Plant above-ground biomass and litter quality drive soil microbial metabolic limitations during vegetation restoration of subtropical forests

Highlights

● Soil C-, N-, P-acquiring enzymes changed significantly during vegetation restoration.

● Microbial metabolisms were co-limited by C and P during vegetation restoration.

● Microbial C limitation was significantly affected by microbial CUE under the influence of litter quality.

● Microbial P limitation was significantly affected by soil elements and their stoichiometry under the influence of AGB.

Abstract

Changes in litter quality (carbon:nitrogen, C:N) and above-ground biomass (AGB) following vegetation restoration significantly impact soil physicochemical properties, yet their effects on soil microbial metabolic limitations remain unclear. We measured litter quality, AGB, soil physicochemical properties, and extracellular enzyme activity (EEA) along a vegetation restoration gradient (7, 14, 49, 70 years, and nearly climax evergreen broadleaved forests) in southern China. We also evaluated soil microbial metabolic limitations by a vector analysis of the EEA. Results revealed the soil microbial metabolisms were co-limited by C and phosphorus (P). The microbial C limitation initially decreased (before 14 years) and then increased, while the microbial P limitation initially increased (before 49 years) and then decreased. Partial least squares path modeling (PLS-PM) showed that the microbial C limitation was mainly attributed to microbial C use efficiency induced by litter quality, suggesting that microorganisms may transfer cellular energy between microbial growth and C-acquiring enzyme production. The microbial P limitation was primarily correlated with AGB-driven change in soil elements and their stoichiometry, highlighting the importance of nutrient stoichiometry and balance in microbial metabolism. The shifts between microbial C and P limitations and the strong connections of plant–soil-microbe processes during vegetation restoration revealed here will provide us with helpful information for optimal management to achieve forest restoration success.

Graphical abstract

Keywords

Extracellular enzymatic stoichiometry / Microbial metabolic limitations / Above-ground biomass / Litter quality / Vegetation restoration / Subtropic

References

[1] Allison, S.D., Vitousek, P.M., 2005. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology & Biochemistry37, 937–944.

[2] Alves, L.F., Vieira, S.A., Scaranello, M.A., Camargo, P.B., Santos, F.A.M., Joly, C.A., Martinelli, L.A., 2010. Forest structure and live aboveground biomass variation along an elevational gradient of tropical Atlantic moist forest (Brazil). Forest Ecology and Management260, 679–691.

[3] Bai, Z., Wu, X., Lin, J.J., Xie, H.T., Yuan, H.S., Liang, C., 2019. Litter-, soil- and C:N-stoichiometry-associated shifts in fungal communities along a subtropical forest succession. Catena178, 350–358.

[4] Bell, C.W., Fricks, B.E., Rocca, J.D., Steinweg, J.M., McMahon, S.K., Wallenstein, M.D., 2013. High-throughput fluorometric measurement of potential soil extracellular enzyme activities. Journal of Visualized Experiments81, e50961.

[5] Berggren, M., Laudon, H., Jonsson, A., Jansson, M., 2010. Nutrient constraints on metabolism affect the temperature regulation of aquatic bacterial growth efficiency. Microbial Ecology60, 894–902.

[6] Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology & Biochemistry17, 837–842.

[7] Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biology & Biochemistry14, 319–329.

[8] Čapek, P., Manzoni, S., Kaštovská, E., Wild, B., Diáková, K., Bárta, J., Schnecker, J., Biasi, C., Martikainen, P.J., Alves, R.J.E., Guggenberger, G., Gentsch, N., Hugelius, G., Palmtag, J., Mikutta, R., Shibistova, O., Urich, T., Schleper, C., Richter, A., Šantrůčková, H., 2018. A plant–microbe interaction framework explaining nutrient effects on primary production. Nature Ecology & Evolution2, 1588–1596.

[9] Chapin, F.S. III, Zavaleta, E.S., Eviner, V.T., Naylor, R.L., Vitousek, P.M., Reynolds, H.L., Hooper, D.U., Lavorel, S., Sala, O.E., Hobbie, S.E., Mack, M.C., Díaz, S., 2000. Consequences of changing biodiversity. Nature405, 234–242.

[10] Chen, C., Fang, X., Xiang, W., Lei, P., Ouyang, S., Kuzyakov, Y., 2020. Soil-plant co-stimulation during forest vegetation restoration in a subtropical area of southern China. Forest Ecosystems7, 32.

[11] Chen, C., Park, T., Wang, X., Piao, S., Xu, B., Chaturvedi, R.K., Fuchs, R., Brovkin, V., Ciais, P., Fensholt, R., Tømmervik, H., Bala, G., Zhu, Z., Nemani, R.R., Myneni, R.B., 2019. China and India lead in greening of the world through land-use management. Nature Sustainability2, 122–129.

[12] Chen, C.R., Condron, L.M., Davis, M.R., Sherlock, R.R., 2000. Effects of afforestation on phosphorus dynamics and biological properties in a New Zealand grassland soil. Plant and Soil220, 151–163.

[13] Cline, L.C., Zak, D.R., 2015. Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology96, 3374–3385.

[14] Córdova, S.C., Olk, D.C., Dietzel, R.N., Mueller, K.E., Archontouilis, S.V., Castellano, M.J., 2018. Plant litter quality affects the accumulation rate, composition, and stability of mineral-associated soil organic matter. Soil Biology & Biochemistry125, 115–124.

[15] Cotrufo, M.F., Wallenstein, M.D., Boot, C.M., Denef, K., Paul, E. 2013. The Microbial Efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?. Global Change Biology19, 988–995.

[16] Cui, Y., Fang, L., Guo, X., Han, F., Ju, W., Ye, L., Wang, X., Tan, W., Zhang, X., 2019. Natural grassland as the optimal pattern of vegetation restoration in arid and semi-arid regions: Evidence from nutrient limitation of soil microbes. Science of the Total Environment648, 388–397.

[17] Cule, E., Moritz, S., Frankowski, D., 2022. ridge: Ridge Regression with Automatic Selection of the Penalty Parameter, R package version 3.1 ed

[18] Deng, L., Peng, C., Huang, C., Wang, K., Liu, Q., Liu, Y., Hai, X., Shangguan, Z., 2019. Drivers of soil microbial metabolic limitation changes along a vegetation restoration gradient on the Loess Plateau, China. Geoderma353, 188–200.

[19] Deng, Q., McMahon, D.E., Xiang, Y., Yu, C.L., Jackson, R.B., Hui, D., 2017. A global meta-analysis of soil phosphorus dynamics after afforestation. New Phytologist213, 181–192.

[20] Deng, Q., Zhang, D., Han, X., Chu, G., Zhang, Q., Hui, D., 2018. Changing rainfall frequency rather than drought rapidly alters annual soil respiration in a tropical forest. Soil Biology & Biochemistry121, 8–15.

[21] Du, E., Terrer, C.T., Pellegrini, A.F., Ahlström, A., van Lissa, C.J., Zhao, X., Xia, N., Wu, X., Jackson, R.B., 2020. Global patterns of terrestrial nitrogen and phosphorus limitation. Nature Geoscience13, 221–226.

[22] Gaston, S., Laura, T., Russolillo, G., 2015. plspm: Tools for Partial Least Squares Path Modeling

[23] Geyer, K.M., Dijkstra, P., Sinsabaugh, R.L., Frey, S.D., 2019. Clarifying the interpretation of carbon use efficiency in soil through methods comparison. Soil Biology & Biochemistry128, 79–88.

[24] Gong, L., Liu, G., Wang, M., Ye, X., Wang, H., Li, Z., 2017. Effects of vegetation restoration on soil organic carbon in China: A meta-analysis. Chinese Geographical Science27, 188–200.

[25] Griffiths, B.S., Spilles, A., Bonkowski, M., 2012. C:N:P stoichiometry and nutrient limitation of the soil microbial biomass in a grazed grassland site under experimental P limitation or excess. Ecological Processes1, 6.

[26] Harris, J. A., Hobbs, R. J., Higgs, E., Aronson, J. 2006. Ecologieal restoraion and global climate change. Restoration Ecology14, 170–176.

[27] Huang, F., Zhang, W., Gan, X., Huang, Y., Guo, Y., Wen, X., 2018. Changes in vegetation and soil properties during recovery of a subtropical forest in South China. Journal of Mountain Science15, 46–58.

[28] Huang, W., Liu, J., Wang, Y., Zhou, G., Han, T., Li, Y., 2013. Increasing phosphorus limitation along three successional forests in southern China. Plant and Soil364, 181–191.

[29] IUSS Working Group WRB, 2007. World reference base for soil resources 2006, first update 2007, World soil resources reports No. 103 ed. FAO, Rome

[30] Jenkinson, D.S., Brookes, P.C., Powlson, D.S., 2004. Measuring soil microbial biomass. Soil Biology & Biochemistry36, 5–7.

[31] Jian, S., Li, J., Chen, J., Wang, G., Mayes, M.A., Dzantor, K.E., Hui, D., Luo, Y., 2016. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biology & Biochemistry101, 32–43.

[32] Jones, D.L., Magthab, E.A., Gleeson, D.B., Hill, P.W., Sánchez-Rodríguez, A.R., Roberts, P.R., Ge, T., Murphy, D.V., 2018. Microbial competition for nitrogen and carbon is as intense in the subsoil as in the topsoil. Soil Biology & Biochemistry117, 72–82.

[33] Kabacoff, R.I., 2015. R in action: Data Analysis and Graphics with R (2nd ed). Manning, New Yorkpp. 1–608.

[34] Kallenbach, C.M., Frey, S.D., Grandy, A.S., 2016. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nature Communications7, 13630.

[35] Kivlin, S.N., Waring, B.G., Averill, C., Hawkes, C.V., 2013. Tradeoffs in microbial carbon allocation may mediate soil carbon storage in future climates. Frontiers in Microbiology4, 261.

[36] Kotroczó, Z., Veres, Z., Fekete, I., Krakomperger, Z., Tóth, J.A., Lajtha, K., Tóthmérész, B., 2014. Soil enzyme activity in response to long-term organic matter manipulation. Soil Biology & Biochemistry70, 237–243.

[37] Krishna, M.P., Mohan, M., 2017. Litter decomposition in forest ecosystems: a review. Energy, Ecology & Environment2, 236–249.

[38] Li, D., Niu, S., Luo, Y., 2012. Global patterns of the dynamics of soil carbon and nitrogen stocks following afforestation: a meta-analysis. New Phytologist195, 172–181.

[39] Li, T., Wang, R., Cai, J., Meng, Y., Wang, Z., Feng, X., Liu, H., Turco, R.F., Jiang, Y., 2021. Enhanced carbon acquisition and use efficiency alleviate microbial carbon relative to nitrogen limitation under soil acidification. Ecological Processes10, 32.

[40] Lohbeck, M., Poorter, L.P., Martínez-Ramos, M., Bongers, F., 2015. Biomass is the main driver of changes in ecosystem process rates during tropical forest succession. Ecology96, 1242–1252.

[41] Malik, A.A., Puissant, J., Goodall, T., Allison, S.D., Griffiths, R.I., 2019. Soil microbial communities with greater investment in resource acquisition have lower growth yield. Soil Biology & Biochemistry132, 36–39.

[42] Manzoni, S., Taylor, P., Richter, A., Porporato, A., Ågren, G.I., 2012. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist196, 79–91.

[43] Manzoni, S., Trofymow, J.A., Jackson, R.B., Porporato, A., 2010. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecological Monographs80, 89–106.

[44] Moorhead, D.L., Rinkes, Z.L., Sinsabaugh, R.L., Weintraub, M.N., 2013. Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Frontiers in Microbiology4, 223.

[45] Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry93, 1–7.

[46] Moreno-Mateos, D., Alberdi, A., Morriën, E., van der Putten, W.H., Rodríguez-Uña, A., Montoya, D., 2020. The long-term restoration of ecosystem complexity. Nature Ecology & Evolution4, 676–685.

[47] Mori, T. 2020. Does ecoenzymatic stoichiometry really determine microbial nutrient limitations?. Soil Biology & Biochemistry146, 107816.

[48] Mori, T., Lu, X., Aoyagi, R., Mo, J., 2018. Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Functional Ecology32, 1145–1154.

[49] Nelson, D.W., Sommers, L.E., 1996. Total carbon, organic carbon, and organic matter. In: Sparks, D.L., Page, A.L., Helmke, P.A., eds. Methods of Soil Analysis. Madison: Soil Science Society of America, pp. 961–1010.

[50] Ouyang, S., Xiang, W., Wang, X., Zeng, Y., Lei, P., Deng, X., Peng, C., 2016. Significant effects of biodiversity on forest biomass during the succession of subtropical forest in south China. Forest Ecology and Management372, 291–302.

[51] Parton, W., Silver, W.L., Burke, I.C., Grassens, L., Harmon, M.E., Currie, W.S., King, J.Y., Adair, E.C., Brandt, L.A., Hart, S.C., Fasth, B., 2007. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science315, 361–364.

[52] Pickett, S.T.A., 1989. Space-for-time Substitution as an Alternative to Long-term Studies. In: Likens, G.E., ed. Long-term Studies in Ecology: Approaches and Alternatives. New York: Springer, 110–135.

[53] Qu, L., Wang, C., Bai, E., 2020. Evaluation of the ¹⁸O-H₂O incubation method for measurement of soil microbial carbon use efficiency. Soil Biology & Biochemistry145, 107802.

[54] R Core Team, 2020. R: A language and environment for statistical computing, 4.0.3 ed. R foundation for statistical computing, Vienna, Austria

[55] Sauvadet, M., Chauvat, M., Cluzeau, D., Maron, P.A., Villenave, C., Bertrand, I., 2016. The dynamics of soil micro-food web structure and functions vary according to litter quality. Soil Biology & Biochemistry95, 262–274.

[56] Schimel, J.P., Weintraub, M.N., 2003. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology & Biochemistry35, 549–563.

[57] Sinsabaugh, R.L., Hill, B.H., Shah, J.J.F., 2009. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature462, 795–798.

[58] Sinsabaugh, R.L., Manzoni, S., Moorhead, D.L., Richter, A., 2013. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecology Letters16, 930–939.

[59] Sinsabaugh, R.L., Shah, J.J.F., 2012. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics43, 313–343.

[60] Smith, A.P., Marín-Spiotta, E., Balser, T., 2015. Successional and seasonal variations in soil and litter microbial community structure and function during tropical postagricultural forest regeneration: a multiyear study. Global Change Biology21, 3532–3547.

[61] Soong, J.L., Fuchslueger, L., Marañon-Jimenez, S., Torn, M.S., Janssens, I.A., Penuelas, J., Richter, A., 2020. Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling. Global Change Biology26, 1953–1961.

[62] Turner, B.L., Brenes-Arguedas, T., Condit, R., 2018. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature555, 367–370.

[63] Veldkamp, E., Schmidt, M., Powers, J.S., Corre, M.D., 2020. Deforestation and reforestation impacts on soils in the tropics. Nature Reviews Earth & Environment1, 590–605.

[64] Weand, M.P., Arthur, M.A., Lovett, G.M., Sikora, F.S., Weathers, K.C., 2010. The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization. Biogeochemistry97, 159–181.

[65] Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag

[66] Wu, J., He, Z.L., Wei, W.X., O’Donnell, A.G., Syers, J.K., 2000. Quantifying microbial biomass phosphorus in acid soils. Biology and Fertility of Soils32, 500–507.

[67] Xiang, W., Zhou, J., Ouyang, S., Zhang, S., Lei, P., Li, J., Deng, X., Fang, X., Forrester, D., 2016. Species-specific and general allometric equations for estimating tree biomass components of subtropical forests in southern China. European Journal of Forest Research135, 963–979.

[68] Xu, S., Liu, L.L., Sayer, E.J., 2013. Variability of above-ground litter inputs alters soil physicochemical and biological processes: a meta-analysis of litterfall-manipulation experiments. Biogeosciences10, 7423–7433.

[69] Yang, Y., Liang, C., Wang, Y., Cheng, H., An, S., Chang, S., 2020. Soil extracellular enzyme stoichiometry reflects the shift from P- to N-limitation of microorganisms with grassland restoration. Soil Biology & Biochemistry149, 107928.

[70] Zhou, G., Xu, S., Ciais, P., Manzoni, S., Fang, J., Yu, G., Tang, X., Zhou, P., Wang, W., Yan, J., Wang, G., Ma, K., Li, S., Du, S., Han, S., Ma, Y., Zhang, D., Liu, J., Liu, S., Chen, X., 2019. Climate and litter C/N ratio constrain soil organic carbon accumulation. National Science Review6, 746–757.

[71] Zhu, Q., Riley, W.J., Tang, J., 2017. A new theory of plant-microbe nutrient competition resolves inconsistencies between observations and model predictions. Ecological Applications27, 875–886.

[72] Zhu, W., Xiang, W., Pan, Q., Zeng, Y., Ouyang, S., Lei, P., Deng, X., Fang, X., Peng, C., 2016. Spatial and seasonal variations of leaf area index (LAI) in subtropical secondary forests related to floristic composition and stand characters. Biogeosciences13, 3819–3831.

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China for Distinguished Young Scholars (Grant No. 41825020) and General Program (Grant No. 31870461), the “Hundred Talent Program” of South China Botanical Garden at the Chinese Academy of Sciences (Grant No. Y761031001), the “Young Top-notch Talent” in Pearl River talent plan of Guangdong Province (Grant No. 2019QN01L763), the Guangdong Basic and Applied Basic Research Foundation (Grant No. 2021A1515012147), and the China Scholarships Council (Grant No. 202004910605). We thank Dr. Ji Chen for the English polish of the manuscript. We thank Zhongbing Chang, Yang Chen, and Zhiwei Cao for the help with field sampling. We also thank Shenhua Wang, Lingxue Ma, Fengcai Liu, Xiaoying You, Xiaoping Pan for the help with laboratory analysis.

Conflicts of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-022-0154-2 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press