Long-term inorganic fertilizer exposure disturbed functional traits and gut bacterial conditionally rare or abundant taxa in collembolan (Entomobrya proxima Folsom)

Xinyue Yang, Gang Li, Weiming Xiu

Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (3) : 250307.

PDF(5936 KB)
Soil Ecology Letters All Journals
PDF(5936 KB)
Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (3) : 250307. DOI: 10.1007/s42832-025-0307-1

Long-term inorganic fertilizer exposure disturbed functional traits and gut bacterial conditionally rare or abundant taxa in collembolan (Entomobrya proxima Folsom)

Author information +
History +

Highlights

● The inorganic fertilizer addition with a low amount promoted the elongation of some functional traits of Entomobrya proxima .

● The conditionally rare or abundant taxa were more susceptible to the disturbance of inorganic fertilizer than abundant taxa in the gut of Entomobrya proxima .

● Multiple dominant genera in the conditionally rare or abundant taxa have the potential to indicate the changes of functional traits of Entomobrya proxima .

Abstract

The functional traits of soil fauna are closely related to ecosystem functions. The gut microbiota, which can reflect environmental changes, may be associated with functional traits. Therefore, in this study, collembolan (Entomobrya proxima) was used to clarify the linkage response of specific gut taxa and traits under long-term urea exposure. A small amount of urea had positive effects on functional traits of E. proxima. Chao1 and Shannon indices of gut bacteria conditionally rare or abundant taxa (CRAT) gradually decreased under low and medium fertilizer, while increased under high fertilizer. Shannon index of abundant taxa (AT) showed a similar trend to that of CRAT except that the value of Shannon index was higher at high fertilizer than that of medium treatments. The structure and community assembly of CRAT changed significantly, and with the increase of urea addition amount, the dominant mechanism of community assembly changed from a deterministic process to a stochastic process. The niche width of AT and CRAT decreased. Relative abundance of some genera in AT and CRAT was closely related to functional traits. In conclusion, CRAT was more sensitive to urea than AT, had the potential to characterize functional traits of E. proxima, which will provide a basis for predicting the changes of soil animal traits and functions under the change of agricultural fertilizer strategy in the future.

Graphical abstract

Keywords

collembolan / functional traits / intestinal bacterial community / AT / CRAT

Cite this article

Download citation ▾
Xinyue Yang, Gang Li, Weiming Xiu. Long-term inorganic fertilizer exposure disturbed functional traits and gut bacterial conditionally rare or abundant taxa in collembolan (Entomobrya proxima Folsom). Soil Ecology Letters, 2025, 7(3): 250307 https://doi.org/10.1007/s42832-025-0307-1
This is a preview of subscription content, contact us for subscripton.

References

[1]
Adams, H.E., Crump, B.C., Kling, G.W., 2010. Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environmental Microbiology12, 1319–1333.
CrossRef Google scholar
[2]
Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature515, 505–511.
CrossRef Google scholar
[3]
Berg, M., Stenuit, B., Ho, J., Wang, A., Parke, C., Knight, M., Alvarez-Cohen, L., Shapira, M., 2016. Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. The ISME Journal10, 1998–2009.
CrossRef Google scholar
[4]
Bokova, A.I., Panina, K.S., Dridiger, V.K., Gadzhiumarov, R.G., Kuznetsova, N.A., Potapov, M.B., 2023. Soil-dwelling springtails as indicators of the efficiency of no-till technologies with different amounts of mineral fertilizers in the crop rotation on chernozem soils. Soil and Tillage Research232, 105760.
CrossRef Google scholar
[5]
Chao, H.Z., Kong, L.Y., Zhang, H.X., Sun, M.M., Ye, M., Huang, D., Zhang, Z.Y., Sun, D.W., Zhang, S.T., Yuan, Y.L., Liu, M.Q., Hu, F., Jiang, X., 2019. Metaphire guillelmi gut as hospitable micro-environment for the potential transmission of antibiotic resistance genes. Science of the Total Environment669, 353–361.
CrossRef Google scholar
[6]
Chelinho, S., Maleita, C.M.N., Francisco, R., Braga, M.E.M., da Cunha, M.J.M., Abrantes, I., de Sousa, H.C., Morais, P.V., Sousa, J.P., 2017. Toxicity of the bionematicide 1,4-naphthoquinone on non-target soil organisms. Chemosphere181, 579–588.
CrossRef Google scholar
[7]
Dai, T.J., Zhang, Y., Tang, Y.S., Bai, Y.H., Tao, Y.L., Huang, B., Wen, D.H., 2016. Identifying the key taxonomic categories that characterize microbial community diversity using full-scale classification: a case study of microbial communities in the sediments of Hangzhou Bay. FEMS Microbiology Ecology92, fiw150.
CrossRef Google scholar
[8]
de Vries, F.T., Thébault, E., Liiri, M., Birkhofer, K., Tsiafouli, M. A., Bjørnlund, L., Bracht Jørgensen, H., Brady, M.V., Christensen, S., de Ruiter, P.C., d'Hertefeldt, T., Frouz, J., Hedlund, K., Hemerik, L., Hol, W.H.G., Hotes, S., Mortimer, S.R., Setälä, H., Sgardelis, S.P., Uteseny, K., van der Putten, W.H., Wolters, V., Bardgett, R.D., 2013. Soil food web properties explain ecosystem services across European land use systems. Proceedings of the National Academy of Sciences of the United States of America110, 14296–14301.
[9]
Decaëns, T., Jiménez, J.J., Gioia, C., Measey, G.J., Lavelle, P., 2006. The values of soil animals for conservation biology. European Journal of Soil Biology42, S23–S38.
CrossRef Google scholar
[10]
Douglas, A.E., 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annual Review of Entomology60, 17–34.
CrossRef Google scholar
[11]
Du, S.C., Dini-Andreote, F., Zhang, N., Liang, C.L., Yao, Z.Y., Zhang, H.J., Zhang, D.M., 2020. Divergent co-occurrence patterns and assembly processes structure the abundant and rare bacterial communities in a salt marsh ecosystem. Applied and Environmental Microbiology86, e00322–20.
[12]
Duan, H.J., Yin, Y., Wang, Y.F., Liu, Z.L., Cai, T.G., Zhu, D., Chen, C., Duan, G.L., 2025. Effects of reductive soil disinfestation on potential pathogens and antibiotic resistance genes in soil. Journal of Environmental Sciences150, 373–384.
CrossRef Google scholar
[13]
Elshahed, M.S., Youssef, N.H., Spain, A.M., Sheik, C., Najar, F.Z., Sukharnikov, L.O., Roe, B.A., Davis, J.P., Schloss, P.D., Bailey, V.L., Krumholz, L.R., 2008. Novelty and uniqueness patterns of rare members of the soil biosphere. Applied and Environmental Microbiology74, 5422–5428.
CrossRef Google scholar
[14]
Engel, P., Moran, N.A., 2013. The gut microbiota of insects – diversity in structure and function. FEMS Microbiology Reviews37, 699–735.
CrossRef Google scholar
[15]
Fu, B.X., Yu, Y.T., Wei, Y.J., Pan, C.Y., Zhang, D.Y., Zhu, Z.R., 2023. Sensory structures and electrophysiology of termite antennae and the roles in its social behaviors. Acta Entomologica Sinica66, 1638–1648.
[16]
Gilbert, B., Levine, J.M., 2017. Ecological drift and the distribution of species diversity. Proceedings of the Royal Society B: Biological Sciences284, 20170507.
CrossRef Google scholar
[17]
Jin, J.F., Zhao, Y.X., Zhang, G.Q., Pan, Z.X., Zhang, F., 2023. The first chromosome-level genome assembly of Entomobrya proxima Folsom, 1924 (Collembola: Entomobryidae). Scientific Data10, 541.
CrossRef Google scholar
[18]
Joimel, S., Jules, A., Vieublé Gonod, L., 2022. Collembola dispersion, selection, and biological interactions in urban ecosystems: a review. Environmental Chemistry Letters20, 2123–2133.
CrossRef Google scholar
[19]
Jousset, A., Bienhold, C., Chatzinotas, A., Gallien, L., Gobet, A., Kurm, V., Küsel, K., Rillig, M.C., Rivett, D.W., Salles, J.F., van der Heijden, M.G.A., Youssef, N.H., Zhang, X.W., Wei, Z., Hol, W.H.G., 2017. Where less may be more: how the rare biosphere pulls ecosystems strings. The ISME Journal11, 853–862.
CrossRef Google scholar
[20]
Ju, H., Zhu, D., Qiao, M., 2019. Effects of polyethylene microplastics on the gut microbial community, reproduction and avoidance behaviors of the soil springtail, Folsomia candida. Environmental Pollution247, 890–897.
CrossRef Google scholar
[21]
Kong, Y., Zhang, T., Li, G., Yang, D.L., Zhao, J.N., Zhang, G.L., Wang, L.L., Xiu, W.M., 2020. Soil meso-and micro-arthropods community characteristics and stability in maize soil with different fertilization regimes. Journal of Maize Sciences28, 156–162.
[22]
Laliberté, E., Kardol, P., Didham, R.K., Teste, F.P., Turner, B.L., Wardle, D.A., 2017. Soil fertility shapes belowground food webs across a regional climate gradient. Ecology Letters20, 1273–1284.
CrossRef Google scholar
[23]
Lehman, R.M., Cambardella, C.A., Stott, D.E., Acosta-Martinez, V., Manter, D.K., Buyer, J.S., Maul, J.E., Smith, J.L., Collins, H.P., Halvorson, J.J., Kremer, R.J., Lundgren, J.G., Ducey, T.F., Jin, V.L., Karlen, D.L., 2015. Understanding and enhancing soil biological health: the solution for reversing soil degradation. Sustainability7, 988–1027.
CrossRef Google scholar
[24]
Li, S.M., Li, Z., Ke, X., Wisawapipat, W., Christie, P., Wu, L.H., 2024. Cadmium toxicity to and accumulation in a soil collembolan (Folsomia candida): major factors and prediction using a back-propagation neural network model. Environmental Science and Pollution Research31, 23790–23801.
CrossRef Google scholar
[25]
Lynch, M.D.J., Neufeld, J.D., 2015. Ecology and exploration of the rare biosphere. Nature Reviews Microbiology13, 217–229.
CrossRef Google scholar
[26]
Mcgill, B.J., Enquist, B.J., Weiher, E., Westoby, M., 2006. Rebuilding community ecology from functional traits. Trends in Ecology & Evolution21, 178–185.
[27]
Nemergut, D.R., Schmidt, S.K., Fukami, T., O'Neill, S.P., Bilinski, T.M., Stanish, L.F., Knelman, J.E., Darcy, J.L., Lynch, R.C., Wickey, P., Ferrenberg, S., 2013. Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews77, 342–356.
CrossRef Google scholar
[28]
Nolte, V., Pandey, R.V., Jost, S., Medinger, R., Ottenwälder, B., Boenigk, J., Schlötterer, C., 2010. Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Molecular Ecology19, 2908–2915.
CrossRef Google scholar
[29]
OECD, 2016. Test No.232: Collembolan Reproduction Test in Soil. Paris: OECD Publishing.
[30]
Pass, D.A., Morgan, A.J., Read, D.S., Field, D., Weightman, A.J., Kille, P., 2015. The effect of anthropogenic arsenic contamination on the earthworm microbiome. Environmental Microbiology17, 1884–1896.
CrossRef Google scholar
[31]
Pedrós-Alió, C., 2012. The rare bacterial biosphere. Annual Review of Marine Science4, 449–466.
CrossRef Google scholar
[32]
Ren, H.F., Gao, W., Huang, S.W., Zhang, G.G., Tang, J.W., Li, M.Y., Luan, H.A., 2020. Effects of partial substitution of chemical fertilizer with manure and/or straw on soil nematode community in greenhouse vegetable production. Journal of Plant Nutrition and Fertilizers26, 1303–1317.
[33]
Sechi, V., De Goede, R.G.M., Rutgers, M., Brussaard, L., Mulder, C., 2018. Functional diversity in nematode communities across terrestrial ecosystems. Basic and Applied Ecology30, 76–86.
CrossRef Google scholar
[34]
Stegen, J.C., Lin, X.J., Fredrickson, J.K., Konopka, A.E., 2015. Estimating and mapping ecological processes influencing microbial community assembly. Frontiers in Microbiology6, 370.
[35]
Sun, J.N., Zhang, C.Z., Yu, D.Y., Yin, X.Y., Cheng, Y.H., Chen, X.Y., Liu, M.Q., 2024a. Responses of invertebrate traits to litter chemistry accelerate decomposition under nitrogen enrichment. Soil Biology and Biochemistry198, 109572.
CrossRef Google scholar
[36]
Sun, X., Xie, Z.J., Qiao, Z.H., Gao, M.X., Yin, R., Chang, L., Wu, D.H., Liu, M.Q., Zhu, Y.G., 2024b. Research advances in trait-based approaches in soil animal community ecology. Chinese Journal of Applied Ecology35, 1150–1158.
[37]
Sun, Y., Lan, X.P., Shao, H.T., 2014. Advances of researches on soil-dwelling springtails as bioindicators. Chinese Agricultural Science Bulletin30, 6–9.
[38]
Thakuria, D., Schmidt, O., Finan, D., Egan, D., Doohan, F.M., 2010. Gut wall bacteria of earthworms: a natural selection process. The ISME Journal4, 357–366.
CrossRef Google scholar
[39]
Vellend, M., 2010. Conceptual synthesis in community ecology. The Quarterly Review of Biology85, 183–206.
CrossRef Google scholar
[40]
Wang, Y.F., Xu, J.Y., Liu, Z.L., Cui, H.L., Chen, P., Cai, T.G., Li, G., Ding, L.J., Qiao, M., Zhu, Y.G., Zhu, D., 2024. Biological interactions mediate soil functions by altering rare microbial communities. Environmental Science & Technology58, 5866–5877.
[41]
Xiang, Q., Chen, Q.L., Yang, X.R., Li, G., Zhu, D., 2022. Microbial multitrophic communities drive the variation of antibiotic resistome in the gut of soil woodlice (Crustacea: Isopoda). Environmental Science & Technology56, 15034–15043.
[42]
Xie, Z.J., Chen, T.W., Potapov, M., Zhang, F., Wu, D.H., Scheu, S., Sun, X., 2022. Ecological and evolutionary processes shape below-ground springtail communities along an elevational gradient. Journal of Biogeography49, 469–482.
CrossRef Google scholar
[43]
Xu, Q.C., Vandenkoornhuyse, P., Li, L., Guo, J.J., Zhu, C., Guo, S.W., Ling, N., Shen, Q.R., 2022. Microbial generalists and specialists differently contribute to the community diversity in farmland soils. Journal of Advanced Research40, 17–27.
CrossRef Google scholar
[44]
Xu, X., Wang, W.F., Ruan, H.H., 2019. Effects of soil fauna on the decomposition of forest litter: mechanism and modeling. Chinese Journal of Ecology38, 2858–2865.
[45]
Yang, X.Y., Li, G., Xiu, W.M., 2025. Responses of a soil-inhabiting collembolan (Entomobrya proxima Folsom) to organic fertilizer addition illustrated by functional traits and gut bacterial community. Frontiers in Microbiology16, 1509447.
CrossRef Google scholar
[46]
Yang, X.Y., Li, G., Xiu, W.M., 2024. Transcriptome responses of the soil-dwelling collembolan (Entomobrya proxima Folsom) to fertilizer type and concentration. Biology13, 950.
CrossRef Google scholar
[47]
Yin, R., Kardol, P., Thakur, M.P., Gruss, I., Wu, G.L., Eisenhauer, N., Schädler, M., 2020. Soil functional biodiversity and biological quality under threat: Intensive land use outweighs climate change. Soil Biology and Biochemistry147, 107847.
CrossRef Google scholar
[48]
Zhou, J.Z., Ning, D.L., 2017. Stochastic community assembly: does it matter in microbial ecology? Microbiology and Molecular Biology Review 81, e00002–17.
[49]
Zhu, D., Chen, Q.L., An, X.L., Yang, X.R., Christie, P., Ke, X., Wu, L.H., Zhu, Y.G., 2018a. Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition. Soil Biology and Biochemistry116, 302–310.
CrossRef Google scholar
[50]
Zhu, D., Zheng, F., Chen, Q.L., Yang, X.R., Christie, P., Ke, X., Zhu, Y.G., 2018b. Exposure of a soil collembolan to Ag nanoparticles and AgNO3 disturbs its associated microbiota and lowers the incidence of antibiotic resistance genes in the gut. Environmental Science & Technology52, 12748–12756.

Author contributions

Xinyue Yang: Conceptualization, Methodology, Software, Validation, Formal analysis, Investigation, Resources, Data curation, Writing—original draft preparation, Writing—review and editing, Visualization. Gang Li: Conceptualization, Methodology, Software, Validation, Writing—review and editing, Supervision. Weiming Xiu: Writing—review and editing, Supervision, Funding acquisition, Project administration. All authors have read and agreed to the published version of the manuscript.

Declaration of competing interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgements

This study was funded by the Scientific and Technological Innovation Project of the Chinese Academy of Agricultural Sciences (Grant No. CAASZDRW202408).

Data availability statement

No data was used for the research described in the article. The sequencing data were submitted to NCBI under Bio Project PRJNA1196609.

Institutional review board statement

This study did not require ethical approval; all data are available in the public domain. The collected Entomobrya proxima does not fall within the protection scope stipulated in the Wildlife Protection Law of the People’s Republic of China.

RIGHTS & PERMISSIONS

2025 Higher Education Press
PDF(5936 KB)

Part of a collection:

Biodiversity and Ecological Functions of Soil Fauna

20

Accesses

0

Citations

Detail

Sections
Recommended

/