Straw biochar strengthens the life strategies and network of rhizosphere fungi in manure fertilized soils

Abstract

Soil fungi have many important ecological functions, however, their life strategies and interactions in manure fertilized soils are not well understood. The aim of this study was to investigate the effects of biochar amendment on the fungal life strategies and species interactions in ryegrass (Lolium perenne L.) rhizosphere soil by high-throughput sequencing. Three soil treatments were evaluated: soil and pig manure mixture without planting ryegrass and biochar application (bulk soil), mixture with ryegrass planting (rhizosphere soil (RS)), and addition of 2% (w/w) biochar with ryegrass (RS+ biochar). Our results indicated that temporal turnover, defined as the slope of linear regression between community similarity and time, was significantly higher in the biochar amendment (slope= -0.2689, p<0.0001) relative to the rhizosphere soil. Following biochar addition, the percentage of species employing slow acclimation ecological strategies decreased (from 27% to 17%) and the percentage of sensitive species increased (from 40% to 50%) in comparison to the rhizosphere soil. Network analysis indicated that fungal communities in the biochar amendment enhanced positive correlations compared to the rhizosphere soil and bulk soil. Structural equation model indicated that soil pH was the most important factor in altering fungal life strategies and interactions in manure fertilized soils.

Graphical abstract

Keywords

rhizosphere / Biochar / Fungal community / Life strategies / Network analysis

References

[1] Abel, S., Peters, A., Trinks, S., Schonsky, H., Facklam, M., Wessolek, G., 2013. Impact of biochar and hydrochar addition on water retention and water repellency of sandy soil. Geoderma 202–203, 183–191

[2] Agler, M.T., Ruhe, J., Kroll, S., Morhenn, C., Kim, S.T., Weigel, D., Kemen, E.M., 2016. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biology 14, e1002352

[3] Ameloot, N., Neve, S.D., Jegajeevagan, K., Yildiz G., Buchan D., Funkuin Y.N., Prins W., Bouckaert L., Sleutel S., 2013. Short-term CO₂ and N₂O emissions and microbial properties of biochar amended sandy loam soils. Soil Biology & Biochemistry 57, 401–410

[4] Cookson, W.R., Abaye, D.A., Marschner, P., Murphy, D.V., Stockdale, E.A., Goulding, K.W.T., 2005. The contribution of soil organic matter fractions to carbon and nitrogen mineralization and microbial community size and structure. Soil Biology & Biochemistry 37, 1726–1737

[5] Deng, Y., Jiang, Y.H., Yang, Y., He, Z., Luo, F., Zhou, J., 2012. Molecular ecological network analyses. BMC Bioinformatics 13, 113

[6] Dickie, I.A., Cooper, J.A., Bufford, J.L., Hulme, P.E., Bates, S.T., 2016. Loss of functional diversity and network modularity in introduced plant-fungal symbioses. AoB Plants 9, plw084.

[7] Ducey, T., Novak, J., Johnson, M., 2015. Effects of biochar blends on microbial community composition in two coastal plain soils. Agriculture 5, 1060–1075

[8] Durenkamp, M., Luo, Y., Brookes, P.C., 2010. Impact of black carbon addition to soil on the determination of soil microbial biomass by fumigation extraction. Soil Biology & Biochemistry 42, 2026–2029

[9] Elad, Y., David, D.R., Harel, Y.M., Borenshtein, M., Kalifa, H.B., Silber, A., Graber, E.R., 2010. Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 100, 913–921

[10] Evans, S.E., Wallenstein, M.D., 2014. Climate change alters ecological strategies of soil bacteria. Ecology Letters 17, 155–164

[11] Fierer, N., 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nature Reviews. Microbiology 15, 579–590

[12] Fuhrman, J.A., 2009. Microbial community structure and its functional implications. Nature 459, 193–199

[13] Gilbert, J.A., Steele, J.A., Caporaso, J.G., Steinbrück, L., Reeder, J., Temperton, B., Huse, S., McHardy, A.C., Knight, R., Joint, I., Somerfield, P., Fuhrman, J.A., Field, D., 2012. Defining seasonal marine microbial community dynamics. ISME Journal 6, 298–308

[14] Graber, E.R., Harel, Y.M., Kolton, M., Cytryn E., Silber A., David D.R., Tsechansky L., Borenshtein M., Elad Y., 2010. Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant and Soil 337, 481–496

[15] Grime, J.P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169–1194

[16] Hammesfahr, U., Heuer, H., Manzke, B., Smalla, K., Thiele-Bruhn, S., 2008. Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biology & Biochemistry 40, 1583–1591

[17] Hatosy, S.M., Martiny, J.B., Sachdeva, R., Steele, J., Fuhrman, J.A., Martiny, A.C., 2013. Beta diversity of marine bacteria depends on temporal scale. Ecology 94, 1898–1904

[18] Holland, M.D., Hastings, A., 2008. Strong effect of dispersal network structure on ecological dynamics. Nature 456, 792–794

[19] Housman, D.C., Yeager, C.M., Darby, B.J., Sanford, R.L. Jr, Kuske, C.R., Neher, D.A., Belnap, J., 2007. Heterogeneity of soil nutrients and subsurface biota in a dryland ecosystem. Soil Biology & Biochemistry 39, 2138–2149

[20] Jia, M., Wang, F., Bian, Y., Stedtfeld, R.D., Liu, G., Yu, J., Jiang, X., 2018. Sorption of sulfamethazine to biochars as affected by dissolved organic matters of different origin. Bioresource Technology 248, 36–43

[21] 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

[22] Korhonen, J.J., Soininen, J., Hillebrand, H., 2010. A quantitative analysis of temporal turnover in aquatic species assemblages across ecosystems. Ecology 91, 508–517

[23] 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

[24] Lehmann, J., Rillig, M.C., Thies, J., Masiello, C.A., Hockaday, W.C., Crowley, D., 2011. Biochar effects on soil biota – A review. Soil Biology & Biochemistry 43, 1812–1836

[25] Liang, Y., Jiang, Y., Wang, F., Wen, C., Deng, Y., Xue, K., Qin, Y., Yang, Y., Wu, L., Zhou, J., Sun, B., 2015. Long-term soil transplant simulating climate change with latitude significantly alters microbial temporal turnover. ISME Journal 9, 2561–2572

[26] Liang, Y., Pei, M., Wang, D., Cao, S., Xiao, X., Sun, B., 2017. Improvement of soil ecosystem multifunctionality by dissipating manure-induced antibiotics and resistance genes. Environmental Science & Technology 51, 4988–4998

[27] Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., Wang, G., 2015. Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biology & Biochemistry 83, 29–39

[28] Moll, J., Goldmann, K., Kramer, S., Hempel, S., Kandeler, E., Marhan, S., Ruess, L., Krüger, D., Buscot, F., 2015. Resource type and availability regulate fungal communities along arable soil profiles. Microbial Ecology 70, 390–399

[29] Nekola, J.C., White, P.S., 1999. The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867–878

[30] Nguyen, N.H., Song, Z., Bates, S.T., Branco, S., Tedersoo, L., Menke, J., Schilling, J.S., Kennedy, P.G., 2016. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20, 241–248

[31] Op De Beeck, M., Lievens, B., Busschaert, P., Declerck, S., Vangronsveld, J., Colpaert, J.V., 2014. Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS One 9, e97629

[32] Paz-Ferreiro, J., Fu, S., Méndez, A., Gascó G., 2013. Interactive effects of biochar and the earthworm Pontoscolex corethrurus on plant productivity and soil enzyme activities. Journal of Soils and Sediments 14, 483–494

[33] Pereira e Silva, M.C., Dias, A.C., van Elsas, J.D., Salles, J.F., 2012. Spatial and temporal variation of archaeal, bacterial and fungal communities in agricultural soils. PLoS One 7, e51554

[34] Quilliam, R.S., Glanville, H.C., Wade, S.C., Jones, D.L., 2013. Life in the “charosphere” - does biochar in agricultural soil provide a significant habitat for microorganisms? Soil Biology & Biochemistry 65, 287–293

[35] Rousk, J., Bååth, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351

[36] Rudnick, M.B., van Veen, J.A., de Boer, W., 2015. Baiting of rhizosphere bacteria with hyphae of common soil fungi reveals a diverse group of potentially mycophagous secondary consumers. Soil Biology & Biochemistry 88, 73–82

[37] Shade, A., Caporaso, J.G., Handelsman, J., Knight, R., Fierer, N., 2013. A meta-analysis of changes in bacterial and archaeal communities with time. ISME Journal 7, 1493–1506

[38] Shi, S., Nuccio, E.E., Shi, Z.J., He, Z., Zhou, J., Firestone, M.K., 2016. The interconnected rhizosphere: High network complexity dominates rhizosphere assemblages. Ecology Letters 19, 926–936

[39] Singh, G., Mukerji, K.G., 2006. Root exudates as determinant of rhizospheric microbial biodiversity. In: Mukerji K.G., Manoharachary C., Singh J. (eds.). Microbial Activity in the Rhizosphere. Heidelberg: Springer, 39–53.

[40] Solaiman, Z.M., Blackwell, P., Abbott, L.K., Storer, P., 2010. Direct and residual effect of biochar application on mycorrhizal root colonization, growth and nutrition of wheat. Australian Journal of Soil Research 48, 546–554

[41] Song, Y., Li, Y., Zhang, W., Wang, F., Bian, Y., Boughner, L.A., Jiang, X., 2016. Novel biochar-plant tandem approach for remediating hexachlorobenzene contaminated soils: proof-of-concept and new insight into the rhizosphere. Journal of Agricultural and Food Chemistry 64, 5464–5471

[42] Steinbeiss, S., Gleixner, G., Antonietti, M., 2009. Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biology & Biochemistry 41, 1301–1310

[43] Sun, R., Dsouza, M., Gilbert, J.A., Guo, X., Wang, D., Guo, Z., Ni, Y., Chu, H., 2016. Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environmental Microbiology 18, 5137–5150

[44] Toju, H., Kishida, O., Katayama, N., Takagi, K., 2016. Networks depicting the fine-scale co-occurrences of fungi in soil horizons. PLoS One 11, e0165987

[45] Wang, H., Wei, Z., Mei, L., Gu, J., Yin, S., Faust, K., Raes, J., Deng, Y., Wang, Y., Shen, Q., Yin, S., 2017. Combined use of network inference tools identifies ecologically meaningful bacterial associations in a paddy soil. Soil Biology & Biochemistry 105, 227–235

[46] Wang, S., Spor, A., Nidelet, T., Montalent, P., Dillmann, C., de Vienne, D., Sicard, D., 2011. Switch between life history strategies due to changes in glycolytic enzyme gene dosage in Saccharomyces cerevisiae. Applied and Environmental Microbiology 77, 452–459

[47] Warnock, D.D., Lehmann, J., Kuyper, T.W., Rillig, M.C., 2007. Mycorrhizal responses to biochar in soil – concepts and mechanisms. Plant and Soil 300, 9–20

[48] Xiao, X., Liang, Y., Zhou, S., Zhuang S., Sun B., 2017. Fungal community reveals less dispersal limitation and potentially more connected network than that of bacteria in bamboo forest soils. Molecular Ecology 27, 550–563

[49] Xu, H.J., Wang, X.H., Li, H., Yao, H.Y., Su, J.Q., Zhu, Y.G., 2014. Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environmental Science & Technology 48, 9391–9399

[50] Yamato, M., Okimori, Y., Wibowo, I.F., Anshori, S., Ogawa, M., 2006. Effects of the application of charred bark of Acacia mangiumon the yield of maize, cowpea and peanut, and soil chemical properties in South Sumatra, Indonesia. Soil Science and Plant Nutrition 52, 489–495

[51] Zhu, X., Chen, B., Zhu, L., Xing, B., 2017. Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: A review. Environ Pollut 227, 98–115

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