Changes in the soil microbial communities of different soil aggregations after vegetation restoration in a semiarid grassland, China

Highlights

• The soil aggregate stability increased with increasing duration of vegetation restoration.

• Natural restoration has a positve effect on soil microbial diversity was generally higher in large particle size aggregates, which leads to low environmental stress and strong stability.

• Microorganism continually changed their regulation of pathways as their environment changed.

• Environment adaptability influences soil physiological indicators to varying degrees.

• After years of natural restoration, the soil microbial community generally transformed from nutrient-rich to heterotroph-dominan.

Abstract

Soil aggregate fractions can regulate microbial community composition and structure after vegetation restoration. However, there has been less focus on the effects of soil aggregate fractions on the distributions of microbial communities. Here, we used phospholipid fatty acid (PLFA) analysis to explore the effects of different years of vegetation restoration (a 35-year-old Thymus mongolicus community (Re-35yrs) and a 2-year-old nongrazing grassland (Ug-2yrs)) on microbial communities within different soil aggregate sizes (<0.25 mm, 0.25–1 mm, 1–2 mm, 2–3 mm, 3–5 mm and>5 mm). The results indicated that the amount of total PLFA in Re-35yrs was 10 times greater than that in Ug-2yrs. The soil aggregate stability increased with increasing duration of vegetation restoration. In Re-35yrs, the total PLFA shown an increase as the soil aggregate size increased, and the highest values were observed in 3~5 mm. Ug-2yrs differed from Re-35yrs, the soil microbial diversity was higher in medium particle sizes (1–2 mm and 2–3 mm) and lower in microaggregates (<0.25 mm and 0.25–1 mm) and macroaggregates (3~5 mm and>5 mm). Soil microbial diversity was highest in large particle size aggregates, which resulted in low environmental stress and strong stability. The same tendency was observed in the high values of cyc/prec, S/M and soil organic matter, which indicated a lower turnover speed (F/B) of fungal energy utilization and a higher fixation rate. After years of natural restoration, the soil microbial community generally transformed from nutrient-rich to heterotroph-dominant, especially in microaggregates (reflected in the G⁺/G⁻ ratio).

Graphical abstract

Keywords

Vegetation restoration / Plant succession / Phospholipid fatty acid (PLFA) / Soil aggregate fractions / Soil microorganism group

References

[1] Allison, V.J., Miller R.M., Jastrow, J.D., Matamala, R., Zak, D.R., 2005. Changes in soil microbial community structure in a tallgrass prairie chronosequence. Soil Science Society of America Journal 69, 1412–1421

[2] An, S.S., Cheng, Y., Huang, Y.M., Liu, D., 2013. Effects of revegetation on soil microbial biomass, enzyme activities, and nutrient cycling on the Loess Plateau in China. Restoration Ecology 5, 600–607

[3] Bardgett, R.D., McAlister, E., 1999. The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biology and Fertility of Soils 29, 282–290

[4] Bell, C.W., Asao, S., Calderon, F., Wolk, B., Wallenstein, M.D., 2015. Plant nitrogen uptake drives rhizosphere bacterial community assembly during plant growth. Soil Biology & Biochemistry 85, 170–182

[5] Bonanomi, G., Cesarano, G., Lombardi, N., Motti, R., Scala, F., Mazzoleni, S., Incerti, G., 2017. Litter chemistry explains contrasting feeding preferences of bacteria, fungi, and higher plants. Scientific Reports 7, 9208

[6] Bossio, D.A., Scow, K.M., Gunapala, N., Graham, K.J., 1998. Determination of soil microbial communities: effects of agricultural management, season, and soil type on phospholipids fatty acid profiles. Microbial Ecology 36, 1–12

[7] Briar, S.S., Fonte, S.J., Park, I., Six, J., Scow, K., Ferris, H., 2011. The distribution of nematodes and soil microbial communities across soil aggregate fractionsand farm management systems. Soil Biology & Biochemistry 43, 905–914

[8] Cao, C.Y., Zhang, Y., Qian, W., Liang, C., Wang, C., Tao, S., 2017. Land-use changes influence soil bacterial communities in a meadow grassland in Northeast China. Solid Earth 8, 1119–1129

[9] Carrasco, L., Gattinger, A., Fliessbach, A., Roldán, A., Schloter, M., Caravaca, F., 2010. Estimation by PLFA of microbial community structure associated with the rhizosphere of Lygeum spartum and Piptatherum miliaceum growing in semiarid mine tailings. Microbial Ecology 60, 265–271

[10] Chen, X., Li, Z., Liu, M., Jiang, C., Che, Y., 2015. Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years. Journal of Soils and Sediments 15, 292–301

[11] Chen, Y.L., Xu, T., Veresoglou, S.D., Hu, H.W., Hao, Z.P., Hu, Y.J., Liu, L., Deng, Y., Rillig, M.C., Chen, B.D., 2017. Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biology & Biochemistry 110, 12–21

[12] Daynes, C.N., Zhang, N., Saleeba, J.A., McGee, P.A., 2012. Soil aggregates formed in vitro by saprotrophic Trichocomaceae have transient water-stability. Soil Biology & Biochemistry 48, 151–161

[13] Deng, L., Kim, D.G., Peng, C.H., Shangguan, Z., 2018. Controls of soil and aggregate associated organic carbon variations following natural vegetation restoration on the Loess Plateau in China. Land Degradation & Development 29, 3974–3984

[14] Deng, L., Shangguan, Z.P., 2017. Afforestation drives soil carbon and nitrogen changes in China. Land Degradation & Development 28, 151–165

[15] Deng, L., Zhang, Z., Shangguan, Z., 2014. Long-term fencing effects on plant diversity and soil properties in China. Soil & Tillage Research 137, 7–15

[16] Fanin, N., Moorhead, D., Bertrand, I., 2016. Eco-enzymatic stoichiometry and enzymatic vectors reveal differential C, N, P dynamics in decaying litter along a land-use gradient. Biogeochemistry 129, 21–36

[17] Federle, T.W., Dobbins, D.C., Thorton-Manning, J.R., Jones, D.D., 1986. Microbial biomass, activity, and community structure in subsurface soils. Ground Water 24, 365–374

[18] Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364

[19] 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

[20] Frostegård, A., Tunlid, A., Bååth, 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

[21] Guo, Y.Q., Hou, L.J., Zhang, Z.Y., Zhang, J., Cheng, J., Wei, G., Lin, Y., 2019. Soil microbial diversity during 30 years of grassland restoration on the Loess Plateau China: Tight linkages with plant diversity. Research Article 30, 1172–1182

[22] Herrera, P.S., Lebeis, S.L., Bailey, J.K., 2016. Giving back to the community: microbial mechanisms of plant–soil interactions. Functional Ecology 30, 1043–1052

[23] Janine, B.R., Jasmin, J., Bernhard, S., Helmut, B., Teri, B., 2005. Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspectives in Plant Ecology, Evolution and Systematics 7, 27–49

[24] Jiang, Y., Liu, M., Zhang, J., Chen, Y., Chen, X., Chen, L., Li, H., Zhang, X.X., Sun, B., 2017. Nematode grazing promotes bacterial community dynamics in soil at the aggregate level. ISME Journal 11, 2705–2717

[25] Kieft, T.L., Wilch, E., O’connor, K., Ringelberg, D.B., White, D.C., 1997. Survival and phospholipid fatty acid profiles of surface and subsurface bacteria in natural sediment microcosms. Applied and Environmental Microbiology 63, 1531–1542

[26] Kroppenstedt, R., 1985. Fatty acid and menaquinone analysis of actinomycetes and related organisms. In: Goodfellow, M., Minnikin, D., eds. Chemicalmethods in Bacterial Systematics, London: Academic Press, pp. 173–199.

[27] Leff, J.W., Jones, S.E., Prober, S.M., Barberán, A., Borer, E.T., Firn, J.L., Harpole, W.S., Hobbie, S.E., Hofmockel, K.S., Knops, J.M.H., McCulley, R.L., La Pierre, K., Risch, A.C., Seabloom, E.W., Schütz, M., Steenbock, C., Stevens, C.J., Fierer, N., 2015. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America 112, 10967–10972

[28] Lenka, N.K., Dass, A., Sudhishri, S., Patnaik, U.S., 2012. Soil carbon sequestration and erosion control potential of hedgerows and grass filter strips in sloping agricultural lands of eastern India. Agriculture, Ecosystems & Environment 158, 31–40

[29] Li, C., Fultz, L.M., Moore-Kucera, J., Acosta-Martínez, V., Kakarla, M., Weindorf, D.C., 2018. Soil microbial community restoration in Conservation Reserve Program semi-arid grasslands. Soil Biology & Biochemistry 118, 166–177

[30] Liao, H., Zhang, Y., Zuo, Q., Du, B., Chen, W., Wei, D., Huang, Q., 2018. Contrasting responses of bacterial and fungal communities to aggregate-size fractions and long-term fertilizations in soils of northeastern China. Science of the Total Environment 635, 784–792

[31] Liu J., Jia X. Y., Yan W. M., Zhong Y.Q., Shangguan Z.P., 2020a. Changes in soil microbial community structure during long-term secondary succession. Land Degradation & Development

[32] Liu, J., Li, S., Ouyang, Z., Tam, C., Chen, X., 2008. Ecological and socioeconomic effects of China’s policies for ecosystem services. Proceedings of the National Academy of Sciences of the United States of America 105, 9477–9482

[33] Liu, J.J., Zheng, Y.M., Yan, J.X., 2013. Succession of plant and soil microbial communities with restoration of abandoned land in the Loess Plateau, China. Journal of Soils and Sediments 13, 760–769

[34] Liu, Y.L., Zhu, G.Y., Hai X.Y., Li, J.W., Shangguan Z.P., Peng C.H., Deng L., 2020b. Long-term forest succession improves plant diversity and soil quality but not significantly increase soil microbial diversity: evidence from the Loess Plateau. Ecological Engineering 142, 105431

[35] Luo, S.S., Wang, S.J., Tian, L., Shi, S., Xu, S., Yang, F., Li, X., Wang, Z., Tian, C., 2018. Aggregate-related changes in soil microbial communities under different ameliorant applicaitons in saline-sodic soils. Geoderma 329, 108–117

[36] Mackay, J.E., Macdonald, L.M., Smernik, R.J., Cavagnaro, T.R., 2017. Organic amendments as phosphorus fertilisers: chemical analyses, biological processes and plant P uptake. Soil Biology & Biochemistry 107, 50–59

[37] Mäkipää, R., Rajala, T., Schigel, D., Rinne, K.T., Pennanen, T., Abrego, N., Ovaskainen, O., 2017. Interactions between soil- and dead wood-inhabiting fungal communities during the decay of Norway spruce logs. ISME Journal 11, 1964–1974

[38] Muruganandam, S., Israel, D.W., Robarge, W.P., 2010. Nitrogen transformations and microbial communities in soil aggregates from three tillage systems. Soil Science Society of America Journal 74, 120–129

[39] O’Leary, M.H., 1988. Carbon isotopes in photosynthesis. Bioscience 38, 328–336

[40] Pollierer, M.M., Ferlian, O., Scheu, S., 2015. Temporal dynamics and variation with forest type of phospholipid factty acids in litter and soil of temperate forests across regions. Soil Biology & Biochemistry 91, 248–257

[41] Ranjard, L., Richaume, A., 2001. Quantitative and qualitative microscale distribution of bacteria in soil. Research in Microbiology 152, 707–716

[42] Richardson, A.E., Lynch, J.P., Ryan, P.R., Delhaize, E., Smith, F.A., Smith, S.E., Harvey, P.R., Ryan, M.H., Veneklaas, E.J., Lambers, H., Oberson, A., Culvenor, R.A., Simpson, R.J., 2011. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil 349, 121–156

[43] Ringelberg, D.B., Stair, J.O., Almeida, J., Norby, R.J., O’Neill, E.G., White, D.C., 1997. Consequences of rising atmospheric carbon dioxide levels for the belowground microbiota associated with white oak. Journal of Environmental Quality 26, 495–503

[44] Sarker, T.C., Incerti, G., Spaccini, R., Piccolo, A., Mazzoleni, S., Bonanomi, G., 2018. Linking organic matter chemistry with soil aggregate stability: insight from ¹³C NMR spectroscopy. Soil Biology & Biochemistry 117, 175–184

[45] Schlüter s., Henjes S., Zawallich J., Bergaust, L., Horn, M., Lppisch, O., Vogel, H., Dorsch, P, 2018. Denitrification in soil aggregate analogues-effect of aggregate size and oxygen diffusion. Frontiers in Environmental Science 6, 17.

[46] Shi, X., Yu, D., Xu, S., Warner, E.D., Wang, H.J., Sun, W.X., Zhao, Y.C., Gong, Z.T., 2010. Cross-reference for relating genetic soil classification of China with WRB at different scales. Geoderma 155, 344–350

[47] Six, J., Elliott, E.T., Paustian, K., 2000. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry 32, 2099–2103

[48] Six, J., Frey, S.D., Thiet, R.K., Batten, K.M., 2006. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal 70, 555–569

[49] Smith, A.P., Marín-Spiotta, E., Graaff, M A D., Balser, T.C., 2014. Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biology & Biochemistry 77, 292–303

[50] Soil Survey Staff, 2010. Keys to Soil Taxonomy, U.S. Department of Agriculture11th ed. NRCS.

[51] Trivedi, P., Anderson, I.C., Singh, B.K., 2013. Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends in Microbiology 21, 641–651

[52] Trivedi, P., Delgado-Baquerizo, M., Jeffries, T.C., Trivedi, C., Anderson, I.C., Lai, K., McNee, M., Flower, K., Pal Singh, B., Minkey, D., Singh, B.K., 2017. Soil aggregation and associated microbial communities modify the impact of agricultural management on carbon content. Environmental Microbiology 19, 3070–3086

[53] Trivedi, P., Rochester, I.J., Trivedi, C., Van Nostrand, J.D., Zhou, J., Karunaratne, S., Anderson, I.C., Singh, B.K., 2015. Soil aggregate size mediates the impacts of cropping regimes on soil carbon and microbial communities. Soil Biology & Biochemistry 91, 169–181

[54] Upton, R.N., Bach, E.M., Hofmockel, K.S., 2019. Spatio-temporal microbial community dynamics within soil aggregates. Soil Biology & Biochemistry 132, 58–68

[55] Vos, M., Wolf, A.B., Jennings, S.J., Kowalchuk, G.A., 2013. Micro-scale determinants of bacterial diversity in soil. FEMS Microbiology Reviews 37, 936–954

[56] Walker, L.R., Walker, J., Hobbs, R.J., 2007. Linking Restoration and Ecological Succession. Berlin: Springer

[57] Wang, K., Zhang, Y., Tang, Z., Shangguan, Z., Chang, F., Jia, F., Chen, Y., He, X., Shi, W., Deng, L., 2019. Effects of grassland afforestation on structure and function of soil bacterial and fungal communities. Science of the Total Environment 676, 396–406

[58] Waring, B.G., Averill, C., Hawkes, C.V., 2013. Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecology Letters 16, 887–894

[59] Wilkinson, S.C., 1988. Gram-negative Bacteria. In: Ratledge, C., Wilkinson, S.C., eds. Microbial Lipids, vol 1. London: Academic Press, pp. 299–488.

[60] Xiao, L., Yao, K.H., Li, P., Liu, Y., Chang, E., Zhang, Y., Zhu, T., 2020. Increased soil aggregate stability is strongly correlated with root and soil properties along a gradient of secondary succession on the Loess Plateau. Ecological Engineering 143, 105671

[61] Yan, Y., Dai, Q., Hu, G., Jiao, Q., Mei, L., Fu, W., 2020. Effects of vegetation type on the microbial characteristics of the fissure soil-plant systems in karst rocky desertification regions of SW China. Science of the Total Environment 712, 136543

[62] Zelles L. 1999. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biology and Fertility of Soils 29, 111–129

[63] Zelles, L., Bai, Q.Y., Rackwitz, R., Chadwick, D., Beese, F., 1995. Determination of phospholipid-and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biology and Fertility of Soils 19, 115–123

[64] Zeng, J., Liu, X., Song, L., Lin, X., Zhang, H., Shen, C., Chu, H., 2015. Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biology & Biochemistry 92, 41–49

[65] Zhang, Q., Liang, G., Guo, T., He, P., Wang, X., Zhou, W., 2017. Evident variations of fungal and actinobacterial cellulolytic communities associated with different humified particle-size fractions in a long-term fertilizer experiment. Soil Biology & Biochemistry 113, 1–13

[66] Zhang, Q., Liang, G., Zhou, W., Sun, J., Wang, X., He, P., 2016. Fatty-acid profiles and enzyme activities in soil particle-size fractions under long-term fertilization. Soil Science Society of America Journal 80, 97–111

[67] Zhao, C., Long, J., Liao, H., Zheng, C., Li, J., Liu, L., Zhang, M., 2019. Dynamics of soil microbial communities following vegetation succession in a karst mountain ecosystem, Southwest China. Southwest China. 9, 2160

[68] Zhao, F.Z., Bai, L., Wang, J.Y., Deng, J., Ren, C.J., Han, X.H., Yang, G.H., Wang, J., 2019. Change in soil bacterial community during secondary succession depend on plant soil characteristics. Catena 173, 246–252

[69] Zhu, G.Y., Tang, Z.S., Shangguan, Z.P., Peng, C.H., Deng, L., 2019. Factors affecting the spatial and temporal variations in soil erodibility of China. Journal of Geophysical Research. Earth Surface 124, 737–749

[70] Zou, H.Y., Guan, X.Q., 1997. Approach to management path way of Yun Wushan mountain natural protecting area. Caoye Kexue 14, 1–2 (Chinese with English Abstract).

Acknowledgements

This study was supported by the National Natural Sciences Foundation of China (41807060, 41977061), National Special Research and Development Project during the Thirty Five-year Plan Period (2017YFC0504702).

RIGHTS & PERMISSIONS

2020 Higher Education Press