Abstract
The objective of this study was to quantify the responses of root exudates and nitrogen (N) mineralization of Abies fabri to warming and to identify links between root exudation and microbial N mineralization via interactions with the soil microbial characteristics. We conducted a 2-year study to assess the effects of warming on root traits, root exudation, soil microbial community, net N mineralization, and soil N availability within the rhizosphere of A. fabri. Results showed that warming enhanced the exudation rate of total organic carbon (REC) in both years, while warming tended to increase the exudation rate of total N (REN) in the first year, but decrease it in the second year. At the end of the second year, the C/N ratio of root exudates was higher under elevated temperature than under ambient (control) conditions. Warming increased the net N mineralization and net nitrification rates during the first year, but these effects were not observed in the second year. Although warming showed no significant effect on the content of bacteria and fungi in the first year, warming significantly increased the fungi, Gram-positive bacteria, and fungi/bacteria ratio in the second year. Warming effects on rhizosphere soil N mineralization were mainly positively correlated with the REC and REN. These results suggest that net N mineralization rates may be controlled by the quantity and C/N ratio of root exudates, rather than by the simple enhancement in root exudation rates. Our results suggest that warming could promote soil N cycling in cold regions via increased quality and quantity of root exudates.
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The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
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References
Bowsher AW, Ali R, Harding SA, Tsai CJ, Donovan LA (2016) Evolutionary divergences in root exudate composition among ecologically-contrasting Helianthus species. PLoS ONE 11:e0148280. https://doi.org/10.1371/journal.pone.0148280
Chen H, Zhao XR, Chen XJ, Lin QM, Li GT (2018) Seasonal changes of soil microbial C, N, P and associated nutrient dynamics in a semiarid grassland of north China. Appl Soil Ecol 128:89–97. https://doi.org/10.1016/j.apsoil.2018.04.008
Coskun D, Britto DT, Shi WM, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673. https://doi.org/10.1016/j.tplants.2017.05.004
Drake JE, Darby BA, Giasson MA, Kramer MA, Phillips RP, Finzi AC (2013) Stoichiometry constrains microbial response to root exudation-insights from a model and a field experiment in a temperate forest. Biogeosci 10:821–838. https://doi.org/10.5194/bg-10-821-2013
Federle TW (1986) Microbial distribution in soil-new techniques. In: Gantar M (ed) Megusar F. Slovene society for microbiology, Ljubljana, pp 493–498
Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094. https://doi.org/10.1111/gcb.12816
Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8:1075–1087. https://doi.org/10.1111/j.1461-0248.2005.00813.x
Frostegard A, Tunlid A, Baath E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14:151–163. https://doi.org/10.1016/0167-7012(91)90018-L
Frostegard A, Baath E, Tunlid A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty-acid analysis. Soil Biol Biochem 25:723–730. https://doi.org/10.1016/0038-0717(93)90113-P
Fu G, Shen ZX, Zhang XZ, Zhou YT (2012) Response of soil microbial biomass to short-term experimental warming in alpine meadow on the Tibetan Plateau. Appl Soil Ecol 61:158–160. https://doi.org/10.1016/j.apsoil.2012.05.002
George TS, Fransson AM, Hammond JP, White PJ (2011) Phosphorus nutrition: rhizosphere processes, plant response and adaptations. In: Bünemann E, Oberson A, Frossard E (eds). Springer, Berlin, pp 245–271
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N: P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129. https://doi.org/10.1016/j.soilbio.2015.02.029
Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. https://doi.org/10.1007/s11104-008-9885-9
Huang ZQ, Wan XH, He ZM, Yu ZP, Wang MH, Hu ZH, Yang YS (2013) Soil microbial biomass, community composition and soil nitrogen cycling in relation to tree species in subtropical China. Soil Biol Biochem 62:68–75. https://doi.org/10.1016/j.soilbio.2013.03.008
Jiang JS, Huang H, Huang YM, Liu XL, Liu D (2018) Relationship between maturity and microbial communities during pig manure composting by phospholipid fatty acid (PLFA) and correlation analysis. J Environ Manag 206:532–539. https://doi.org/10.1016/j.jenvman.2017.10.067
Kuypers MMM, Marchant HK, Kartal B (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276. https://doi.org/10.1038/nrmicro.2018.9
Liu L, Gundersen P, Zhang W, Zhang T, Chen H, Mo JM (2015) Effects of nitrogen and phosphorus additions on soil microbial biomass and community structure in two reforested tropical forests. Sci Rep-Uk 4:14378. https://doi.org/10.1038/srep14378
Lucas-Borja ME, Hedo J, Cerda A, Candel-Perez D, Vinegla B (2016) Unravelling the importance of forest age stand and forest structure driving microbiological soil properties, enzymatic activities and soil nutrients content in Mediterranean Spanish black pine (Pinus nigra Ar. ssp salzmannii) Forest. Sci Total Environ 562:145–154. https://doi.org/10.1016/j.scitotenv.2016.03.160
Ma ZQ, Guo DL, Xu XL et al (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97. https://doi.org/10.1038/nature25783
Ma WJ, Li J, Gao Y et al (2020) Responses of soil extracellular enzyme activities and microbial community properties to interaction between nitrogen addition and increased precipitation in a semi-arid grassland ecosystem. Sci Total Environ 703:134691. https://doi.org/10.1016/j.scitotenv.2019.134691
Meier IC, Avis PG, Phillips RP (2013) Fungal communities influence root exudation rates in pine seedlings. Fems Microbiol Ecol 83:585–595. https://doi.org/10.1111/1574-6941.12016
Parsapour MK, Kooch Y, Hosseini SM, Alavi SJ (2018) C and N cycle monitoring under Quercus castaneifolia plantation. Forest Ecol Manag 427:26–36. https://doi.org/10.1016/j.foreco.2018.05.060
Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999. https://doi.org/10.1111/j.1365-2435.2008.01495.x
Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. https://doi.org/10.1111/j.1461-0248.2010.01570.x
Remus R, Augustin J (2016) Dynamic linking of 14Cpartitioning with shoot growth allows a precise determination of plant-derived C input to soil. Plant Soil 408:493–513. https://doi.org/10.1007/s11104-016-3006-y
Rousk K, Michelsen A, Rousk J (2016) Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Global Change Biol 22:4150–4161. https://doi.org/10.1111/gcb.13296
Ruf M, Brunner I (2003) Vitality of tree fine roots: reevaluation of the tetrazolium test. Tree Physiol 23:257–263. https://doi.org/10.1093/treephys/23.4.257
Salazar A, Rousk K, Jonsdottir IS, Bellenger JP, Andresson OS (2020) Faster nitrogen cycling and more fungal and root biomass in cold ecosystems under experimental warming: a meta-analysis. Ecology 101:e02938. https://doi.org/10.1002/ecy.2938
Schindlbacher A, Rodler A, Kuffner M, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425. https://doi.org/10.1016/j.soilbio.2011.03.005
Sun LJ, Ataka M, Kominami Y, Yoshimura K (2017) Relationship between fine-root exudation and respiration of two Quercus species in a Japanese temperate forest. Tree Physiol 37:1011–1020. https://doi.org/10.1093/treephys/tpx026
Sun LJ, Ataka M, Kominami Y, Yoshimura K, Kitayama K (2021) A constant microbial C/N ratio mediates the microbial nitrogen mineralization induced by root exudation among four co-existing canopy species. Rhizosphere 17:100317. https://doi.org/10.1016/j.rhisph.2021.100317
Vanhala P, Karhu K, Tuomi M, Bjorklof K, Fritze H, Hyvarinen H, Liski J (2011) Transplantation of organic surface horizons of boreal soils into warmer regions alters microbiology but not the temperature sensitivity of decomposition. Global Change Biol 17:538–550. https://doi.org/10.1111/j.1365-2486.2009.02154.x
Wan S, Luo Y, Wallace LL (2002) Changes in microclimate induced by experimental warming and clipping in tallgrass prairie. Global Change Biol 8:754–768. https://doi.org/10.1046/j.1365-2486.2002.00510.x
Wang XX, Dong SK, Gao QZ, Zhou HK, Liu SL, Su XK, Li YY (2014) Effects of short-term and long-term warming on soil nutrients, microbial biomass and enzyme activities in an alpine meadow on the Qinghai-Tibet Plateau of China. Soil Biol Biochem 76:140–142. https://doi.org/10.1016/j.soilbio.2014.05.014
Wang C, Lu XK, Mori T et al (2018) Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol Biochem 121:103–112. https://doi.org/10.1016/j.soilbio.2018.03.009
Xu WF, Yuan WP (2017) Responses of microbial biomass carbon and nitrogen to experimental warming: a meta-analysis. Soil Biol Biochem 115:265–274. https://doi.org/10.1016/j.soilbio.2017.08.033
Yang Y, Wang GX, Yang LD, Guo JY (2013) Effects of drought and warming on biomass, nutrient allocation, and oxidative stress in Abies fabri in Eastern Tibetan Plateau. J Plant Growth Regul 32:298–306. https://doi.org/10.1007/s00344-012-9298-0
Yin HJ, Li YF, Xiao J, Xu ZF, Cheng XY, Liu Q (2013) Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Global Change Biol 19:2158–2167. https://doi.org/10.1111/gcb.12161
Yuan YS, Zhao WQ, Xiao J, Zhang ZL, Qiao MF, Liu Q, Yin HJ (2017) Exudate components exert different influences on microbially mediated C losses in simulated rhizosphere soils of a spruce plantation. Plant Soil 419:127–140. https://doi.org/10.1007/s11104-017-3334-6
Zhao CZ, Zhu LY, Liang J et al (2014) Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in Eastern Tibetan Plateau, China. Plant Soil 382:189–201. https://doi.org/10.1007/s11104-014-2153-2
Zhao Q, Sundqvist MK, Newman GS, Classen AT (2018) Soils beneath different arctic shrubs have contrasting responses to a natural gradient in temperature. Ecosphere 9:e02290. https://doi.org/10.1002/ecs2.2290
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The research was supported by the National Natural Science Foundation of China (No. 31770439) and Gongga Alpine Ecosystem Observation Station of the Chinese Academy of Sciences.
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Weilong Liu and Yonglei Jiang led the manuscript preparation with substantial contributions from all the coauthors. Yan Su contributed substantially to the data collection and also to the critical revisions of the manuscript. Joseph M. Smoak revised the manuscript. Baoli Duan supervised the research work and revised the manuscript.
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Liu, W., Jiang, Y., Su, Y. et al. Warming Affects Soil Nitrogen Mineralization via Changes in Root Exudation and Associated Soil Microbial Communities in a Subalpine Tree Species Abies fabri. J Soil Sci Plant Nutr 22, 406–415 (2022). https://doi.org/10.1007/s42729-021-00657-z
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DOI: https://doi.org/10.1007/s42729-021-00657-z