Contribution of bacterivorous nematodes to soil resistance and resilience under copper or heat stress

Abstract

The functional performance of soil ecosystems following disturbance determines ecosystem stability, and although contributions of bacterivorous nematodes to soil ecosystems are recognized, their roles in functional stability have received little attention. The objective of this study was to evaluate the roles of bacterivorous nematodes in functional stability following stress. In a factorial laboratory experiment, soil microcosms were prepared with two levels of nematode abundance, either an enriched abundance of bacterivores (Nema soil) or background abundance of nematodes (CK soil), and three levels of stress, copper, heat, or an unstressed control. The resistance and resilience of nematode abundance, as well as soil microbial function by determining decomposition of plant residues and microbial substrate utilization pattern using a BIOLOG microplate, were followed post stress. The relative changes of two dominant bacterivores, Acrobeloides and Protorhabditis, responded differently to stresses. The resistance and resilience of Protorhabditis were greater than that of Acrobeloides to copper stress during the whole incubation period, while both bacterivores only showed higher resilience under heat stress at the end of incubation. The enrichment of bacterivores had no significant effects on the soil microbial resistance but significantly increased its resilience to copper stress. Under heat stress, the positive effect of bacterivores on soil resilience was only evident from 28 days to the end of incubation. The differences in the responses of soil function to stress with or without bacterivores suggested that soil nematodes could be conducive to ecosystem stability, highlighting the soil fauna should be taken into account in soil sustainable management.

Keywords

Stress / Soil resistant / Soil resilience / Bacterivores / Functional stability

References

[1] Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511

[2] Beare, M.H., Reddy, M.V., Tian, G., Srivastava, S.C., 1997. Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: The role of decomposer biota. Applied Soil Ecology 6, 87–108

[3] Bongers, T., Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology 10, 239–251

[4] Bongers, T., Ferris, H., 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution 14, 224–228

[5] Bonkowski, M., Cheng, W., Griffiths, B.S., Alphei, J., Scheu, S., Cheng, W.X., 2000. Microbial-faunal interactions in the rhizosphere and effects on plant growth. European Journal of Soil Biology 36, 135–147

[6] Brussaard, L., de Ruiter, P.C., Brown, G.G., 2007. Soil biodiversity for agricultural sustainability. Agriculture, Ecosystems & Environment 121, 233–244

[7] Chen, X., Liu, M., Hu, F., Mao, X., Li, H., 2007. Contributions of soil microfauna (protozoa and nematodes) to rhizosphere ecological functions. Acta Ecologica Sinica 27, 3132–3143

[8] Coleman, D.C., Crossley, D.A. Jr, Hendrix, P.F., 2004. Fundamentals of Soil Ecology, 2nd ed. Elsevier Academic Press, San Diego, CA.

[9] Cortois, R., Veen, G.F., Duyts, H., Abbas, M., Strecker, T., Kostenko, O., Eisenhauer, N., Scheu, S., Gleixner, G., De Deyn, G.B., van der Putten, W.H., 2017. Possible mechanisms underlying abundance and diversity responses of nematode communities to plant diversity. Ecosphere 8, 1–14

[10] Danneyrolles, V., Dupuis, S., Fortin, G., Leroyer, M., de Romer, A., Terrail, R., Vellend, M., Boucher, Y., Laflamme, J., Bergeron, Y., Arseneault, D., 2019. Stronger influence of anthropogenic disturbance than climate change on century-scale compositional changes in northern forests. Nature Communications 10, 1265

[11] de Vries, F.T., Liiri, M.E., Bjørnlund, L., Bowker, M.A., Christensen, S., Setälä, H.M., Bardgett, R.D., 2012. Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change 2, 276–280

[12] Delgado-Baquerizo, M., Eldridge, D.J., Ochoa, V., Gozalo, B., Singh, B.K., Maestre, F.T., 2017. Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe. Ecology Letters 20, 1295–1305

[13] Delgado-Baquerizo, M., Reich, P.B., Trivedi, C., Eldridge, D.J., Abades, S., Alfaro, F.D., Bastida, F., Berhe, A.A., Cutler, N.A., Gallardo, A., García-Velázquez, L., Hart, S.C., Hayes, P.E., He, J.Z., Hseu, Z.Y., Hu, H.W., Kirchmair, M., Neuhauser, S., Pérez, C.A., Reed, S.C., Santos, F., Sullivan, B.W., Trivedi, P., Wang, J.T., Weber-Grullon, L., Williams, M.A., Singh, B.K., 2020. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nature Ecology & Evolution 4, 210–220

[14] Doran, J.W., Zeiss, M.R., 2000. Soil health and sustainability: managing the biotic component of soil quality. Applied Soil Ecology 15, 3–11

[15] Dussault, M., Bécaert, V., Francois, M., Sauvé, S., Deschênes, L., 2008. Effect of copper on soil functional stability measured by relative soil stability index (RSSI) based on two enzyme activities. Chemosphere 72, 755–762

[16] Ekschmitt, K., Korthals, G.W., 2006. Nematodes as sentinels of heavy metals and organic toxicants in the soil. Journal of Nematology 38, 13–19.

[17] Ferris, H., Bongers, T., 2006. Nematode indicators of organic enrichment. Journal of Nematology 38, 3–12.

[18] Fiscus, D.A., Neher, D.A., 2002. Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances. Ecological Applications 12, 565–575

[19] Geisen, S., Wall, D.H., van der Putten, W.H., 2019. Challenges and opportunities for soil biodiversity in the Anthropocene. Current Biology 29, R1036–R1044

[20] Girvan, M.S., Campbell, C.D., Killham, K., Prosser, J.I., Glover, L.A., 2005. Bacterial diversity promotes community stability and functional resilience after perturbation. Environmental Microbiology 7, 301–313

[21] Griffiths, B.S., Bonkowski, M., Dobson, G., Caul, S., 1999. Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43, 297–304.

[22] Griffiths, B.S., Bonkowski, M., Roy, J., Ritz, K., 2001. Functional stability, substrate utilisation and biological indicators of soils following environmental impacts. Applied Soil Ecology 16, 49–61

[23] Griffiths, B.S., Philippot, L., 2013. Insights into the resistance and resilience of the soil microbial Community. FEMS Microbiology Reviews 37, 112–129

[24] Griffiths, B.S., Ritz, K., Bardgett, R.D., Cook, R., Christensen, S., Ekelund, F., Sørensen, S., Bååth, E., Bloem, J., de Ruiter, P.C., Dolfing, J., Nicolardot, B., 2000. Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity ecosystem function relationship. Oikos 90, 279–294

[25] Hewitt, J., Thrush, S., Lohrer, A., Townsend, M., 2010. A latent threat to biodiversity: consequences of small-scale heterogeneity loss. Biodiversity and Conservation 19, 1315–1323

[26] 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 Monographs 55, 119–140

[27] Jones, D., Candido, E.P.M., 1999. Feeding is inhibited by sublethal concentrations of toxicants and by heat stress in the nematode Caenorhabditis elegans: Relationship to the cellular stress response. Journal of Experimental Zoology 284, 147–157

[28] Kardol, P., Throop, H.L., Adkins, J., de Graaff, M.A., 2016. A hierarchical framework for studying the role of biodiversity in soil food web processes and ecosystem services. Soil Biology & Biochemistry 102, 33–36

[29] Korthals, G.W., van de Ende, A., van Megen, H., Lexmond, T.M., Kammenga, J.E., Bongers, T., 1996. Short-term effects of cadmium, copper, nickel and zinc on soil nematodes from different feeding and life-history strategy groups. Applied Soil Ecology 4, 107–117

[30] Kuan, H.L., Fenwick, C., Glover, L.A., Griffiths, B.S., Ritz, K., 2006. Functional resilience of microbial communities from perturbed upland grassland soils to further persistent or transient stresses. Soil Biology & Biochemistry 38, 2300–2306

[31] Li, J., Peng, P., Zhao, J., 2020. Assessment of soil nematode diversity based on different taxonomic levels and functional groups. Soil Ecology Letters 2, 33–39

[32] Li, Q., Jiang, Y., Liang, W.J., 2006. Effect of heavy metals on soil nematode communities in the vicinity of a metallurgical factory. Journal of Environmental Sciences (China) 18, 323–328.

[33] Liu, M., Chen, X., Griffiths, B.S., Huang, Q., Li, H., Hu, F., 2012. Dynamics of nematode assemblages and soil function in adjacent restored and degraded soils following disturbance. European Journal of Soil Biology 49, 37–46

[34] Liu, M., Chen, X., Qin, J., Wang, D., Griffiths, B., Hu, F., 2008. A sequential extraction procedure reveals that water management affects soil nematode communities in paddy fields. Applied Soil Ecology 40, 250–259

[35] Mao, X.F., Hu, F., Griffiths, B.S., Li, H.X., 2006. Bacterial-feeding nematodes enhance root growth of tomato seedlings. Soil Biology & Biochemistry 38, 1615–1622

[36] Neher, D.A., 2010. Ecology of plant and free-living nematodes in natural and agricultural soil. Annual Review of Phytopathology 48, 371–394

[37] Nielsen, U.N., Wall, D.H., Six, J., 2015. Soil biodiversity and the environment. Annual Review of Environment and Resources 40, 63–90

[38] Orgiazzi, A., Bardgett, R.D., Barrios, E., Behan-Pelletier, V., Briones, M.J.I., Chotte, J., De Deyn, G.B., Eggleton, P., Fierer, N., Fraser, T., Hedlund, K., Jeffery, S., Johnson, N.C., Jones, A., 2016. Global Soil Biodiversity Atlas. European Commission. Luxembourg: Publications Office of the European Union.

[39] Orwin, K.H., Wardle, D.A., 2004. New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biology & Biochemistry 36, 1907–1912

[40] Pothula, S.K., Grewal, P.S., Auge, R.M., Saxton, A.M., Bernard, E.C., 2019. Agricultural intensification and urbanization negatively impact soil nematode richness and abundance: a meta-analysis. Journal of Nematology 51, 1–17

[41] Rein, I.V., Gessler, A., Katrin, P., Claudia, K., Andreas, U., Kayler, Z.E., 2016. Forest understory plant and soil microbial response to an experimentally induced drought and heat-pulse event: the importance of maintaining the continuum. Global Change Biology 22, 2861–2874

[42] Schratzberger, M., Holterman, M., van Oevelen, D., Helder, J., 2019. A worm’s world: Ecological flexibility pays off for free-living nematodes in sediments and soils. Bioscience 69, 867–876

[43] Schwarz, B., Barnes, A.D., Thakur, M.P., Brose, U., Ciobanu, M., Reich, P.B., Rich, R.L., Rosenbaum, B., Stefanski, A., Eisenhauer, N., 2017. Warming alters the energetic structure and function but not resilience of soil food webs. Nature Climate Change 7, 895–900

[44] Sturhan, D., 1986. Influence of heavy metals and other elements on soil nematodes. Revue de Nématologie 9, 311.

[45] Thakur, M.P., Geisen, S., 2019. Trophic regulations of the soil microbiome. Trends in Microbiology 27, 771–780

[46] Thakur, M.P., Tilman, D., Purschke, O., Ciobanu, M., Cowles, J., Isbell, F., Wragg, P.D., Eisenhauer, N., 2017. Climate warming promotes species diversity, but with greater taxonomic redundancy, in complex environments. Science Advances 3, e1700866

[47] Tilman, D., Cassman, K.G., Matson, P.A., Naylor, R., Polasky, S., 2002. Agricultural sustainability and intensive production practices. Nature 418, 671–677

[48] Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E., 2016. Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil 398, 1–24

[49] Wagg, C., Bender, S.F., Widmer, F., van der Heijden, M.G.A., 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America 111, 5266–5270

[50] Yang, G., Wagg, C., Veresoglou, S.D., Hempel, S., Rillig, M.C., 2018. How soil biota drive ecosystem stability. Trends in Plant Science 23, 1057–1067

[51] Yeates, G., 2007. Abundance, diversity, and resilience of nematode assemblages in forest soils. Canadian Journal of Forest Research 37, 216–225

[52] Yeates, G.W., 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils 37, 199–210

[53] Zhang, X.K., Li, Q., Zhu, A.N., Liang, W.J., Zhang, J.B., Steinberger, Y., 2012. Effects of tillage and residue management on soil nematode communities in North China. Ecological Indicators 13, 75–81

[54] Zhao, J., Neher, D.A., 2013. Soil nematode genera that predict specific types of disturbance. Applied Soil Ecology 64, 135–141

[55] Zhu, B., Xue, J., Xia, R., Jin, M., Wu, Y., Tian, S., Chen, X., Liu, M., Hu, F., 2019. Effect of soil nematode functional guilds on plant growth and aboveground herbivores. Shengwu Duoyangxing 27, 409–418

[56] Zhu, T., Yang, C., Wang, J., Zeng, S., Liu, M., Yang, J., Bai, B., Cao, J., Chen, X., Müller, C., 2018. Bacterivore nematodes stimulate soil gross N transformation rates depending on their species. Biology and Fertility of Soils 54, 107–118

Acknowledgment

This work was supported by the National Foundation of Sciences in China (No. 41877056) and China Agriculture Research System-Green Manure (No. CARS-22-G-10).

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