Land rehabilitation improves edaphic conditions and increases soil microbial biomass and abundance

Abstract

Rehabilitation of farmland improves the local eco-environmental conditions. But to what extent this transformation influences soil microbial properties is less known. In our study we compared variations in soil microbial attributes following changes in land-use types to understand the influence of altered soil properties on microbial biomass and their community structure using chloroform fumigation extraction method and phospholipid fatty acid (PLFA) analysis. For this purpose, 3 agricultural (AL) (farmland, apple orchard and 2 years abandoned land) and 4 rehabilitated lands (RL) of various vegetations grassland, shrubland, mixed forest (Amorpha fruticosa and Pinus tabuliformis Carr.) and forest (Robinia pseudoacacia) were selected. Our results showed higher soil organic carbon (SOC) contents in RL soils (forest>mixed forest>grassland>shrub land) than that in AL soils. In RL soils, soil microbial biomass and abundance of group specific PLFA were significantly higher than those in AL soils. Under different land-use types, microbial community was bacteria dominated over fungi. The microbial physiological indices (G⁺/G⁻, cyc/prec and S/M) indicated decreased environmental stress in RL soils in comparison with AL soils. In loess soils, SOC and total N correlated positively (p<0.05) with microbial biomass C, N and P and also with fungal and bacterial PLFA, indicating a positive microbial mediation in improving soil fertility. Taking together, our findings suggest that land rehabilitation, especially Robinia pseudoacacia planation, improves overall edaphic conditions and accelerates soil microbial biomass accumulation in local regions.

Keywords

Land-use change / Soil microbial carbon / Chloroform fumigation extraction / PLFA / Physiological indices

References

[1] Achat, D.L., Augusto, L., Bakker, M.R., Gallet-Budynek, A., Morel, C., 2012. Microbial processes controlling P availability in forest spodosols as affected by soil depth and soil properties. Soil Biology & Biochemistry 44, 39–48

[2] Almagro, M., Querejeta, J.I., Boix-Fayos, C., Martínez-Mena, M., 2013. Links between vegetation patterns, soil C and N pools and respiration rate under three different land uses in a dry Mediterranean ecosystem. Journal of Soils and Sediments 13, 641–653

[3] An, S.S., Cheng, Y., Huang, Y.M., Liu, D., 2012. Effects of revegetation on soil microbial biomass, enzyme activities, and nutrient cycling on the Loess Plateau in China. Restoration Ecology 21, 600–607

[4] Aoki, M., Fujii, K., Kitayama, K., 2012. Environmental control of root exudation of low-molecular weight organic acids in tropical rainforests. Ecosystems 15, 1194–1203

[5] Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology & Biochemistry 35, 955–963

[6] Bao, S.D., 2007. Soil Agricultural Chemistry Analysis, 3rd edition. Beijing: China Agriculture Press.

[7] Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biology & Biochemistry 14, 319–329

[8] Buckeridge, K.M., Banerjee, S., Siciliano, S.D., Grogan, P., 2013. The seasonal pattern of soil microbial community structure in mesic low arctic tundra. Soil Biology & Biochemistry 65, 338–347

[9] Cookson, W.R., Osman, M., Marschner, P., Abaye, D.A., Clark, I., Murphy, D.V., Stockdale, E.A., Watson, C.A., 2007. Controls on soil nitrogen cycling and microbial community composition across land use and incubation temperature. Soil Biology & Biochemistry 39, 744–756

[10] Corti, G., Agnelli, A., Cuniglio, R., Sanjurjo, M.F., Cocco, S., 2005. Characteristics of Rhizosphere Soil from Natural and Agricultural Environments. In: Huang, P.M., Gobran G.R., eds. Biogeochemistry of Trace Elements in the Rhizosphere. Amsterdam: Elsevier, 57–128.

[11] Courty, P.E., Buée, M., Diedhiou, A.G., Frey-Klett, P., Le Tacon, F., Rineau, F., Turpault, M.P., Uroz, S., Garbaye, J., 2010. The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts. Soil Biology & Biochemistry 42, 679–698

[12] de Andrés, F., Walter, I., Tenorio, J.L., 2007. Revegetation of abandoned agricultural land amended with biosolids. Science of the Total Environment 378, 81–83

[13] Delgado-Baquerizo, M., Reich, P.B., Khachane, A.N., Campbell, C.D., Thomas, N., Freitag, T.E., Abu Al-Soud, W., Sørensen, S., Bardgett, R.D., Singh, B.K., 2017. It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environmental Microbiology 19, 1176–1188

[14] Deng, L., Shangguan, Z., Li, R., 2012. Effects of the grain-for-green program on soil erosion in China. International Journal of Sediment Research 27, 120–127

[15] Deng, L., Shangguan, Z.P., Sweeney, S., 2013. Changes in soil carbon and nitrogen following land abandonment of farmland on the Loess Plateau, China. PLoS One 8, e71923

[16] Drenovsky, R.E., Elliott, G.N., Graham, K.J., Scow, K.M., 2004. Comparison of phospholipid fatty acid (PLFA) and total soil fatty acid methyl esters (TSFAME) for characterizing soil microbial communities. Soil Biology & Biochemistry 36, 1793–1800

[17] Drenovsky, R.E., Steenwerth, K.L., Jackson, L.E., Scow, K.M., 2010. Land use and climatic factors structure regional patterns in soil microbial communities. Global Ecology and Biogeography 19, 27–39

[18] Fazhu, Z., Jiao, S., Chengjie, R., Di, K., Jian, D., Xinhui, H., Gaihe, Y., Yongzhong, F., Guangxin, R., 2015. Land use change influences soil C, N and P stoichiometry under ‘Grain-to-Green Program’ in China. Scientific Reports 5, 10195

[19] Fierer, N., Schimel, J.P., Holden, P.A., 2003. Influence of drying-rewetting frequency on soil bacterial community structure. Microbial Ecology 45, 63–71

[20] Frostegård, A., Bååth, E., 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22, 59–65

[21] Frostegard, A., Tunlid, A., Baath, E., 1993. Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Applied and Environmental Microbiology 59, 3605–3617

[22] Graesser, J., Aide, T.M., Grau, H.R., Ramankutty, N., 2015. Cropland/pastureland dynamics and the slowdown of deforestation in Latin America. Environmental Research Letters 10, 034017

[23] Grayston, S.J., Campbell, C.D., Bardgett, R.D., Mawdsley, J.L., Clegg, C.D., Ritz, K., Griffiths, B.S., Rodwell, J.S., Edwards, S.J., Davies, W.J., Elston, D.J., Millard, P., 2004. Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Applied Soil Ecology 25, 63–84

[24] Guan, X., Wang, J., Zhao, H., Wang, J., Luo, X., Liu, F., Zhao, F., 2013. Soil bacterial communities shaped by geochemical factors and land use in a less-explored area, Tibetan Plateau. BMC Genomics 14, 820

[25] Guo, S., Han, X., Li, H., Wang, T., Tong, X., Ren, G., Feng, Y., Yang, G., 2018. Evaluation of soil quality along two revegetation chronosequences on the Loess Hilly Region of China. Science of the Total Environment 633, 808–815

[26] Güsewell, S., Gessner, M.O., 2009. N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Functional Ecology 23, 211–219

[27] Havlin, J.L., Kissel, D.E., Maddux, L.D., Claassen, M.M., Long, J.H., 1990. Crop rotation and tillage effects on soil organic carbon and nitrogen. Soil Science Society of America Journal 54, 448–452

[28] Holl, K.D., 2002. Effect of shrubs on tree seedling establishment in an abandoned tropical pasture. Journal of Ecology 90, 179–187

[29] Hoyle, F.C., Murphy, D.V., 2011. Influence of organic residues and soil incorporation on temporal measures of microbial biomass and plant available nitrogen. Plant and Soil 347, 53–64

[30] Iyyemperumal, K., Israel, D.W., Shi, W., 2007. Soil microbial biomass, activity and potential nitrogen mineralization in a pasture: Impact of stock camping activity. Soil Biology & Biochemistry 39, 149–157

[31] Jangid, K., Williams, M.A., Franzluebbers, A.J., Schmidt, T.M., Coleman, D.C., Whitman, W.B., 2011. Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biology & Biochemistry 43, 2184–2193

[32] Joergensen, R., Wichern, F., 2008. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology & Biochemistry 40, 2977–2991

[33] Joergensen, R.G., Mueller, T., 1996. The fumigation-extraction method to estimate soil microbial biomass: Calibration of the kEN value. Soil Biology & Biochemistry 28, 33–37

[34] Kim, Y., Ullah, S., Moore, T.R., Roulet, N.T., 2014. Dissolved organic carbon and total dissolved nitrogen production by boreal soils and litter: The role of flooding, oxygen concentration, and temperature. Biogeochemistry 118, 35–48

[35] Knoke, T., Bendix, J., Pohle, P., Hamer, U., Hildebrandt, P., Roos, K., Gerique, A., Sandoval, M.L., Breuer, L., Tischer, A., Silva, B., Calvas, B., Aguirre, N., Castro, L.M., Windhorst, D., Weber, M., Stimm, B., Günter, S., Palomeque, X., Mora, J., Mosandl, R., Beck, E., 2014. Afforestation or intense pasturing improve the ecological and economic value of abandoned tropical farmlands. Nature Communications 5, 5612

[36] Kooijman, A.M., Van Mourik, J.M., Schilder, M.L.M., 2009. The relationship between N mineralization or microbial biomass N with micromorphological properties in beech forest soils with different texture and pH. Biology and Fertility of Soils 45, 449–459

[37] Kou, M., Garcia-Fayos, P., Hu, S., Jiao, J., 2016a. The effect of Robinia pseudoacacia afforestation on soil and vegetation properties in the Loess Plateau (China): A chronosequence approach. Forest Ecology and Management 375, 146–158

[38] Kou, M., Jiao, J., Yin, Q., Wang, N., Wang, Z., Li, Y., Yu, W., Wei, Y., Yan, F., Cao, B., 2016b. Successional trajectory over 10€years of vegetation restoration of abandoned slope croplands in the Hill-Gully Region of the Loess Plateau. Land Degradation & Development 27, 919–932

[39] Lapola, D.M., Martinelli, L.A., Peres, C.A., Ometto, J.P.H.B., Ferreira, M.E., Nobre, C.A., Aguiar, A.P.D., Bustamante, M.M.C., Cardoso, M.F., Costa, M.H., Joly, C.A., Leite, C.C., Moutinho, P., Sampaio, G., Strassburg, B.B.N., Vieira, I.C.G., 2014. Pervasive transition of the Brazilian land-use system. Nature Climate Change 4, 27–35

[40] Lauber, C.L., Ramirez, K.S., Aanderud, Z., Lennon, J., Fierer, N., 2013. Temporal variability in soil microbial communities across land-use types. ISME Journal 7, 1641–1650

[41] Lauber, C.L., Strickland, M.S., Bradford, M.A., Fierer, N., 2008. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biology & Biochemistry 40, 2407–2415

[42] Li, J., Tong, X., Awasthi, M.K., Wu, F., Ha, S., Ma, J., Sun, X., He, C., 2018. Dynamics of soil microbial biomass and enzyme activities along a chronosequence of desertified land revegetation. Ecological Engineering 111, 22–30

[43] Li, Q., Liang, J.H., He, Y.Y., Hu, Q.J., Yu, S., 2014. Effect of land use on soil enzyme activities at karst area in Nanchuan, Chongqing, Southwest China. Plant, Soil and Environment 60, 15–20

[44] Liu, D., An, S.S., Cheng, Y., Keiblinger, K., Huang, Y.M., 2014a. Variability in soil microbial biomass and diversity among different aggregate-size fractions of different land use types. Soil Science 179, 242–249

[45] Liu, D., Huang, Y., Sun, H., An, S., 2018b. The restoration age of Robinia pseudoacacia plantation impacts soil microbial biomass and microbial community structure in the Loess Plateau. Catena 165, 192–200

[46] Liu, D., Keiblinger, K.M., Leitner, S., Mentler, A., Zechmeister-Boltenstern, S., 2016. Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay? Geoderma 272, 93–100

[47] Liu, D., Keiblinger, K.M., Leitner, S., Wegner, U., Zimmermann, M., Fuchs, S., Lassek, C., Riedel, K., Zechmeister-Boltenstern, S., 2019. Response of microbial communities and their metabolic functions to drying–rewetting stress in a temperate forest soil. Microorganisms 7, 129–142

[48] Liu, D., Yang, Y., An, S., Wang, H., Wang, Y., 2018d. The biogeographical distribution of soil bacterial communities in the loess plateau as revealed by high-throughput sequencing. Frontiers in Microbiology 9, 9

[49] Liu, H.Y., Huang, Y., An, S., Sun, H., Bhople, P., Chen, Z., 2018a. Soil physicochemical and microbial characteristics of contrasting land-use types along soil depth gradients. Catena 162, 345–353

[50] Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., Wang, G., 2014b. High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biology & Biochemistry 70, 113–122

[51] Liu, X., Liu, X., Shao, X., Songer, M., He, B., He, X., Zhu, Y., 2018c. Plant diversity patterns of temperate forests with logging and restoration practices in northwest China. Ecological Engineering 124, 116–122

[52] Martens, D., 2000. Plant residue biochemistry regulates soil carbon cycling and carbon sequestration. Soil Biology & Biochemistry 32, 361–369

[53] McGuire, K.L., Bent, E., Borneman, J., Majumder, A., Allison, S.D., Treseder, K.K., 2010. Functional diversity in resource use by fungi. Ecology 91, 2324–2332

[54] Menyailo, O.V., Hungate, B.A., Abraham, W.R., Conrad, R., 2008. Changing land use reduces soil CH₄ uptake by altering biomass and activity but not composition of high-affinity methanotrophs. Global Change Biology 14, 2405–2419

[55] Nilsson, S., 2015. Global trends and possible future land use. In: Westholm, E., Lindahl B. K., Kraxner, F., eds. The Future Use of Nordic Forests: A Global Perspective. Berlin: Springer-Verlag, 43–62.

[56] Nu, R.K., 1999. Soil Agricultural Chemical Analysis. Beijing: China Agricultural Science and Technology Press.

[57] O’Connor, R.J., 1988. Multivariate analysis of ecological communities. Trends in Ecology & Evolution 3, 121

[58] Olsson, P.A., 1999. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiology Ecology 29, 303–310

[59] Ordway, E.M., Asner, G.P., Lambin, E.F., 2017. Deforestation risk due to commodity crop expansion in sub-Saharan Africa. Environmental Research Letters 12, 044015

[60] Poyatos, R., Latron, J., Llorens, P., 2003. Land use and land cover change after agricultural abandonment. Mountain Research and Development 23, 362–368

[61] Raiesi, F., 2012a. Land abandonment effect on N mineralization and microbial biomass N in a semi-arid calcareous soil from Iran. Journal of Arid Environments 76, 80–87

[62] Raiesi, F., 2012b. Soil properties and C dynamics in abandoned and cultivated farmlands in a semi-arid ecosystem. Plant and Soil 351, 161–175

[63] Riitters, K.H., Wickham, J.D., Wade, T.G., Vogt, P., 2012. Global survey of anthropogenic neighborhood threats to conservation of grass-shrub and forest vegetation. Journal of Environmental Management 97, 116–121

[64] Schloter, M., Dilly, O., Munch, J.C., 2003. Indicators for evaluating soil quality. Agriculture, Ecosystems & Environment 98, 255–262

[65] Shen, C., Xiong, J., Zhang, H., Feng, Y., Lin, X., Li, X., Liang, W., Chu, H., 2013. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biology & Biochemistry 57, 204–211

[66] Singh, K., Singh, B., Singh, R.R., 2012. Changes in physico-chemical, microbial and enzymatic activities during restoration of degraded sodic land: Ecological suitability of mixed forest over monoculture plantation. Catena 96, 57–67

[67] Starke, R., Kermer, R., Ullmann-Zeunert, L., Baldwin, I.T., Seifert, J., Bastida, F., von Bergen, M., Jehmlich, N., 2016. Bacteria dominate the short-term assimilation of plant-derived N in soil. Soil Biology & Biochemistry 96, 30–38

[68] Stirzaker, R.J., Passioura, J.B., Wilms, Y., 1996. Soil structure and plant growth: Impact of bulk density and biopores. Plant and Soil 185, 151–162

[69] Strickland, M.S., Rousk, J., 2010. Considering fungal:bacterial dominance in soils – Methods, controls, and ecosystem implications. Soil Biology & Biochemistry 42, 1385–1395

[70] Syers, J.K., 1997. Managing soils for long-term productivity. Philosophical Transactions of the Royal Society B, Biological Sciences 352, 1011–1021

[71] Tian, F., Feng, X., Zhang, L., Fu, B., Wang, S., Lv, Y., Wang, P., 2017. Effects of revegetation on soil moisture under different precipitation gradients in the Loess Plateau, China. Hydrology Research 48, 1378–1390

[72] Torsvik, V., Øvreås, L., 2002. Microbial diversity and function in soil: From genes to ecosystems. Current Opinion in Microbiology 5, 240–245

[73] van Asselen, S., Verburg, P.H., 2013. Land cover change or land-use intensification: simulating land system change with a global-scale land change model. Global Change Biology 19, 3648–3667

[74] Van Wijk, M.T., Williams, M., Gough, L., Hobbie, S.E., Shaver, G.R., 2003. Luxury consumption of soil nutrients: A possible competitive strategy in above-ground and below-ground biomass allocation and root morphology for slow-growing arctic vegetation? Journal of Ecology 91, 664–676

[75] Volkmar, K.M., 1993. A comparison of minirhizotron techniques for estimating root length density in soils of different bulk densities. Plant and Soil 157, 239–245

[76] Wang, B., Liu, G., Xue, S., Zhu, B., 2011. Changes in soil physico-chemical and microbiological properties during natural succession on abandoned farmland in the Loess Plateau. Environmental Earth Sciences 62, 915–925

[77] Wang, J., Liu, L., Qiu, X., Wei, Y., Li, Y., Shi, Z., 2016. Contents of soil organic carbon and nitrogen in water-stable aggregates in abandoned agricultural lands in an arid ecosystem of Northwest China. Journal of Arid Land 8, 350–363

[78] Wang, Z., Liu, G., Xu, M.X., Zhang, J., Wang, Y., Tang, L., 2012. Temporal and spatial variations in soil organic carbon sequestration following revegetation in the hilly Loess Plateau, China. Catena 99, 26–33

[79] Wang, Z.J., Jiao, J.Y., Su, Y., Chen, Y., 2014. The efficiency of large-scale afforestation with fish-scale pits for revegetation and soil erosion control in the steppe zone on the hill-gully Loess Plateau. Catena 115, 159–167

[80] Weigelt, A., Bol, R., Bardgett, R.D., 2005. Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142, 627–635

[81] Wheeler, K.A., Hurdman, B.F., Pitt, J.I., 1991. Influence of pH on the growth of some toxigenic species of Aspergillus, Penicillium and Fusarium. International Journal of Food Microbiology 12, 141–149

[82] Wu, J., Joergensen, R.G., Pommerening, B., Chaussod, R., Brookes, P.C., 1990. Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biology & Biochemistry 22, 1167–1169

[83] Wu, Y., Ma, B., Zhou, L., Wang, H., Xu, J., Kemmitt, S., Brookes, P.C., 2009. Changes in the soil microbial community structure with latitude in eastern China, based on phospholipid fatty acid analysis. Applied Soil Ecology 43, 234–240

[84] Wu, Y.T., Gutknecht, J., Nadrowski, K., Geißler, C., Kühn, P., Scholten, T., Both, S., Erfmeier, A., Böhnke, M., Bruelheide, H., Wubet, T., Buscot, F., 2012. Relationships between soil microorganisms, plant communities, and soil characteristics in Chinese subtropical forests. Ecosystems (New York, N.Y.) 15, 624–636

[85] Xiao, L., Liu, G., Zhang, J., Xue, S., 2016. Long-term effects of vegetational restoration on soil microbial communities on the Loess Plateau of China. Restoration Ecology 24, 794–804

[86] Xu, M., Zhang, J., Liu, G., Yamanaka, N., 2014. Soil properties in natural grassland, Caragana korshinskii planted shrubland, and Robinia pseudoacacia planted forest in gullies on the hilly Loess Plateau, China. Catena 119, 116–124

[87] Xu, Q., Jiang, P., Wang, H., 2010. Improvement of biochemical and biological properties of eroded red soil by artificial revegetation. Journal of Soils and Sediments 10, 255–262

[88] Xu, X., Zhang, T., Zhang, W., 2009. Function types and dynamic of landscape patchs along Zhifanggou watershed in last 25 years. Linye Kexue 45, 154–160.

[89] Yang, Y., Dou, Y., An, S., 2018. Testing association between soil bacterial diversity and soil carbon storage on the Loess Plateau. Science of the Total Environment 626, 48–58

[90] Zelles, L., Bai, Q.Y., Ma, R.X., Rackwitz, R., Winter, K., Beese, F., 1994. Microbial biomass, metabolic activity and nutritional status determined from fatty acid patterns and poly-hydroxybutyrate in agriculturally-managed soils. Soil Biology & Biochemistry 26, 439–446

[91] Zhang, C., Xue, S., Liu, G., Song, Z.L., 2011b. A comparison of soil qualities of different revegetation types in the Loess Plateau, China. Plant and Soil 347, 163–178

[92] Zhang, G., Chan, K.Y., Li, G.D., Huang, G., 2011a. The effects of stubble retention and tillage practices on surface soil structure and hydraulic conductivity of a loess soil. Acta Ecologica Sinica 31, 298–302

[93] Zhao, F., Han, X., Yang, G., Feng, Y., Ren, G., 2013. Policy-guided nationwide ecological recovery: Assessment of the Grain-to-Green Program of China. Journal of Food Agriculture and Environment 11, 1882–1890.

Acknowledgments

The authors are grateful to Z.J. Xue and Y. Chen for invaluable assistance during soil sampling. We thank Dr. Hanying Sun’s comments for the first draft, and J. H. Qi for technical assistance in laboratory. This work was funded by the National Natural Science Foundation of China (41701317), Science and Technology Service Network Initiative, Chinese Academy of Sciences (2017), and Open-Funds of Scientific Research Programs of State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau (A314021402-2002).

Conflict of interest

Dong Liu, Baorong Wang, Parag Bhople, Fayzmamad Davlatbekov and Fuqiang Yu declare that they have no conflict of interest.

RIGHTS & PERMISSIONS

2020 Higher Education Press