systems: how can nematode communities infer soil health? Appl. Soil. Ecol. 178, 104553. https://doi.org/10.1016/j.apsoil.2022.104553 (2022).

    Google Scholar 

  32. Wang, K. H. et al. Relationships between soil tillage systems, nematode communities and weed seed predation. Horticulturae 8 (5), 425. https://doi.org/10.3390/horticulturae8050425 (2022).

    Google Scholar 

  33. Ferris, H. & Benavides, I. V. Opinions and suggestions on nematode faunal analysis. J. Nematol. 56 (1), 20240049. https://doi.org/10.2478/jofnem-2024-0049 (2024).

    Google Scholar 

  34. Zhou, D. et al. Rhizosphere microbiomes from root knot nematode non-infested plants suppress nematode infection. Microb. Ecol. 78 (2), 470–481. https://doi.org/10.1007/s00248-019-01319-5 (2019).

    Google Scholar 

  35. Topalović, O., Hussain, M. & Heuer, H. Plants and associated soil microbiota cooperatively suppress plant-parasitic nematodes. Front. Microbiol. 11, 313. https://doi.org/10.3389/fmicb.2020.00313 (2020).

    Google Scholar 

  36. Khan, S. A. et al. Plant growth promotion and Penicillium citrinum. BMC microbiol. 8, 231. https://doi.org/10.1186/1471-2180-8-231 (2008).

    Google Scholar 

  37. Radhakrishnan, R., Kang, S. M., Baek, I. Y. & Lee, I. J. Characterization of plant growth-promoting traits of Penicillium species against the effects of high soil salinity and root disease. J. Plant. Interact. 9 (1), 754–762. https://doi.org/10.1080/17429145.2014.930524 (2014).

    Google Scholar 

  38. Daroodi, Z., Taheri, P. & Tarighi, S. Acrophialophora jodhpurensis: an endophytic plant growth promoting fungus with biocontrol effect against Alternaria alternata. Front. Plant. Sci. 13, 984583. https://doi.org/10.3389/fpls.2022.984583 (2022).

    Google Scholar 

Download references

Acknowledgements

We thank the former students in our laboratory (Tanioka K., Sawada H., Senoo Y., Nezu Y., Ueda K., Hayashi D., Matsumoto R., Iwamoto N., Tanaka T., Hashimoto T., Hashimoto M., Onishi F., Sato A., Watanabe R. and Yoshimoto T.) for their dedicated efforts in both fieldwork and laboratory work, particularly in handling soil samples. We are grateful to Dr. Wang, KH. at the University of Hawaii for critical reading of this manuscript. This research was supported by a grant (2021-2022) from the Research Institute for Food and Agriculture, Ryukoku University.

Funding

This research was supported by a grant (2021–2022) from the Research Institute for Food and Agriculture, Ryukoku University.

Author information

Authors and Affiliations

Authors

Contributions

E.A. conceived the conception of this study, performed analyses, wrote the manuscript. A.S. and D.Y. performed field practices, acquired data. H.D. and S.S. designed the methodology and interpreted the results. All authors read and approved the manuscript.

Corresponding author

Correspondence to
Erika Asamizu.

Ethics declarations

Ethical approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

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.

Supplementary Material 1

Supplementary Material 2

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Cite this article

Sudo, A., Yoshimura, D., Daimon, H. et al. Green manure-induced shifts in nematode communities associated with soil bacterial and fungal biomes.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-31442-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-025-31442-y

Keywords

  • Green manure
  • Nematode index
  • Oat (Avena sativa)
  • rRNA amplicon sequence
  • Soil bacteria
  • Soil fungi


Source: Ecology - nature.com

Breeding male mole-rats (Fukomys) use strong bites to defend reproductive monopoly

Interplay between climate and childhood mixing can explain a sudden shift in RSV seasonality in Japan

Back to Top