Assembly process and source tracking of microbial communities in sediments of Dongting Lake

Highlights

● Soil erosion resulted in homogenization of bacterial communities in the watershed.

● Microbial community heterogeneity among erosion sites made soil tracing possible.

● Assembly process results showed that the tracking results can achieve high precision.

● Dryland was the main source of sediment deposition based on the result of FEAST.

Abstract

Sediment source tracing can accurately provide a theoretical basis for controlling soil erosion effectively, by identifying the most serious types of land use. Traditional sediment tracing methods are based on physical, chemical, biological, and composite fingerprinting, which have not included microbes. As high-throughput sequencing becomes more prevalent, microorganisms can provide more information than what we think. Thus, whether the microorganism can also be used as a special fingerprint factor for sediment source identification during soil erosion, we have tested it by using microbial source tracking tool FEAST to quantify the microbe contribution from five types of eroded land (including dryland, urban, paddy field, forest and grassland) to the depositional areas (Niubitan) in the Yuanjiang basin. The source microbial community in the erosive area was heterogeneous, and assembly process analysis further demonstrated that the source tracking results could reach higher accuracy. The results of FEAST showed that dryland (35.50%), urban (17.21%), paddy field (8.14%), and forest (1.07%) were the major contributors to Niubitan. Our results follow the general soil erosion rules and prove its validity. Taken together, a new perspective is provided by these results for tracing sediment sources in erosion-sedimentary systems.

Graphical abstract

Keywords

assembly processes / soil erosion / land types / microbial source tracking / FEAST

References

[1] Bamshad, M.J., Ng, S.B., Bigham, A.W., Tabor, H.K., Emond, M.J., Nickerson, D.A., Shendure, J., 2011. Exome sequencing as a tool for Mendelian disease gene discovery. Nature Reviews Genetics12, 745–755.

[2] Borrelli, P., Robinson, D.A., Fleischer, L.R., Lugato, E., Ballabio, C., Alewell, C., Meusburger, K., Modugno, S., Schutt, B., Ferro, V., Bagarello, V., Van Oost, K., Montanarella, L., Panagos, P., 2017. An assessment of the global impact of 21st century land use change on soil erosion. Nature Communications8, 2013.

[3] Chen, S.K., Chen, R.S., Yang, T.Y., 2014. Application of a tank model to assess the flood-control function of a terraced paddy field. Hydrological Sciences Journal59, 1020–1031.

[4] Chen, S.K., Chen, Y.R., Peng, Y.H., 2013. Experimental study on soil erosion characteristics in flooded terraced paddy fields. Paddy and Water Environment11, 433–444.

[5] Clark, H.M., Hartwich, R.B., 2001. A re-examination of the ‘particle size effect’ in slurry erosion. Wear248, 147–161.

[6] Collins, A.L., Walling, D.E., Leeks, G.J.L., 1997. Source type ascription for fluvial suspended sediment based on a quantitative composite fingerprinting technique. Catena29, 1–27.

[7] den Biggelaar, C., Lal, R., Wiebe, K., Breneman, V., 2003. The global impact of soil erosion on productivity: I: Absolute and relative erosion-induced yield losses. Advances in Agronomy81, 1–48.

[8] Droppo, I.G., 2001. Rethinking what constitutes suspended sediment. Hydrological Processes15, 1551–1564.

[9] Fang, X.H., Peng, B., Zhang, K., Zeng, D.Z., Kuang, X.L., Wu, B.J., Tu, X.L., Song, Z.L., Xiao, Y., Yang, Z.X., Xie, W.C., Bao, Z.C., Tan, C.Y., Wang, X., Wan, D.J., 2018. Geochemistry of major and trace elements in sediments from inlets of the Xiangjiang and Yuanjiang River to Dongting Lake, China. Environmental Earth Sciences77, 16.

[10] Fargione, J., Brown, C.S., Tilman, D., 2003. Community assembly and invasion: An experimental test of neutral versus niche processes. Proceedings of the National Academy of Sciences of the United States of America100, 8916–8920.

[11] Gibbs, M.M., 2008. Identifying source soils in contemporary estuarine sediments: A new compound-specific isotope method. Estuaries and Coasts31, 344–359.

[12] Guo, Z.W., Xiao, X.M., Gan, Y.L., Zheng, Y.J., 2001. Ecosystem functions, services and their values−a case study in Xingshan County of China. Ecological Economics38, 141–154.

[13] Han, Z.M., An, W., Yang, M., Zhang, Y., 2020. Assessing the impact of source water on tap water bacterial communities in 46 drinking water supply systems in China. Water Research172, 115469.

[14] Huang, J.Q., Li, Z.W., Zeng, G.M., Zhang, J.C., Li, J.B., Nie, X.D., Ma, W.M., Zhang, X., 2013. Microbial responses to simulated water erosion in relation to organic carbon dynamics on a hilly cropland in subtropical China. Ecological Engineering60, 67–75.

[15] Jiao, S., Chen, W.M., Wang, J.L., Du, N.N., Li, Q.P., Wei, G.H., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome6, 146.

[16] Kircher, M., Kelso, J., 2010. High-throughput DNA sequencing−concepts and limitations. BioEssays32, 524–536.

[17] Knights, D., Kuczynski, J., Charlson, E.S., Zaneveld, J., Mozer, M.C., Collman, R.G., Bushman, F.D., Knight, R., Kelley, S.T., 2011. Bayesian community-wide culture-independent microbial source tracking. Nature Methods8, 761–U107.

[18] Lal, R., Pimentel, D 2008. Soil erosion: A carbon sink or source?. Science319, 1040–1042.

[19] Liao, W.F., Tong, D., Li, Z.W., Nie, X.D., Liu, Y.J., Ran, F.W., Liao, S.S., 2021. Characteristics of microbial community composition and its relationship with carbon, nitrogen and sulfur in sediments. Science of the Total Environment795, 148848.

[20] Liu, C.S., Zhao, D.F., Ma, W.J., Guo, Y.D., Wang, A.J., Wang, Q.L., Lee, D.J., 2016. Denitrifying sulfide removal process on high-salinity wastewaters in the presence of Halomonas sp. Applied Microbiology and Biotechnology100, 1421–1426.

[21] Liu, N.N., Hu, H.F., Ma, W.H., Deng, Y., Wang, Q.G., Luo, A., Meng, J.H., Feng, X.J., Wang, Z.H., 2021. Relative importance of deterministic and stochastic processes on soil microbial community assembly in temperate grasslands. Microorganisms9, 1929.

[22] Ma, W.M., Li, Z.W., Ding, K.Y., Huang, B., Nie, X.D., Lu, Y.M., Xiao, H.B., Zeng, G.M., 2016. Stability of soil organic carbon and potential carbon sequestration at eroding and deposition sites. Journal of Soils and Sediments16, 1705–1717.

[23] Malhotra, K., Lamba, J., Shepherd, S., 2020. Sources of stream bed sediment in an urbanized watershed. Catena184, 104228.

[24] Nguyen, V.B., Nguyen, Q.B., Zhang, Y.W., Lim, C.Y.H., Khoo, B.C., 2016. Effect of particle size on erosion characteristics. Wear348, 126–137.

[25] Nosrati, K., Govers, G., Ahmadi, H., Sharifi, F., Amoozegar, M.A., Merckx, R., Vanmaercke, M. 2011. An exploratory study on the use of enzyme activities as sediment tracers: biochemical fingerprints?. International Journal of Sediment Research26, 136–151.

[26] Pimentel, D., Harvey, C., Resosudarmo, P., Sinclair, K., Kurz, D., McNair, M., Crist, S., Shpritz, L., Fitton, L., Saffouri, R., Blair, R., 1995. Environmental and economic costs of soil erosion and conservation benefits. Science267, 1117–1123.

[27] Pulley, S., Foster, I., Antunes, P., 2015. The uncertainties associated with sediment fingerprinting suspended and recently deposited fluvial sediment in the Nene river basin. Geomorphology228, 303–319.

[28] Qi, Y.Z., Li, Y.P., Xie, W.W., Lu, R., Mu, F.F., Bai, W.Y., Du, S.L., 2020. Temporal-spatial variations of fungal composition in PM2.5 and source tracking of airborne fungi in mountainous and urban regions. Science of the Total Environment708, 135027.

[29] Ran, F.W., Nie, X.D., Li, Z.W., Xiao, L.H., Sun, Y.Z., Wang, S.L., Liao, W.F., Tong, D., Li, Z.T., Peng, Y.J., 2021. Chronological records of sediment organic carbon at an entrance of Dongting Lake: Response to historical meteorological events. Science of the Total Environment794, 148801.

[30] Ravi, S., Breshears, D.D., Huxman, T.E., D’Odorico, P., 2010. Land degradation in drylands: Interactions among hydrologic-aeolian erosion and vegetation dynamics. Geomorphology116, 236–245.

[31] Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., Weber, C.F., 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology75, 7537–7541.

[32] Shenhav, L., Thompson, M., Joseph, T.A., Briscoe, L., Furman, O., Bogumil, D., Mizrahi, I., Pe’er, I., Halperin, E., 2019. FEAST: fast expectation-maximization for microbial source tracking. Nature Methods16, 627–632.

[33] Smith, R.W., Bianchi, T.S., Allison, M., Savage, C., Galy, V., 2015. High rates of organic carbon burial in fjord sediments globally. Nature Geoscience8, 450–U446.

[34] Stegen, J.C., Lin, X.J., Fredrickson, J.K., Chen, X.Y., Kennedy, D.W., Murray, C.J., Rockhold, M.L., Konopka, A., 2013. Quantifying community assembly processes and identifying features that impose them. ISME Journal7, 2069–2079.

[35] Stegen, J.C., Lin, X.J., Fredrickson, J.K., Konopka, A.E., 2015. Estimating and mapping ecological processes influencing microbial community assembly. Frontiers in Microbiology6, 370.

[36] Vale, S.S., Fuller, I.C., Procter, J.N., Basher, L.R., Smith, I.E., 2016. Characterization and quantification of suspended sediment sources to the Manawatu River, New Zealand. Science of the Total Environment543, 171–186.

[37] Van Oost, K., Quine, T.A., Govers, G., De Gryze, S., Six, J., Harden, J.W., Ritchie, J.C., McCarty, G.W., Heckrath, G., Kosmas, C., Giraldez, J.V., da Silva, J.R.M., Merckx, R., 2007. The impact of agricultural soil erosion on the global carbon cycle. Science318, 626–629.

[38] Vercruysse, K., Grabowski, R.C., 2018. Using source-specific models to test the impact of sediment source classification on sediment fingerprinting. Hydrological Processes32, 3402–3415.

[39] Vercruysse, K., Grabowski, R.C., Rickson, R.J., 2017. Suspended sediment transport dynamics in rivers: Multi-scale drivers of temporal variation. Earth-Science Reviews166, 38–52.

[40] Walling, D.E., 2005. Tracing suspended sediment sources in catchments and river systems. Science of the Total Environment344, 159–184.

[41] Wu, H.P., Hu, X.Y., Sun, S.Q., Dai, J., Ye, S.J., Du, C.Y., Chen, H., Yu, G.L., Zhou, L., Chen, J., 2020. Effect of increasing of water level during the middle of dry season on landscape pattern of the two largest freshwater lakes of China. Ecological Indicators113, 106283.

[42] Xiao, H.B., Li, Z.W., Chang, X.F., Huang, J.Q., Nie, X.D., Liu, C., Liu, L., Wang, D.Y., Dong, Y.T., Jiang, J.Y., 2017. Soil erosion-related dynamics of soil bacterial communities and microbial respiration. Applied Soil Ecology119, 205–213.

[43] Yang, T., Shi, Y., Zhu, J., Zhao, C., Wang, J.M., Liu, Z.Y., Fu, X., Liu, X., Yan, J.W., Yuan, M.Q., Chu, H.Y., 2021. The spatial variation of soil bacterial community assembly processes affects the accuracy of source tracking in ten major Chinese cities. Science China Life Sciences64, 1546–1559.

[44] Yang, X.H., Ci, L.J., Zhang, X.S., 2008. Dryland characteristics and its optimized eco-productive paradigms for sustainable development in China. Natural Resources Forum32, 215–227.

[45] Yuan, Y.J., Zeng, G.M., Liang, J., Huang, L., Hua, S.S., Li, F., Zhu, Y., Wu, H.P., Liu, J.Y., He, X.X., He, Y., 2015. Variation of water level in Dongting Lake over a 50-year period: Implications for the impacts of anthropogenic and climatic factors. Journal of Hydrology (Amsterdam)525, 450–456.

[46] Zha, Y.G., Chong, H., Qiu, H., Kang, K., Dun, Y., Chen, Z.X., Cui, X.F., Ning, K., 2022. Ontology-aware deep learning enables ultrafast and interpretable source tracking among sub-million microbial community samples from hundreds of niches. Genome Medicine14, 43.

[47] Zhang, W.L., Gu, J.F., Li, Y., Lin, L., Wang, P.F., Wang, C., Qian, B., Wang, H.L., Niu, L.H., Wang, L.F., Zhang, H.J., Gao, Y., Zhu, M.J., Fang, S.Q., 2019. New insights into sediment transport in interconnected river-lake systems through tracing microorganisms. Environmental Science & Technology53, 4099–4108.

[48] Zheng, X.L., Chen, L.H., Gong, W.Y., Yang, X., Kang, Y.L., 2019. Evaluation of the water conservation function of different forest types in northeastern China. Sustainability (Basel)11, 4075.

[49] Zhou, J.Z., Ning, D.L. 2017. Stochastic community assembly: Does it matter in microbial ecology?. Microbiology and Molecular Biology Reviews81, e00002-17.

Acknowledgements

The National Natural Science Foundation of China provided funding for this project (U19A2047).

Compliance with ethical standards

The authors declare that they have no financial or other conflicts of interest.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-023-0173-7 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press