Earth-Surface Processes; Soil Science; Agronomy and Crop Science
Abstract :
[en] Glomalin-related soil proteins (GRSP), derived from arbuscular mycorrhizal fungi (AMF), contributes significantly to soil stability and carbon sequestration. However, the responses of GRSP accumulation and associated AMF community and diversity to long-term fertilization regimes remain unclear. Here, we investigated the dynamics of GRSP contents, AMF biomass and diversity based on a 29-year fertilization experiment (including control, mineral fertilization, manuring and straw returning treatments). Results showed that GRSP contents increased over years across fertilization treatments. Compared with no fertilization, long-term manuring and straw returning significantly increased bulk soil GRSP by 100% and 80%, respectively, and altered the chemical
composition of GRSP by increasing the recalcitrant (aromatic) C proportion. The proportion of aromatic C in GRSP was positively correlated with AMF biomass and diversity (Shannon and Chao1), indicating that the chemical composition of GRSP could be regulated by AMF community and diversity. Moreover, manuring facilitated the formation of macro-aggregates (>250 μm), thus increasing the physical protection of GRSP. The structural equation modeling further demonstrated that GRSP content was positively regulated by soil macroaggregates, AMF biomass and diversity and their linkage with GRSP chemical composition. Collectively, longterm manuring could facilitate GRSP accumulation by shifts in AMF-mediated GRSP chemical composition (aromatic C) along with enhanced protection of macro-aggregates. This study highlights a feasible way forward for soil quality improvement and carbon sequestration for sustainable agriculture.
Disciplines :
Agriculture & agronomy
Author, co-author :
Yang, Hongbo ; Université de Liège - ULiège > TERRA Research Centre
Xiao, Qiong
Huang, Yaping
Cai, Zejiang
Li, Dongchu
Wu, Lei
Meersmans, Jeroen ; Université de Liège - ULiège > Département GxABT > Echanges Eau - Sol - Plantes
Colinet, Gilles ; Université de Liège - ULiège > TERRA Research Centre > Echanges Eau - Sol - Plantes
Zhang, Wenju
Language :
English
Title :
Long-term manuring facilitates glomalin-related soil proteins accumulation by chemical composition shifts and macro-aggregation formation
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Bibliography
Aggarwal, A., Kadian, N., Tanwar, A., Yadav, A., Gupta, K.K., Role of arbuscular mycorrhizal fungi (AMF) in global sustainable development. J. Appl. Nat. Sci. 3 (2011), 340–351.
Agnihotri, R., Sharma, M.P., Prakash, A., Ramesh, A., Bhattacharjya, S., Patra, A.K., Manna, M.C., Kurganova, I., Kuzyakov, Y., Glycoproteins of arbuscular mycorrhiza for soil carbon sequestration: Review of mechanisms and controls. Sci. Total Environ., 806, 2022, 150571.
Baltruschat, H., Santos, V.M., da Silva, D.K.A., Schellenberg, I., Deubel, A., Sieverding, E., Oehl, F., Unexpectedly high diversity of arbuscular mycorrhizal fungi in fertile Chernozem croplands in Central Europe. Catena, 182, 2019, 104135.
Bedini, S., Avio, L., Argese, E., Giovannetti, M., Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agric. Ecosyst. Environ. 120:2–4 (2007), 463–466.
Bedini, S., Pellegrino, E., Avio, L., Pellegrini, S., Bazzoffi, P., Argese, E., Giovannetti, M., Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol. Biochem. 41:7 (2009), 1491–1496.
Bertagnoli, B.G.P., Oliveira, J.F., Barbosa, G.M.C., Colozzi Filho, A., Poultry litter and liquid swine slurry applications stimulate glomalin, extraradicular mycelium production, and aggregation in soils. Soil Tillage Res., 202, 2020, 104657.
Bottinelli, N., Angers, D.A., Hallaire, V., Michot, D., Le Guillou, C., Cluzeau, D., Heddadj, D., Menasseri-Aubry, S., Tillage and fertilization practices affect soil aggregate stability in a Humic Cambisol of Northwest France. Soil Tillage Res., 2017, 14–17.
Cambardella, C.A., Elliott, E.T., Carbon and nitrogen distribution in aggregates from cultivated and native grassland soils. Soil Sci. Soc. Am. J. 57 (1993), 1071–1076.
Camenzind, T., Homeier, J., Dietrich, K., Hempel, S., Hertel, D., Krohn, A., Rillig, M.C., Opposing effects of nitrogen versus phosphorus additions on mycorrhizal fungal abundance along an elevational gradient in tropical montane forests. Soil Biol. Biochem. 94 (2016), 37–47.
Chen, L., Liu, L.I., Qin, S., Yang, G., Fang, K., Zhu, B., Kuzyakov, Y., Chen, P., Xu, Y., Yang, Y., Regulation of priming effect by soil organic matter stability over a broad geographic scale. Nat. Commun., 10, 2019, 5112.
Choudhary, M., Meena, V.S., Panday, S.C., Mondal, T., Yadav, R.P., Mishra, P.K., Bisht, J.K., Pattanayak, A., Long-term effects of organic manure and inorganic fertilization on biological soil quality indicators of soybean-wheat rotation in the Indian mid-Himalaya. Appl. Soil Ecol., 157, 2021, 103754, 10.1016/j.apsoil.2020.103754.
Cissé, G., Essi, M., Kedi, B., Mollier, A., Staunton, S., Contrasting effects of long term phosphorus fertilization on glomalin-related soil protein (GRSP). Eur. J. Soil Biol. 107 (2021), 3–6, 10.1016/j.ejsobi.2021.103363.
Cissé, G., van Oort, F., Chenu, C., Essi, M., Staunton, S., Is the operationally defined fraction of soil organic matter,“GRSP”(glomalin‐related soil protein), stable in soils? Evidence from trends in long‐term bare fallow soil. Eur. J. Soil Sci. 72:3 (2021), 1101–1112.
Delavaux, C.S., Smith‐Ramesh, L.M., Kuebbing, S.E., Beyond nutrients: a meta‐analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98 (2017), 2111–2119.
Dia, J., Hu, J., Lin, X., Yang, A., Wang, R., Zhang, J., Wong, M.H., Arbuscular mycorrhizal fungal diversity, external mycelium length, and glomalin-related soil protein content in response to long-term fertilizer management. J. Soils Sediment. 13 (2013), 1–11.
Dinesh, R., Suryanarayana, M.A., Chaudhuri, S.G., Sheeja, T.E., Long-term influence of leguminous cover crops on the biochemical properties of a sandy clay loam fluventic sulfaquent in a humid tropical region of India. Soil Tillage Res. 77 (2004), 69–77.
Driver, J.D., Holben, W.E., Rillig, M.C., Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 37 (2005), 101–106.
Duan, Y., Yang, H., Shi, T., Zhang, W., Xu, M., Gao, S., Long-term manure application to improve soil macroaggregates and plant-available nitrogen in a Mollisol. Soil Tillage Res., 211, 2021, 105035, 10.1016/j.still.2021.105035.
Garo, G., Van Geel, M., Eshetu, F., Swennen, R., Honnay, O., Vancampenhout, K., Arbuscular mycorrhizal fungi community composition, richness and diversity on enset (Ensete ventricosum (Welw.) Cheesman) in Ethiopia is influenced by manure application intensity in low-input farming systems. Plant Soil 478:1–2 (2022), 409–425.
Guo, Z., Zhang, J., Fan, J., Yang, X., Yi, Y., Han, X., Wang, D., Zhu, P., Peng, X., Does animal manure application improve soil aggregation? Insights from nine long-term fertilization experiments. Sci. Total Environ. 660 (2019), 1029–1037.
Guo, Z., Liu, J., Wu, J., Yang, D., Mei, K., Li, H., Lu, H., Yan, C., Spatial heterogeneity in chemical composition and stability of glomalin-related soil protein in the coastal wetlands. Sci. Total Environ., 835, 2022, 155351.
Gupta, V.V.S.R., Germida, J.J., Soil aggregation: influence on microbial biomass and implications for biological processes. Soil Biol. Biochem. 80 (2015), A3–A9.
Guzman, A., Montes, M., Hutchins, L., DeLaCerda, G., Yang, P., Kakouridis, A., Dahlquist‐Willard, R.M., Firestone, M.K., Bowles, T., Kremen, C., Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol. 231 (2021), 447–459.
Harner, M.J., Ramsey, P.W., Rillig, M.C., Protein accumulation and distribution in floodplain soils and river foam. Ecol. Lett. 7 (2004), 829–836.
Holátko, J., Brtnický, M., Kučerík, J., Kotianová, M., Elbl, J., Kintl, A., Jansa, J., Glomalin–Truths, myths, and the future of this elusive soil glycoprotein. Soil Biol. Biochem., 153, 2021, 108116.
Huo, W., Chai, X., Wang, X., Batchelor, W.D., Kafle, A., Gu, F., Indigenous arbuscular mycorrhizal fungi play a role in phosphorus depletion in organic manure amended high fertility soil. J. Integr. Agric. 21 (2022), 3051–3066.
Ji, L., Tan, W., Chen, X., Arbuscular mycorrhizal mycelial networks and glomalin-related soil protein increase soil aggregation in Calcaric Regosol under well-watered and drought stress conditions. Soil Tillage Res. 185 (2019), 1–8.
Johnson, N.C., Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185 (2010), 631–647.
Johnson, N.C., Angelard, C., Sanders, I.R., Kiers, E.T., Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol. Lett. 16 (2013), 140–153.
Kohler, J., Roldán, A., Campoy, M., Caravaca, F., Unraveling the role of hyphal networks from arbuscular mycorrhizal fungi in aggregate stabilization of semiarid soils with different textures and carbonate contents. Plant Soil 410 (2017), 273–281.
Lee, S.W., Lee, E.H., Eom, A.H., Effects of organic farming on communities of arbuscular myeorrhizal fungi. Mycobiology 36:1 (2008), 19–23.
Li, T., Yuan, Y., Mou, Z., Li, Y., Kuang, L., Zhang, J., Wu, W., Wang, F., Wang, J., Lambers, H., Sardans, J., Peñuelas, J., Ren, H., Liu, Z., Faster accumulation and greater contribution of glomalin to the soil organic carbon pool than amino sugars do under tropical coastal forest restoration. Glob. Change Biol. 29 (2023), 533–546, 10.1111/gcb.16467.
Lin, X., Feng, Y., Zhang, H., Chen, R., Wang, J., Zhang, J., Chu, H., Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ. Sci. Technol. 46 (2012), 5764–5771.
Liu, D., Ju, W., Jin, X., Li, M., Shen, G., Duan, C., Guo, L., Liu, Y., Zhao, W., Fang, L., Associated soil aggregate nutrients and controlling factors on aggregate stability in semiarid grassland under different grazing prohibition timeframes. Sci. Total Environ., 777, 2021, 146104.
Liu, M., Han, G., Zhang, Q., Effects of agricultural abandonment on soil aggregation, soil organic carbon storage and stabilization: Results from observation in a small karst catchment, Southwest China. Agric. Ecosyst. Environ., 288, 2020, 106719.
Liu, M., Shen, Y., Li, Q., Xiao, W., Song, X., Arbuscular mycorrhizal fungal colonization and soil pH induced by nitrogen and phosphorus additions affects leaf C: N: P stoichiometry in Chinese fir (Cunninghamia lanceolata) forests. Plant Soil 461 (2021), 421–440.
Liu, W., Ma, K., Wang, X., Wang, Z., Negrete-Yankelevich, S., Effects of no-tillage and biologically-based organic fertilizer on soil arbuscular mycorrhizal fungal communities in winter wheat field. Appl. Soil Ecol., 178, 2022, 104564.
Luo, X., Shi, S., Liu, Y., Yang, H., Li, N., Dong, Z., Zhu, B., He, X., Arbuscular mycorrhizal fungal communities of topsoil and subsoil of an annual maize-wheat rotation after 15-years of differential mineral and organic fertilization. Agric. Ecosyst. Environ., 315, 2021, 107442.
Ma, N., Yokoyama, K., Marumoto, T., Promotion of host plant growth and infection of roots with arbuscular mycorrhizal fungus Gigaspora margarita by the application of peat. Soil Sci. Plant Nutr. 52 (2006), 162–167.
Malusà, E., Pinzari, F., Canfora, L., 2016. Efficacy of biofertilizers: challenges to improve crop production. Microb. Inoculants Sustain. Agric. Product. Vol. 2 Funct. Appl. 17–40.
Olsson, P.A., Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 29 (1999), 303–310.
Ozlu, E., Sandhu, S.S., Kumar, S., Arriaga, F.J., Soil health indicators impacted by long-term cattle manure and inorganic fertilizer application in a corn-soybean rotation of South Dakota. Sci. Rep., 9, 2019, 11776.
Porras-Alfaro, A., Herrera, J., Natvig, D.O., Sinsabaugh, R.L., Effect of long-term nitrogen fertilization on mycorrhizal fungi associated with a dominant grass in a semiarid grassland. Plant Soil 296 (2007), 65–75.
Prommer, J., Walker, T.W., Wanek, W., Braun, J., Zezula, D., Hu, Y., Hofhansl, F., Richter, A., Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity. Glob. Change Biol. 26:2 (2020), 669–681.
Qin, Z., Zhang, H., Feng, G., Christie, P., Zhang, J., Li, X., Gai, J., Soil phosphorus availability modifies the relationship between AM fungal diversity and mycorrhizal benefits to maize in an agricultural soil. Soil Biol. Biochem., 144, 2020, 107790.
Rillig, M.C., Mummey, D.L., Mycorrhizas and soil structure. New Phytol. 171 (2006), 41–53.
Rillig, M.C., Wright, S.F., Nichols, K.A., Schmidt, W.F., Torn, M.S., Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233 (2001), 167–177, 10.1023/A:1010364221169.
Šarapatka, B., Alvarado-Solano, D.P., Čižmár, D., Can glomalin content be used as an indicator for erosion damage to soil and related changes in organic matter characteristics and nutrients?. Catena, 181, 2019, 104078.
Scheublin, T.R., Ridgway, K.P., Young, J.P.W., Van Der Heijden, M.G.A., Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl. Environ. Microbiol. 70 (2004), 6240–6246.
Schindler, F.V., Mercer, E.J., Rice, J.A., Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content. Soil Biol. Biochem. 39 (2007), 320–329.
Sekaran, U., Loya, J.R., Abagandura, G.O., Subramanian, S., Owens, V., Kumar, S., Intercropping of kura clover (Trifolium ambiguum M. Bieb) with prairie cordgrass (Spartina pectinata link.) enhanced soil biochemical activities and microbial community structure. Appl. Soil Ecol., 147, 2020, 103427.
Singh, A.K., Rai, A., Singh, N., Effect of long term land use systems on fractions of glomalin and soil organic carbon in the Indo-Gangetic plain. Geoderma 277 (2016), 41–50.
Song, G., Chen, R., Xiang, W., Yang, F., Zheng, S., Zhang, J., Lin, X., Contrasting effects of long-term fertilization on the community of saprotrophic fungi and arbuscular mycorrhizal fungi in a sandy loam soil. Plant, Soil Environ. 61 (2015), 127–136.
Tian, S., Zhu, B., Yin, R., Wang, M., Jiang, Y., Zhang, C., Li, D., Chen, X., Kardol, P., Liu, M., Organic fertilization promotes crop productivity through changes in soil aggregation. Soil Biol. Biochem., 165, 2022, 108533.
Tisdall, J.M., OADES, J.M., Organic matter and water‐stable aggregates in soils. J. Soil Sci. 33 (1982), 141–163.
Tivet, F., de Moraes Sá, J.C., Lal, R., Milori, D.M.B.P., Briedis, C., Letourmy, P., Pinheiro, L.A., Borszowskei, P.R., da Cruz Hartman, D., Assessing humification and organic C compounds by laser-induced fluorescence and FTIR spectroscopies under conventional and no-till management in Brazilian Oxisols. Geoderma 207, 2013, 71–81.
Trivedi, P., Delgado‐Baquerizo, M., Jeffries, T.C., Trivedi, C., Anderson, I.C., Lai, K., McNee, M., Flower, K., Pal Singh, B., Minkey, D., Soil aggregation and associated microbial communities modify the impact of agricultural management on carbon content. Environ. Microbiol. 19 (2017), 3070–3086.
Van Geel, M., Busschaert, P., Honnay, O., Lievens, B., Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J. Microbiol. Methods 106 (2014), 93–100.
Van-Camp, L., Bujarrabal, B., Gentile, A.R., Jones, R.J.A., Montanarella, L., Olazabal, C., Selvaradjou, S., Technical Working Groups Established under the Thematic Strategy for Soil Protection. 2004, JRC Publ. Repos.
Wang, Q., Lu, H., Chen, J., Jiang, Y., Williams, M.A., Wu, S., Li, J., Liu, J., Yang, G., Yan, C., Interactions of soil metals with glomalin-related soil protein as soil pollution bioindicators in mangrove wetland ecosystems. Science of the Total Environment, 2020, Elsevier B.V., 10.1016/j.scitotenv.2019.136051.
Wang, C., Ning, P., Li, J., Wei, X., Ge, T., Cui, Y., Deng, X., Jiang, Y., Shen, W., Responses of soil microbial community composition and enzyme activities to long-term organic amendments in a continuous tobacco cropping system. Appl. Soil Ecol., 169, 2022, 104210, 10.1016/j.apsoil.2021.104210.
Wang, H., Parent, S., Gosselin, A., Desjardins, Y., Vesicular-arbuscular mycorrhizal peat-based substrates enhance symbiosis establishment and growth of three micropropagated species. J. Am. Soc. Hortic. Sci. 118 (1993), 896–901.
Wang, Q., Wang, W., Zhong, Z., Wang, H., Fu, Y., Variation in glomalin in soil profiles and its association with climatic conditions, shelterbelt characteristics, and soil properties in poplar shelterbelts of Northeast China. J. Res. 31 (2020), 279–290.
Wang, Q., Wu, Y., Wang, W., Zhong, Z., Pei, Z., Ren, J., Wang, H., Zu, Y., Spatial variations in concentration, compositions of glomalin related soil protein in poplar plantations in northeastern China, and possible relations with soil physicochemical properties. Sci. World J., 2014, 2014.
Williams, A., Manoharan, L., Rosenstock, N.P., Olsson, P.A., Hedlund, K., Long‐term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (H ordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol. 213 (2017), 874–885.
Wright, S.F., Upadhyaya, A., Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci. 161 (1996), 575–586.
Wright, S.F., Upadhyaya, A., Buyer, J.S., Comparison of N-linked oligosaccharides of glomalin from arbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biol. Biochem. 30 (1998), 1853–1857.
Xavier, L.J.C., Germida, J.J., Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol. Fertil. Soils 37 (2003), 261–267.
Xiao, D., Che, R., Liu, X., Tan, Y., Yang, R., Zhang, W., He, X., Xu, Z., Wang, K., Arbuscular mycorrhizal fungi abundance was sensitive to nitrogen addition but diversity was sensitive to phosphorus addition in karst ecosystems. Biol. Fertil. Soils 55 (2019), 457–469.
Xiao, Q., Huang, Y., Wu, L., Tian, Y., Wang, Q., Wang, B., Xu, M., Zhang, W., Long-term manuring increases microbial carbon use efficiency and mitigates priming effect via alleviated soil acidification and resource limitation. Biol. Fertil. Soils 57 (2021), 925–934.
Yu, L., Nicolaisen, M., Larsen, J., Ravnskov, S., Organic fertilization alters the community composition of root associated fungi in Pisum sativum. Soil Biol. Biochem. 58 (2013), 36–41.
Zhang, B., Horn, R., Mechanisms of aggregate stabilization in Ultisols from subtropical China. Geoderma 99 (2001), 123–145.
Zhang, W., Xu, M., Wang, B., Wang, X., Soil organic carbon, total nitrogen and grain yields under long-term fertilizations in the upland red soil of southern China. Nutr. Cycl. Agroecosyst. 84 (2009), 59–69.
Zhang, X., Wu, X., Zhang, S., Xing, Y., Wang, R., Liang, W., Organic amendment effects on aggregate-associated organic C, microbial biomass C and glomalin in agricultural soils. Catena 123 (2014), 188–194.
Zheng, Y., Kim, Y.C., Tian, X.F., Chen, L., Yang, W., Gao, C., Song, M.H., Xu, X.L., Guo, L.D., Differential responses of arbuscular mycorrhizal fungi to nitrogen addition in a near pristine Tibetan alpine meadow. FEMS Microbiol. Ecol. 89:3 (2014), 594–605.
Zhong, Z., Wang, W., Wang, Q., Wu, Y., Wang, H., Pei, Z., Glomalin amount and compositional variation, and their associations with soil properties in farmland, northeastern China. J. Plant Nutr. Soil Sci. 180 (2017), 563–575.
Zhu, C., Ling, N., Guo, J., Wang, M., Guo, S., Shen, Q., Impacts of fertilization regimes on arbuscular mycorrhizal fungal (AMF) community composition were correlated with organic matter composition in maize rhizosphere soil. Front. Microbiol., 7, 2016, 1840.
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