Aggregate sizes regulate the microbial community patterns in sandy soil profile
Yifei Sun, Meiling Sun, Guowei Chen, Xin Chen, Baoguo Li, Gang Wang
Aggregate sizes regulate the microbial community patterns in sandy soil profile
• Relative abundances of microbial communities were most related to aggregate proportions in clay-layer soils.
• Aggregate content with<0.053 mm in clay-layer soil significantly influence the diversity of soil microbial community.
• Complexity of microbial interactions raised along increasing precipitation across sampling sites.
• Competition for substrates induced niche differentiation in deeper soils.
Soil microorganisms play a key role in the function of soil ecosystem, yet our knowledge about how microbial communities respond to the typically sandy soil environmental properties along the soil profile is still insufficient. We investigated the soil microbial community patterns from top (0 – 20 cm) to clay-layer (>80 cm) of the typical sandy soils in three regions in China with different levels of precipitation, including Lishu County in Jilin Province (LS), Langfang City in Hebei Province (LF) and Zhengzhou City in Henan Province (ZZ). Our findings showed that small-size aggregates (<0.5 mm) rather than large ones (>= 0.5 mm) dominated the soil profile. The relative abundances of Actinobacteria, Crenarchaeota and Firmicutes were highly related to aggregate proportions of the deep clay-layer soil. The network analysis revealed the distinct community patterns among modules, evidencing niche differentiation along the soil profile. The keystone species OTU_11292 was observed having migrated clearly into the other module of the clay-layer soil. Different roles of the OTU_30 (belonging to Gemmatimonadetes) in soil processes might partly explain the different microbial distribution between top- and clay-layer soils. These findings provided new insights into the candidate mechanisms of microbial diversity maintenance and community patterning of sandy soils, which were necessary for better understanding of ecological rules guiding long-term agricultural practice.
Aggregate distributions / 16S rRNA / Microbial community / Sandy soil / Network analysis / Soil profile
[1] |
Acosta-Martínez, V., Dowd, S.E., Bell, C.W., Lascano, R., Booker, J.D., Zobeck, T.M., Upchurch, D.R., 2010. Microbial community composition as affected by dryland cropping systems and tillage in a semiarid sandy soil. Diversity (Basel) 2, 910–931
CrossRef
Google scholar
|
[2] |
Allison, S.D., Wallenstein, M.D., Bradford, M.A., 2010. Soil carbon response to warming dependent on microbial physiology. Nature Geoscience 3, 336–340
CrossRef
Google scholar
|
[3] |
Bao, S.D., 2000. Soil and agricultural Chemistry analysis. 3 th ed. Beijing: China Agriculture Press, 226
|
[4] |
Barber, N.A., Chantos‐Davidson, K.M., Amel Peralta, R., SherwoodJ.P., SwingleyW.D., 2017. Soil microbial community composition in tallgrass prairie restorations converge with remnants across a 27‐year chronosequence. Environmental Microbiology 19, 3118–3131
CrossRef
Google scholar
|
[5] |
Bending, G.D., Turner, M.K., Rayns, F., Marx, M.C., Wood, M., 2004. Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biology & Biochemistry 36, 1785–1792
CrossRef
Google scholar
|
[6] |
Blume, E., Bischoff, M., Reichert, J.M., Moorman, T., Konopka, A., Turco, R.F., 2002. Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season. Applied Soil Ecology 20, 171–181
CrossRef
Google scholar
|
[7] |
Bowen, J.L., Morrison, H.G., Hobbie, J.E., Sogin, M.L., 2012. Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME Journal 6, 2014–2023
CrossRef
Google scholar
|
[8] |
Brockett, B.F.T., Prescott, C.E., Grayston, S.J., 2012. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biology & Biochemistry 44, 9–20
CrossRef
Google scholar
|
[9] |
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high–throughput community sequencing data. Nature Methods 7, 335–336
CrossRef
Google scholar
|
[10] |
Castellazzi, M.S., Brookes, P.C., Jenkinson, D.S., 2004. Distribution of microbial biomass down soil profiles under regenerating woodland. Soil Biology & Biochemistry 36, 1485–1489
CrossRef
Google scholar
|
[11] |
Cheng, X., Luo, Y., Xu, X., Sherry, R., Zhang, Q., 2011. Soil organic matter dynamics in a North America tallgrass prairie after 9 yr of experimental warming. Biogeosciences 8, 1487–1498
CrossRef
Google scholar
|
[12] |
Cho, B.C., Jang, G.I., 2014. Active and diverse rainwater bacteria collected at an inland site in spring and summer 2011. Atmospheric Environment 94, 409–416
CrossRef
Google scholar
|
[13] |
Davinic, M., Fultz, L.M., Acosta-Martinez, V., Calderόn, F.J., Cox, S.B., Dowd, S.E., Allen, V.G., ZakJ.C., Moore-Kucera J., 2012. Pyrosequencing and mid–infrared spectroscopy reveal distinct aggregate stratification of soil bacterial communities and organic matter composition. Soil Biology & Biochemistry 46, 63–72
CrossRef
Google scholar
|
[14] |
Deng, Y., He, Z., Xiong, J., Yu, H., Xu, M., Hobbie, S.E., Reich, P.B., Schadt, C.W., Kent, A., Pendall, E., Wallenstein, M., Zhou, J.Z., 2016. Elevated carbon dioxide accelerates the spatial turnover of soil microbial communities. Global Change Biology 22, 957–964
CrossRef
Google scholar
|
[15] |
Deng, Y., He, Z.L., Xu, M.Y., Qin, Y.J., Van Nostrand, J.D., Wu, L.Y., Roe, B.A., Wiley, G., Hobble, S.E., Relch, P.B., Zhou, J.Z., 2012b. Elevated carbon dioxide alters the structure of soil microbial communities. Applied and Environmental Microbiology 78, 2991–2995
CrossRef
Google scholar
|
[16] |
Deng, Y., Jiang, Y.H., Yang, Y.F., He, Z.L., Luo, F., Zhou, J.Z., 2012a. Molecular ecological network analyses. BMC Bioinformatics 13, 113–132
CrossRef
Google scholar
|
[17] |
Drenovsky, R.E., Vo, D., Graham, K.J., Scow, K.M., 2004. Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microbial Ecology 48, 424–430
CrossRef
Google scholar
|
[18] |
Ebrahimi, A., Or, D., 2016. Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model. Global Change Biology 22, 3141–3156
CrossRef
Google scholar
|
[19] |
Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461
CrossRef
Google scholar
|
[20] |
Eilers, K.G., Debenport, S., Anderson, S., Fierer, N., 2012. Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology & Biochemistry 50, 58–65
CrossRef
Google scholar
|
[21] |
Ekelund, F., Ronn, R., Christensen, S., 2001. Distribution with depth of protozoa, bacteria and fungi in soil profiles from three Danish forest sites. Soil Biology & Biochemistry 33, 475–481
CrossRef
Google scholar
|
[22] |
Fierer, N., Schimel, J.P., Holden, P.A., 2003. Variations in microbial community composition through two soil depth profiles. Soil Biology & Biochemistry 35, 167–176
CrossRef
Google scholar
|
[23] |
Fisher, C.K., Mehta, P., 2014. Identifying keystone species in the human gut microbiome from metagenomic timeseries using sparse linear regression. PLoS One 9, e102451
CrossRef
Google scholar
|
[24] |
Fritze, H., Pietikainen, J., Pennanen, T., 2000. Distribution of microbial biomass and phospholipid fatty acids in Podzol profiles under coniferous forest. European Journal of Soil Science 51, 565–573
CrossRef
Google scholar
|
[25] |
Jiang, Y.J., Liu, M.Q., Zhang, J.B., Chen, Y., Chen, X.Y., Chen, L.J., Li, H.X., Zhang, X.X., Sun, B., 2017. Nematode grazing promotes bacterial community dynamics in soil at the aggregate level. ISME Journal 11, 2705–2717
CrossRef
Google scholar
|
[26] |
Kandeler, E., Marschner, P., Tscherko, D., Gahoonia, T.S., Nielsen, N.E., 2002. Microbial community composition and functional diversity in the rhizosphere of maize. Plant and Soil 238, 301–312
CrossRef
Google scholar
|
[27] |
Kramer, S., Marhan, S., Haslwimmer, H., Ruess, L., Kandeler, E., 2013. Temporal variation in surface and subsoil abundance and function of the soil microbial community in an arable soil. Soil Biology & Biochemistry 61, 76–85
CrossRef
Google scholar
|
[28] |
Langille, M.G.I., Zaneveld, J., Caporaso, J.G., McDonald, D., Knights, D., Reyes, J.A., Clemente, J.C., Burkepile, D.E., Thurber, R.L.V., Knight, R., Beiko, R.G., Huttenhower, C., 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31, 814–821
CrossRef
Google scholar
|
[29] |
Li, Y.T., Adams, J., Shi, Y., Wang, H., He, J.S., Chu, H.Y., 2017. Distinct soil microbial communities in habitats of differing soil water balance on the Tibetan Plateau. Scientific Reports 7, 46407
CrossRef
Google scholar
|
[30] |
Long, T., Or, D., 2005. Aquatic habitats and diffusion constraints affecting microbial coexistence in unsaturated porous media. Water Resources Research 41, 2453–2454
CrossRef
Google scholar
|
[31] |
Louca, S., Parfrey, L.W., Doebeli, M., 2016. Decoupling function and taxonomy in the global ocean microbiome. Science 353, 1272–1277
CrossRef
Google scholar
|
[32] |
Ma, B., Wang, H.Z., Dsouza, M., Lou, J., He, Y., Dai, Z.M., Brookes, P.C., Xu, J.M., Gilbert, J.A., 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME Journal 10, 1891–1901
CrossRef
Google scholar
|
[33] |
Mandiola, M., Studdert, G.A., Domínguez, G.F., Videla, C.C., 2011. Organic matter distribution in aggregate sizes of a mollisol under contrasting managements. Journal of Soil Science and Plant Nutrition 11, 47–57
CrossRef
Google scholar
|
[34] |
Marschner, P., Kandeler, E., Marschner, B., 2003. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biology & Biochemistry 35, 453–461
CrossRef
Google scholar
|
[35] |
Martirosyan, V., Ehrlich, R., Frend, Y., Barness, G., Steinberger, Y., 2013. Spatial heterogeneity of a microbial community in a sandy soil ecosystem. Pedobiologia 56, 195–203
CrossRef
Google scholar
|
[36] |
Mummey, D.L., Rillig, M.C., Six, J., 2006. Endogeic earthworms differentially influence bacterial communities associated with different soil aggregate size fractions. Soil Biology & Biochemistry 38, 1608–1614
CrossRef
Google scholar
|
[37] |
Nelson, D.W., Sommers, L.E., 1982. Total carbon, organic carbon, and organic matter. In: Page, A.L., Miller, R.H., Keenay, D.R., eds. Methods of Soil Analysis. 2nd ed. ASA and SSSA, Madison: WI., 539–580.
|
[38] |
Nie, M., Pendall, E., Bell, C., Wallenstein, M.D., 2014. Soil aggregate size distribution mediates microbial climate change feedbacks. Soil Biology & Biochemistry 68, 357–365
CrossRef
Google scholar
|
[39] |
Or, D., Smets, B.F., Wraith, J.M., Dechesne, A., Friedman, S.P., 2007. Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review. Advances in Water Resources 30, 1505–1527
CrossRef
Google scholar
|
[40] |
Petersen, C.T., Hansen, E., Larsen, H.H., Hansen, L.V., Hauggaard-Nielsen, H., 2016. Pore-size distribution and compressibility of coarse sandy subsoil with added biochar: physical properties of sand with added biochar. European Journal of Soil Science 67, 726–736
CrossRef
Google scholar
|
[41] |
Qin, S.P., Hu, C.S., He, X.H., Dong, W.X., Cui, J.F., Wang, Y., 2010. Soil organic carbon, nutrients and relevant enzyme activities in particle-size fractions under conservational versus traditional agricultural management. Applied Soil Ecology 45, 152–159
CrossRef
Google scholar
|
[42] |
Sanesi, G., Certini, G., 2005. The umbric epipedon in the N Apennines, Italy–an example from the Vallombrosa Forest. Journal of Soil Science and Plant Nutrition 168, 392–398
CrossRef
Google scholar
|
[43] |
Six, J., Bossuyt, H., Degryze, S., Denef, K., 2004. A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil & Tillage Research 79, 7–31
CrossRef
Google scholar
|
[44] |
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
|
[45] |
Smith, A.P., Marín-Spiotta, E., De Graaff, M.A., 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
CrossRef
Google scholar
|
[46] |
Smith, M.D., Knapp, A.K., 2003. Dominant species maintain ecosystem function with non-random species loss. Ecology Letters 6, 509–517
CrossRef
Google scholar
|
[47] |
Sradnick, A., Murugan, R., Oltmanns, M., Raupp, J., Joergensen, R.G., 2013. Changes in functional diversity of the soil microbial community in a heterogeneous sandy soil after long-term fertilization with cattle manure and mineral fertilizer. Applied Soil Ecology 63, 23–28
CrossRef
Google scholar
|
[48] |
Sung, J., Kim, S., Cabatbat, J.J.T., Jang, S., Jin, Y.S., Jung, G.Y., Chia, N., Kim, P.J., 2017. Global metabolic interaction network of the human gut microbiota for context-specific community-scale analysis. Nature Communications 8, 15393
CrossRef
Google scholar
|
[49] |
Trumbore, S., 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 10, 399–411
CrossRef
Google scholar
|
[50] |
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
CrossRef
Google scholar
|
[51] |
Walker, B., Kinzig, A., Langridge, J., 1999. Plant attribute diversity, resilience, and ecosystem function: The nature and significance of dominant and minor species. Ecosystems (New York, N.Y.) 2, 95–113
CrossRef
Google scholar
|
[52] |
Wang, G., Or, D., 2013. Hydration dynamics promote bacterial coexistence on rough surfaces. ISME Journal 7, 395–404
CrossRef
Google scholar
|
[53] |
Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267
CrossRef
Google scholar
|
[54] |
Wang, S., Wang, X.B., Han, X.G., Deng, Y., 2018. Higher precipitation strengthens the microbial interactions in semi-arid grassland soils. Global Ecology and Biogeography 27, 570–580
CrossRef
Google scholar
|
[55] |
Xu, T.L., Chen, X., Hou, Y.H., Zhu, B., 2021. Changes in microbial biomass, community composition and diversity, and functioning with soil depth in two alpine ecosystems on the Tibetan plateau. Plant and Soil 459, 137–153
CrossRef
Google scholar
|
[56] |
Ze, X., Mougen, F.L., Duncan, S.H., Louis, P., Flint, H.J., 2013. Some are more equal than others: the role of “keystone” species in the degradation of recalcitrant substrates. Gut Microbes 4, 236–240
CrossRef
Google scholar
|
[57] |
Zhang, X.M., Johnston, E.R., Li, L.H., Konstantinidis, K.T., Han, X.G., 2016. Experimental warming reveals positive feedbacks to climate change in the Eurasian Steppe. ISME Journal 11, 885–895
CrossRef
Google scholar
|
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