Microscale heterogeneity of soil bacterial communities under long-term fertilizations in fluvo-aquic soils

Haojie Feng, Hong Pan, Chengliang Li, Yuping Zhuge

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Soil Ecology Letters ›› 2022, Vol. 4 ›› Issue (4) : 337-347. DOI: 10.1007/s42832-021-0121-3
RESEARCH ARTICLE
RESEARCH ARTICLE

Microscale heterogeneity of soil bacterial communities under long-term fertilizations in fluvo-aquic soils

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Highlights

• Both organic and inorganic fertilizations stimulate soil aggregation.

• Organic and inorganic fertilizers enhance organic carbon storage at aggregate scale.

• Aggregate-associated bacterial communities were more sensitive to organic fertilizers than to chemical ones.

• The complexity of bacterial network structures decreased with decreasing of aggregate size.

• The competitive interactions among bacterial communities were intensified with decreasing of aggregate size.

Abstract

Differently sized soil aggregates, with non-uniform distribution of space and nutrients, provide spatially heterogeneous microenvironments for microorganisms and are important for controlling microbial community ecology and biogeochemistry in soils. Here, we investigated the prokaryotic communities within different aggregate-size fractions: macroaggregate (>0.25 mm), microaggregate (0.053–0.25 mm) and silt+ clay (<0.053 mm). These were isolated from fluvo-aquic soils under 39-year fertilization strategies: no fertilizer (CK), chemical fertilizer (NPK), manure fertilizer (M), and combination of manure and chemical fertilizers (MNPK). The results showed that the proportion of macroaggregate, soil aggregate-associated organic carbon (SOC) content and aggregate stability were all significantly increased by both manure and chemical fertilizations. Organic fertilizations (M and MNPK) more effectively boosted formation and stability of macroaggregates and enhanced SOC concentration than NPK. The distribution patterns of microorganisms in aggregates were primarily shaped by fertilization and aggregate size. They explained 76.9% of the variance in bacterial community compositions. Fertilizations, especially with organic fertilizers primarily transitioned bacterial communities from slow-growing oligotrophic groups (e.g., Chloroflexi) dominance to fast-growing copiotrophic groups (e.g., Proteobacteria and Bacteroidetes) dominance across all aggregate sizes. Macroaggregates possessed a more stable bacterial community and efficiency of resource transfer, while smaller aggregates increased antagonism and weakened mutualism among bacterial communities. Overall, combination of manure and chemical fertilizers was crucial for increasing SOC content and aggregation, leading to a clear shift in bacterial community structures at aggregate scale.

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Keywords

Bacterial community / Soil aggregate / Long-term fertilization / Soil organic carbon (SOC)

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Haojie Feng, Hong Pan, Chengliang Li, Yuping Zhuge. Microscale heterogeneity of soil bacterial communities under long-term fertilizations in fluvo-aquic soils. Soil Ecology Letters, 2022, 4(4): 337‒347 https://doi.org/10.1007/s42832-021-0121-3

References

[1]
Ashagrie, Y., Zech, W., Guggenberger, G., Mamo, T., 2007. Soil aggregation, and total and particulate organic matter following conversion of native forests to continuous cultivation in Ethiopia. Soil & Tillage Research 94, 101–108
CrossRef Google scholar
[2]
Bailey, V.L., Fansler, S.J., Stegen, J.C., McCue, L.A., 2013. Linking microbial community structure to β-glucosidic function in soil aggregates. ISME Journal 7, 2044–2053
CrossRef Google scholar
[3]
Banerjee, S., Schlaeppi, K., van der Heijden, M.G., 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews. Microbiology 16, 567–576
CrossRef Google scholar
[4]
Bastian, M., Heymann, S., Jacomy, M., 2009. Gephi: an open source software for exploring and manipulating networks. Third International ICWSM Conference, 361–362.
[5]
Biederbeck, V.O., Curtin, D., Bouman, O.T., Campbell, C.A., Ukrainetz, H., 1996. Soil microbial and biochemical properties after ten years of fertilization with urea and anhydrous ammonia. Canadian Journal of Soil Science 76, 7–14
CrossRef Google scholar
[6]
Blanco‐Canqui, H., Schlegel, A.J., 2013. Implications of inorganic fertilization of irrigated corn on soil properties: Lessons learned after 50 years. Journal of Environmental Quality 42, 861–871
CrossRef Google scholar
[7]
Bottinelli, N., Angers, D.A., Hallaire, V., Michot, D., Le Guillou, C., Cluzeau, D., Heddadj, D., Menasseri-Aubry, S., 2017. Tillage and fertilization practices affect soil aggregate stability in a Humic Cambisol of Northwest France. Soil & Tillage Research 170, 14–17
CrossRef Google scholar
[8]
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 fractions and farm management systems. Soil Biology & Biochemistry 43, 905–914
CrossRef Google scholar
[9]
Crouzet, O., Consentino, L., Pétraud, J.P., Marrauld, C., Aguer, J.P., Bureau, S., Le Bourvellec, C.,Touloumet, L., Berard A., , 2019. Soil photosynthetic microbial communities mediate aggregate stability: influence of cropping systems and herbicide use in an agricultural soil. Frontiers in Microbiology 10, 1319
CrossRef Google scholar
[10]
DeBruyn, J. M., Nixon, L. T., Fawaz, M. N., Johnson, A. M., & Radosevich, M., 2011. Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Applied and Environmental Microbiology 77, 6295–6300 doi: 10.1128/AEM.05005-11
[11]
Dai, H., Zang, H., Zhao, Y., Qian, X., Liu, K., Wang, D., Hao, J., Chen, Y., Sui, P., 2019. Linking bacterial community to aggregate fractions with organic amendments in a sandy soil. Land Degradation & Development 30, 1828–1839
CrossRef Google scholar
[12]
DeBruyn, J.M., Nixon, L.T., Fawaz, M.N., Johnson, A.M., Radosevich, M., 2011. Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Applied and Environmental Microbiology 77, 6295–6300
CrossRef Google scholar
[13]
Ding, X., Han, X., 2014. Effects of long-term fertilization on contents and distribution of microbial residues within aggregate structures of a clay soil. Biology and Fertility of Soils 50, 549–554
CrossRef Google scholar
[14]
Elliott, E.T., 1986. Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50, 627–633
CrossRef Google scholar
[15]
Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews. Microbiology 15, 579–590
CrossRef Google scholar
[16]
Feng, H., Wang, S., Gao, Z., Wang, Z., Ren, X., Hu, S., & Pan, H., 2019. Effect of land use on the composition of bacterial and fungal communities in saline–sodic soils. Land Degradation & Development 30, 1851–1860 doi: 10.1002/ldr.3386
[17]
Garbout, A., Munkholm, L. J., & Hansen, S. B., 2013. Tillage effects on topsoil structural quality assessed using X-ray CT, soil cores and visual soil evaluation. Soil and Tillage Research 128, 104–109 doi: 10.1016/j.still.2012.11.003
[18]
Ghosh, B.N., Meena, V.S., Singh, R.J., Alam, N.M., Patra, S., Bhattacharyya, R., Sharma, N.K., Dadhwal, K.S., Mishra, P.K., 2019. Effects of fertilization on soil aggregation, carbon distribution and carbon management index of maize-wheat rotation in the north-western Indian Himalayas. Ecological Indicators 105, 415–424
CrossRef Google scholar
[19]
Guo, T., Zhang, Q., Ai, C., He, P., Zhou, W., 2021. Microbial utilization of rice root residue‐derived carbon explored by DNA stable‐isotope probing. European Journal of Soil Science 72, 460–473
CrossRef Google scholar
[20]
Gupta, V.V., Germida, J.J., 2015. Soil aggregation: Influence on microbial biomass and implications for biological processes. Soil Biology & Biochemistry 80, A3–A9
CrossRef Google scholar
[21]
Han, S., Delgado-Baquerizo, M., Luo, X., Liu, Y., Van Nostrand, J.D., Chen, W., Zhou, J., Huang, Q., 2021. Soil aggregate size-dependent relationships between microbial functional diversity and multifunctionality. Soil Biology & Biochemistry 154, 108143
CrossRef Google scholar
[22]
Han, S., Luo, X., Hao, X., Ouyang, Y., Zeng, L., Wang, L., Wen, S., Wang, B., Van Nostrand, J.D., Chen, W., Zhou, J., Huang, Q., 2020. Microscale heterogeneity of the soil nitrogen cycling microbial functional structure and potential metabolism. Environmental Microbiology 23, 1199–1209 doi: 10.1111/1462-2920.15348.
[23]
Han, S., Xiong, X., Luo, X., Zeng, L., Wei, D., Chen, W., Huang, Q., 2018. Fertilization rather than aggregate size fractions shape the nitrite-oxidizing microbial community in a Mollisol. Soil Biology & Biochemistry 124, 179–183
CrossRef Google scholar
[24]
He, Y., Xu, C., Gu, F., Wang, Y., Chen, J., 2018a. Soil aggregate stability improves greatly in response to soil water dynamics under natural rains in long-term organic fertilization. Soil & Tillage Research 184, 281–290
CrossRef Google scholar
[25]
He, Y.T., He, X.H., Xu, M.G., Zhang, W.J., Yang, X.Y., Huang, S.M., 2018b. Long-term fertilization increases soil organic carbon and alters its chemical composition in three wheat-maize cropping sites across central and south China. Soil & Tillage Research 177, 79–87
CrossRef Google scholar
[26]
He, Y.T., Zhang, W.J., Xu, M.G., Tong, X.G., Sun, F.X., Wang, J.Z., Huang, S.M., Zhu, P., He, X.H., 2015. Long-term combined chemical and manure fertilizations increase soil organic carbon and total nitrogen in aggregate fractions at three typical cropland soils in China. Science of the Total Environment 532, 635–644
CrossRef Google scholar
[27]
Janssen, P.H., 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Applied and Environmental Microbiology 72, 1719–1728
CrossRef Google scholar
[28]
Jiang, M., Wang, X., Liusui, Y., Han, C., Zhao, C., Liu, H., 2017. Variation of soil aggregation and intra-aggregate carbon by long-term fertilization with aggregate formation in a grey desert soil. Catena 149, 437–445
CrossRef Google scholar
[29]
Jiang, Y., Jin, C., Sun, B., 2014. Soil aggregate stratification of nematodes and ammonia oxidizers affects nitrification in an acid soil. Environmental Microbiology 16, 3083–3094
CrossRef Google scholar
[30]
Jiang, Y., Sun, B., Jin, C., Wang, F., 2013. Soil aggregate stratification of nematodes and microbial communities affects the metabolic quotient in an acid soil. Soil Biology & Biochemistry 60, 1–9
CrossRef Google scholar
[31]
Li, F., Chen, L., Zhang, J., Yin, J., Huang, S., 2017. Bacterial community structure after long-term organic and inorganic fertilization reveals important associations between soil nutrients and specific taxa involved in nutrient transformations. Frontiers in Microbiology 8, 1-12
CrossRef Google scholar
[32]
Li, P.P., Han, Y.L., He, J.Z., Zhang, S.Q., Zhang, L.M., 2019. Soil aggregate size and long-term fertilization effects on the function and community of ammonia oxidizers. Geoderma 338, 107–117
CrossRef Google scholar
[33]
Liao, H., Zhang, Y., Wang, K., Hao, X., Chen, W., Huang, Q., 2020. Complexity of bacterial and fungal network increases with soil aggregate size in an agricultural Inceptisol. Applied Soil Ecology 154, 103640
CrossRef Google scholar
[34]
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
CrossRef Google scholar
[35]
Lin, Y., Ye, G., Kuzyakov, Y., Liu, D., Fan, J., Ding, W., 2019. Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biology & Biochemistry 134, 187–196
CrossRef Google scholar
[36]
Liu, M., Wang, C., Liu, X., Lu, Y., Wang, Y., 2020. Saline-alkali soil applied with vermicompost and humic acid fertilizer improved macroaggregate microstructure to enhance salt leaching and inhibit nitrogen losses. Applied Soil Ecology 156, 103705
CrossRef Google scholar
[37]
Morriën, E., Hannula, S.E., Snoek, L.B., Helmsing, N.R., Zweers, H., De Hollander, M., Soto, R.L., Bouffaud, M.L., Buée, M., Dimmers, W., Duyts, H., Geisen, S., Girlanda, M., Griffiths, R.I., Jørgensen, H.B., Jensen, J., Plassart, P., Redecker, D., Schmelz, R.M., Schmidt, O., Thomson, B.C., Tisserant, E., Uroz, S., Winding, A., Bailey, M.J., Bonkowski, M., Faber, J.H., Martin, F., Lemanceau, P., , de Boer, W. van Veen, J.A., van der PuttenW.H., , 2017. Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Communications 8, 14349
CrossRef Google scholar
[38]
Mougi, A., Kondoh, M., 2012. Diversity of interaction types and ecological community stability. Science 337, 349–351
CrossRef Google scholar
[39]
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
CrossRef Google scholar
[40]
Maillard, É., Angers, D. A., Chantigny, M., Bittman, S., Rochette, P., Lévesque, G., Hunt, D., Parent, L. É., 2015. Carbon accumulates in organo-mineral complexes after long-term liquid dairy manure application. Agriculture, Ecosystems & Environment 202, 108–119 doi: 10.1016/j.agee.2014.12.013
[41]
Mustafa, A., Minggang, X., Ali Shah, S.A., Abrar, M.M., Nan, S., Baoren, W., Zejiang, C., Saeed, Q., Naveed, M., Mehmood, K., Núñez-Delgado, A., 2020. Soil aggregation and soil aggregate stability regulate organic carbon and nitrogen storage in a red soil of southern China. Journal of Environmental Management 270, 110894
CrossRef Google scholar
[42]
Neutel, A.M., Heesterbeek, J.A.P., Van De Koppel, J., Hoenderboom, G., Vos, A., Kaldeway, C., Berendse, F., De Ruiter, P.C., 2007. Reconciling complexity with stability in naturally assembling food webs. Nature 449, 599–602
CrossRef Google scholar
[43]
Pan, H., Chen, M., Feng, H., Wei, M., Song, F., Lou, Y., Cui, X., Wang, H., Zhuge, Y., 2020. Organic and inorganic fertilizers respectively drive bacterial and fungal community compositions in a fluvo-aquic soil in northern China. Soil & Tillage Research 198, 104540
CrossRef Google scholar
[44]
Rillig, M.C., Muller, L.A., Lehmann, A., 2017. Soil aggregates as massively concurrent evolutionary incubators. ISME Journal 11, 1943–1948
CrossRef Google scholar
[45]
Sainju, U.M., 2006. Carbon and nitrogen pools in soil aggregates separated by dry and wet sieving methods. Soil Science 171, 937–949
CrossRef Google scholar
[46]
Schellenberger, S., Kolb, S., Drake, H.L., 2010. Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen. Environmental Microbiology 12, 845–861
CrossRef Google scholar
[47]
Six, J., Elliott, E.T., Paustian, K., 1999. Aggregate and soil organic matter dynamics under conventional and no‐tillage systems. Soil Science Society of America Journal 63, 1350–1358
CrossRef Google scholar
[48]
Six, J., Elliott, E.T., Paustian, K., 2000. Soil structure and soil organic matter II. A normalized stability index and the effect of mineralogy. Soil Science Society of America Journal 64, 1042–1049
CrossRef Google scholar
[49]
Stone, D.L., Whitney, D., Janssen, K.A., Long, J.H., 1991. Soil properties after twenty years of fertilization with different nitrogen sources. Soil Science Society of America Journal 55, 1097–1100
CrossRef Google scholar
[50]
Tiemann, L.K., Grandy, A.S., Atkinson, E.E., Marin‐Spiotta, E., McDaniel M.D., 2015. Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecology Letters 18, 761–771
CrossRef Google scholar
[51]
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
CrossRef Google scholar
[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
CrossRef Google scholar
[53]
Wang, C., Dong, D., Wang, H., Müller, K., Qin, Y., Wang, H., Wu, W., 2016. Metagenomic analysis of microbial consortia enriched from compost: new insights into the role of Actinobacteria in lignocellulose decomposition. Biotechnology for Biofuels 29, 22
CrossRef Google scholar
[54]
Wang, M.C., Yang, C.H., 2003. Type of fertilizer applied to a paddy–upland rotation affects selected soil quality attributes. Geoderma 114, 93–108
CrossRef Google scholar
[55]
Wang, X., Bian, Q., Jiang, Y., Zhu, L., Chen, Y., Liang, Y., Sun, B., 2021. Organic amendments drive shifts in microbial community structure and keystone taxa which increase C mineralization across aggregate size classes. Soil Biology & Biochemistry 153, 108062
CrossRef Google scholar
[56]
Whalen, J.K., Chang, C., 2002. Macroaggregate characteristics in cultivated soils after 25 annual manure applications. Soil Science Society of America Journal 66, 1637–1647
CrossRef Google scholar
[57]
Will, C., Thürmer, A., Wollherr, A., Nacke, H., Herold, N., Schrumpf, M., Gutknecht, J., Wubet, T., Buscot, F., Daniel, R., 2010. Horizon-specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Applied and Environmental Microbiology 76, 6751–6759
CrossRef Google scholar
[58]
Wolińska, A., Kuźniar, A., Zielenkiewicz, U., Izak, D., Szafranek-Nakonieczna, A., Banach, A., Błaszczyk, M., 2017. Bacteroidetes as a sensitive biological indicator of agricultural soil usage revealed by a culture-independent approach. Applied Soil Ecology 119, 128–137
CrossRef Google scholar
[59]
Xun, W., Zhao, J., Xue, C., Zhang, G., Ran, W., Wang, B., Shen, Q., Zhang, R., 2016. Significant alteration of soil bacterial communities and organic carbon decomposition by different long‐term fertilization management conditions of extremely low‐productivity arable soil in South China. Environmental Microbiology 18, 1907–1917
CrossRef Google scholar
[60]
Yang, Z., Singh, B.R., Hansen, S., 2007. Aggregate associated carbon, nitrogen and sulfur and their ratios in long-term fertilized soils. Soil & Tillage Research 95, 161–171
CrossRef Google scholar
[61]
Young, I.M., Crawford, J.W., Nunan, N., Otten, W., Spiers, A., 2008. Microbial distribution in soils: physics and scaling. Advances in Agronomy 100, 81–121
CrossRef Google scholar
[62]
Zhou, H., Peng, X., Perfect, E., Xiao, T., Peng, G., 2013. Effects of organic and inorganic fertilization on soil aggregation in an Ultisol as characterized by synchrotron based X-ray micro-computed tomography. Geoderma 195-196, 23–30. doi:10.1016/j.geoderma.2012.11.003

Acknowledgments

This work was funded by the National Natural Science Foundation of China (42007076), the Shandong Provincial Natural Science Foundation (ZR2020QD116 and ZR2019BD032), the China Postdoctoral Science Foundation (2020T130387 and 2019M652448).

Conflict of interest

The authors declare that they have no conflict of interest.

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