Linking soil nematode communities to plant- and microbial-derived carbon in a 15-year field experiment

Jigao Wang , Yanli Jing , Tao Wang , Kai Wei , Rui Yang , Jinlong Yan , Jialiang Tang , Bo Zhu

Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) : 260412

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Soil Ecology Letters ›› 2026, Vol. 8 ›› Issue (3) :260412 DOI: 10.1007/s42832-026-0412-9
RESEARCH ARTICLE
Linking soil nematode communities to plant- and microbial-derived carbon in a 15-year field experiment
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Abstract

Soil nematodes show the highest abundance among animals on Earth, which can affect plant residue decomposition by influencing plant roots and soil microbes, thus affecting plant- and microbial-derived carbon (C) sequestration. However, the relationships between soil nematodes, plant- and microbial-derived C under long-term fertilization remain unclear. The present work performed a 15-year field fertilization experiment (including four treatments: (1) no fertilizer (CK); (2) nitrogen, phosphorus, and potassium fertilizers (NPK); (3) NPK with straw (SNPK); and (4) NPK with pig manure (MNPK)) for investigating how soil nematodes affected soil plant- and microbial-derived C by determining soil nematode, bacterial, and fungal abundances as well as amino sugar and lignin phenol contents (their biomarkers), and their associated relationships. The results revealed that SNPK treatment increased the abundances of soil bacterivores and bacteria as well as the bacterial necromass C (BNC) content. As revealed by partial least squares path modeling (PLS-PM), bacterivores showed indirect and positive impacts on BNC through influencing the abundance of bacteria. Moreover, SNPK treatment increased fungal abundance and fungal necromass C (FNC) content but did not alter fungivore abundance. FNC was significantly and positively correlated with fungal abundance and bacterivore abundance. PLS-PM revealed that BNC indirectly influenced FNC by affecting fungal abundance; thus, bacterivores play an important role in affecting FNC by affecting BNC. Moreover, all the fertilization treatments increased the lignin phenol content, which was significantly and positively correlated with the bacterivore and plant parasite abundances, indicating that the elevated bacterivore and plant parasite abundances during fertilization may contribute to the formation of plant-derived C. Overall, these findings provide insights for developing fertilization strategies that utilize nematode-mediated C pathways to enhance soil C sequestration in agricultural systems.

Graphical abstract

Keywords

soil nematodes / soil organic C / microbial necromass / fertilization

Highlight

● Fertilization boosts bacterivores, enhancing plant- and microbial-derived C formation.

● Fungal necromass C is influenced by bacterivores rather than fungivores.

● Plant-derived C was positively correlated with bacterivores and plant parasites.

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Jigao Wang, Yanli Jing, Tao Wang, Kai Wei, Rui Yang, Jinlong Yan, Jialiang Tang, Bo Zhu. Linking soil nematode communities to plant- and microbial-derived carbon in a 15-year field experiment. Soil Ecology Letters, 2026, 8(3): 260412 DOI:10.1007/s42832-026-0412-9

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References

[1]

Angst, G., Mueller, K.E., Nierop, K.G.J., Simpson, M.J., 2021. Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter. Soil Biology and Biochemistry156, 108189.

[2]

Angst, G., Potapov, A., Joly, F.X., Angst, Š., Frouz, J., Ganault, P., Eisenhauer, N., 2024. Conceptualizing soil fauna effects on labile and stabilized soil organic matter. Nature Communications15, 5005.

[3]

Appuhn, A., Joergensen, R.G., 2006. Microbial colonisation of roots as a function of plant species. Soil Biology and Biochemistry38, 1040–1051.

[4]

Back, M.A., Haydock, P.P.J., Jenkinson, P., 2002. Disease complexes involving plant parasitic nematodes and soilborne pathogens. Plant Pathology51, 683–697.

[5]

Bian, Q., Zhao, L.X., Cheng, K., Jiang, Y.J., Li, D.M., Xie, Z.B., Sun, B., Wang, X.Y., 2024. Divergent accumulation of microbe- and plant-derived carbon in different soil organic matter fractions in paddy soils under long-term organic amendments. Agriculture, Ecosystems & Environment366, 108934.

[6]

Bongers, T., 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia83, 14–19.

[7]

Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology10, 239–251.

[8]

Buckeridge, K.M., Creamer, C., Whitaker, J., 2022. Deconstructing the microbial necromass continuum to inform soil carbon sequestration. Functional Ecology36, 1396–1410.

[9]

Camenzind, T., Mason-Jones, K., Mansour, I., Rillig, M.C., Lehmann, J., 2023. Formation of necromass-derived soil organic carbon determined by microbial death pathways. Nature Geoscience16, 115–122.

[10]

Carvalhais, N., Forkel, M., Khomik, M., Bellarby, J., Jung, M., Migliavacca, M., Mu, M., Saatchi, S., Santoro, M., Thurner, M., Weber, U., Ahrens, B., Beer, C., Cescatti, A., Randerson, J.T., Reichstein, M., 2014. Global covariation of carbon turnover times with climate in terrestrial ecosystems. Nature514, 213–217.

[11]

Chen, X.B., Hu, Y.J., Xia, Y.H., Zheng, S.M., Ma, C., Rui, Y.C., He, H.B., Huang, D.Y., Zhang, Z.H., Ge, T.D., Wu, J.S., Guggenberger, G., Kuzyakov, Y., Su, Y.R., 2021. Contrasting pathways of carbon sequestration in paddy and upland soils. Global Change Biology27, 2478–2490.

[12]

Chen, Z.M., He, L.L., Ma, J.C., Ma, J.W., Ye, J., Yu, Q.G., Zou, P., Sun, W.C., Lin, H., Wang, F., Zhao, X., Wang, Q., 2024. Long-term successive biochar application increases plant lignin and microbial necromass accumulation but decreases their contributions to soil organic carbon in rice-wheat cropping system. Global Change Biology16, e13137.

[13]

De’Ath, G., 2007. Boosted trees for ecological modeling and prediction. Ecology88, 243–251.

[14]

Dupla, X., Gondret, K., Sauzet, O., Verrecchia, E., Boivin, P., 2021. Changes in topsoil organic carbon content in the Swiss leman region cropland from 1993 to present. Insights from large scale on-farm study. Geoderma400, 115125.

[15]

Engelking, B., Flessa, H., Joergensen, R.G., 2007. Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biology and Biochemistry39, 2111–2118.

[16]

Fanin, N., Kardol, P., Farrell, M., Nilsson, M.C., Gundale, M.J., Wardle, D.A., 2019. The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biology and Biochemistry128, 111–114.

[17]

Fu, S.L., Ferris, H., Brown, D., Plant, R., 2005. Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size. Soil Biology and Biochemistry37, 1979–1987.

[18]

Gan, H.J., Wickings, K., 2020. Root herbivory and soil carbon cycling: shedding “green” light onto a “brown” world. Soil Biology and Biochemistry150, 107972.

[19]

Glaser, B., Turrión, M.B., Alef, K., 2004. Amino sugars and muramic acid—biomarkers for soil microbial community structure analysis. Soil Biology and Biochemistry36, 399–407.

[20]

Hastie, T., Tibshirani, R., Friedman, J., 2009. The Elements of Statistical Learning: Data Mining, Inference, and Prediction. 2nd ed. New York: Springer.

[21]

Hicks Pries, C.E., Castanha, C., Porras, R.C., Torn, M.S., 2017. The whole-soil carbon flux in response to warming. Science355, 1420–1423.

[22]

Ingham, R.E., Trofymow, J.A., Ingham, E.R., Coleman, D.C., 1985. Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecological Monographs55, 119–140.

[23]

James, G., Witten, D., Hastie, T., Tibshirani, R., 2021. An Introduction to Statistical Learning: with Applications in R. 2nd ed. New York: Springer.

[24]

Jiang, Y., Wang, Z.H., Liu, Y., Han, Y.L., Wang, Y., Wang, Q., Liu, T., 2023. Nematodes and their bacterial prey improve phosphorus acquisition by wheat. New Phytologist237, 974–986.

[25]

Jiang, Y.J., Liu, M.Q., Zhang, J.B., Chen, Y., Chen, X.Y., Chen, L.J., Li, H.X., Zhang, X.X., Sun, B., 2017. Nematode grazing promotes bacterial community dynamics in soil at the aggregate level. The ISME Journal11, 2705–2717.

[26]

Jiang, Y.J., Luan, L., Hu, K.J., Liu, M.Q., Chen, Z.Y., Geisen, S., Chen, X.Y., Li, H.X., Xu, Q.S., Bonkowski, M., Sun, B., 2020. Trophic interactions as determinants of the arbuscular mycorrhizal fungal community with cascading plant-promoting consequences. Microbiome8, 142.

[27]

Jiang, Y.J., Qian, H.Y., Wang, X.Y., Chen, L.J., Liu, M.Q., Li, H.X., Sun, B., 2018. Nematodes and microbial community affect the sizes and turnover rates of organic carbon pools in soil aggregates. Soil Biology and Biochemistry119, 22–31.

[28]

Kou, X.C., Ma, N.N., Zhang, X.K., Xie, H.T., Zhang, X.D., Wu, Z.F., Liang, W.J., Li, Q., Ferris, H., 2020. Frequency of stover mulching but not amount regulates the decomposition pathways of soil micro-foodwebs in a no-tillage system. Soil Biology and Biochemistry144, 107789.

[29]

Kou, X.C., Morriën, E., Tian, Y.J., Zhang, X.K., Lu, C.Y., Xie, H.T., Liang, W.J., Li, Q., Liang, C., 2023. Exogenous carbon turnover within the soil food web strengthens soil carbon sequestration through microbial necromass accumulation. Global Change Biology29, 4069–4080.

[30]

Kramer, C., Gleixner, G., 2008. Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biology and Biochemistry40, 425–433.

[31]

Lehmann, J., Bossio, D.A., Kögel-Knabner, I., Rillig, M.C., 2020. The concept and future prospects of soil health. Nature Reviews Earth & Environment1, 544–553.

[32]

Lessmann, M., Ros, G.H., Young, M.D., de Vries, W., 2022. Global variation in soil carbon sequestration potential through improved cropland management. Global Change Biology28, 1162–1177.

[33]

Li, Z., Wei, X.M., Zhu, Z.K., Fang, Y.Y, Yuan, H.Z., Li, Y.H., Zhu, Q.H., Guo, X.B., Wu, J.S., Kuzyakov, Y., Ge, T.D., 2024. Organic fertilizers incorporation increased microbial necromass accumulation more than mineral fertilization in paddy soil via altering microbial traits. Applied Soil Ecology193, 105137.

[34]

Liang, C., Amelung, W., Lehmann, J., Kästner, M., 2019. Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology25, 3578–3590.

[35]

Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.

[36]

Neher, D.A., 2010. Ecology of plant and free-living nematodes in natural and agricultural soil. Annual Review of Phytopathology48, 371–394.

[37]

Otto, A., Simpson, M.J., 2006. Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry80, 121–142.

[38]

Panchal, P., Preece, C., Peñuelas, J., Giri, J., 2022. Soil carbon sequestration by root exudates. Trends in Plant Science27, 749–757.

[39]

Puissant, J., Villenave, C., Chauvin, C., Plassard, C., Blanchart, E., Trap, J., 2021. Quantification of the global impact of agricultural practices on soil nematodes: a meta-analysis. Soil Biology and Biochemistry161, 108383.

[40]

Ringle, C.M., Wende, S., Becker, J.M., 2024. "SmartPLS 4." Bönningstedt: SmartPLS. .

[41]

Rønn, R., McCaig, A.E., Griffiths, B.S., Prosser, J.I., 2002. Impact of protozoan grazing on bacterial community structure in soil microcosms. Applied and Environmental Microbiology68, 6094–6105.

[42]

Siddique, S., Coomer, A., Baum, T., Williamson, V.M., 2022. Recognition and response in plant-nematode interactions. Annual Review of Phytopathology60, 143–162.

[43]

Thakur, M.P., Geisen, S., 2019. Trophic regulations of the soil microbiome. Trends in Microbiology27, 771–780.

[44]

Townshend, J.L., 1963. A modification and evaluation of the apparatus for the oostenbrink direct cottonwool filter extraction method. Nematologica9, 106–110.

[45]

van den Hoogen, J., Geisen, S., Routh, D., Ferris, H., Traunspurger, W., Wardle, D.A., de Goede, R.G.M., Adams, B.J., Ahmad, W., Andriuzzi, W.S., Bardgett, R.D., Bonkowski, M., Campos-Herrera, R., Cares, J.E., Caruso, T., de Brito Caixeta, L., Chen, X.Y., Costa, S.R., Creamer, R., da Cunha Castro, J.M., Dam, M., Djigal, D., Escuer, M., Griffiths, B.S., Gutierrez, C., Hohberg, K., Kalinkina, D., Kardol, P., Kergunteuil, A., Korthals, G., Krashevska, V., Kudrin, A.A., Li, Q., Liang, W.J., Magilton, M., Marais, M., Martín, J.A.R., Matveeva, E., Mayad, E.H., Mulder, C., Mullin, P., Neilson, R., Nguyen, T.A.D., Nielsen, U.N., Okada, H., Rius, J.E.P., Pan, K.W., Peneva, V., Pellissier, L., da Silva, J.C.P., Pitteloud, C., Powers, T.O., Powers, K., Quist, C.W., Rasmann, S., Moreno, S.S., Scheu, S., Setälä, H., Sushchuk, A., Tiunov, A.V., Trap, J., van der Putten, W., Vestergård, M., Villenave, C., Waeyenberge, L., Wall, D.H., Wilschut, R., Wright, D.G., Yang, J.I., Crowther, T.W., 2019. Soil nematode abundance and functional group composition at a global scale. Nature572, 194–198.

[46]

Wang, J.G., Wei, K., Jing, Y.L., Wang, Y.L., Yan, J.L., Wang, T., Tang, J.L., Zhu, B., 2026. Soil microbivorous nematodes contribute to the formation of microbial necromass carbon under full straw return. Agriculture, Ecosystems and Environment396, 109975.

[47]

Wang, J.G., Wei, K., Tang, J.L., Yuan, C.Y., Wang, Y.L., Sun, X.M., Zhu, B., 2025. Addition of bacterial-feeding nematodes contributes to soil phosphorus availability by affecting the mineralization of moderately labile organic phosphorus. Applied Soil Ecology205, 105764.

[48]

Wang, J.G., Zhao, X.C., Wei, K., Oladipo, D.G., Yuan, C.Y., Jin, B.C., Sun, X.M., Zhu, B.J., Tang, J.L., Zhu, B., 2022. The relationships of bacterial-feeding nematodes, phoD-harboring bacteria and alkaline phosphomonoesterase activity under the combined application of organic and inorganic fertilizers in an alkaline soil. Applied Soil Ecology179, 104595.

[49]

Wardle, D.A., Yeates, G.W., 1993. The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food-webs. Oecologia93, 303–306.

[50]

Ye, G.P., Lin, Y.X., Kuzyakov, Y., Liu, D.Y., Luo, J.F., Lindsey, S., Wang, W.J., Fan, J.B., Ding, W.X., 2019. Manure over crop residues increases soil organic matter but decreases microbial necromass relative contribution in upland Ultisols: results of a 27-year field experiment. Soil Biology and Biochemistry134, 15–24.

[51]

Yeates, G.W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils37, 199–210.

[52]

Yeates, G.W., Bongers, T., 1999. Nematode diversity in agroecosystems. Agriculture, Ecosystems & Environment74, 113–135.

[53]

Yeates, G.W., Bongers, T., De Goede, R.G., Freckman, D.W., Georgieva, S.S., 1993. Feeding-habits in soil nematode families and genera-an outline for soil ecologists. Journal of Nematology25, 315–331.

[54]

Zhang, X.D., Amelung, W., 1996. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology and Biochemistry28, 1201–1206.

[55]

Zhao, Y.C., Wang, M.Y., Hu, S.J., Zhang, X.F., Ouyang, Z., Zhang, G.L., Huang, B., Zhao, S.W., Wu, J.S., Xie, D.T., Zhu, B., Yu, D.S., Pan, X.Z., Xu, S.X., Shi, X.Z., 2018. Economics- and policy-driven organic carbon input enhancement dominates soil organic carbon accumulation in Chinese croplands. Proceedings of the National Academy of Sciences of the United States of America115, 4045–4050.

[56]

Zheng, T.T., Miltner, A., Liang, C., Nowak, K.M., Kästner, M., 2023. Turnover of bacterial biomass to soil organic matter via fungal biomass and its metabolic implications. Soil Biology and Biochemistry180, 108995.

[57]

Zhou, R.R., Liu, Y., Dungait, J.A.J., Kumar, A., Wang, J.S., Tiemann, L.K., Zhang, F.S., Kuzyakov, Y., Tian, J., 2023. Microbial necromass in cropland soils: a global meta-analysis of management effects. Global Change Biology29, 1998–2014.

[58]

Zhu, B., Wang, T., Kuang, F.H., Luo, Z.X., Tang, J.L., Xu, T.P., 2009. Measurements of nitrate leaching from a hillslope cropland in the Central Sichuan Basin, China. Soil Science Society of America Journal73, 1419–1426.

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