Abstract
Background and aims
Root exudates play a vital role in driving ecosystem carbon (C) cycling; however, few studies have examined the degree to which a specific exudate component affects soil C loss. The objective was to examine the impacts of different exudate components on microbially-mediated C decomposition and their underlying mechanisms.
Methods
In a well-controlled simulated rhizosphere system, we added exudate chemicals (glucose, glycine and oxalic acid) to spruce (Picea asperata) plantation soils over a 35-day period. The total C contents, net N mineralization rates, microbial communities and extracellular enzymes were measured.
Results
The three exudate components induced different C losses by different mechanisms. Oxalic acid promoted net C loss by accelerating microbial mineralization of soil organic matter (SOM). In contrast, glucose resulted in a net C accumulation, which challenged the assumption that glucose serves as a co-metabolite in driving SOM decomposition to lose C. Glycine increased the total C content via negative priming effects.
Conclusions
Exudate-induced rhizosphere priming effects are not entirely dependent on the energy properties of root exudates. Different exudates may affect SOM decomposition differently, thus the component-specialized rhizosphere processes induced by individual exudate components on soil C dynamics should be integrated into forest C cycle-climate feedbacks under environmental changes.
Similar content being viewed by others
References
Bais HP, Weir TL, Perry LG, Simon G, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159
Bird JA, Hermanb DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725. doi:10.1016/j.soilbio.2010.08.010
Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131. doi:10.1007/s00374-008-0334-y
Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105. doi:10.1016/j.apsoil.2007.05.002
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. doi:10.1371/journal.pone.0148280
Bradford MA, Keiser AD, Davies CA, Mersmann CA, Strickland MS (2013) Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth. Biogeochemistry 113:271–288. doi:10.1007/s10533-012-9822-0
Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232. doi:10.1016/j.soilbio.2006.01.022
Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76. doi:10.1007/s10533-012-9818-9
Cheng WX (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801. doi:10.1016/j.soilbio.2008.04.018
Cristofaro AD, He JZ, Zhou DH, Violante A (2000) Adsorption of phosphate and tartrate on hydroxy-aluminum-oxalate precipitates. Soil Sci Soc Am J 64:1347–1355. doi:10.2136/sssaj2000.6441347x
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. doi:10.1023/a:1020809400075
Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216. doi:10.3389/fmicb.2013.00216
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. doi:10.1111/gcb.12816
Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462. doi:10.1111/j.1469-185X.1988.tb00725.x
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi:10.1016/s0038-0717(03)00123-8
Fransson PM, Johansson EM (2010) Elevated CO2 and nitrogen influence exudation of soluble organic compounds by ectomycorrhizal root systems. FEMS Microbiol Ecol 71:186–196. doi:10.1111/j.1574-6941.2009.00795.x
Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398. doi:10.1038/nclimate1796
Grayston SJ, Vaughan D, Jones D (1997). Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5: 29–56. doi: org/10.1016/S0929-1393(96)00126-6
Haichar FE, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. doi:10.1016/j.soilbio.2014.06.017
Haller T, Stolp H (1985) Quantitative estimation of root exudation of maize plants. Plant Soil 86:207–216. doi:10.1007/bf02182895
Hamer U, Marschner B (2005) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454. doi:10.1016/j.soilbio.2004.07.037
van Hees P, Jones D, Finlay R, Godbold D, Lundström U (2005) The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13. doi:10.1016/j.soilbio.2004.06.010
Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292. doi:10.1038/nature06591
Horvath RS (1972) Microbial co-metabolism and the degradation of organic compounds in nature. Bacteriol Rev 36:146–155
Johansson EM, Fransson PMA, Finlay RD, van Hees PAW (2009) Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2. Soil Biol Biochem 41:1111–1116. doi:10.1016/j.soilbio.2009.02.016
Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils - misconceptions and knowledge gaps. Plant Soil 248:31–41. doi:10.1023/A:1022304332313
Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595. doi:10.1038/nclimate2580
Koranda M, Schnecker J, Kaiser C, Fuchslueger L, Kitzler B, Stange CF, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Microbial processes and community composition in the rhizosphere of European beech - the influence of plant C exudates. Soil Biol Biochem 43:551–558. doi:10.1016/j.soilbio.2010.11.022
Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sc 165:382–396. doi:10.1002/1522-2624
Kuzyakov Y, Hill PW, Jones DL (2007) Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant Soil 290:293–305. doi:10.1007/s11104-006-9162-8
Li J, Jiang XM, Yin HJ, Yin CY, Wei YH, Liu Q (2014) Root exudates and soil microbes in three Picea Asperata plantations with different stand ages. Chin. J Appl Ecol 2:325–332. doi:10.13287/j.1001-9332.2014.0035
Moore JA, Jiang J, Patterson CM, Mayes MA, Wang GS, Classen AT (2015) Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes. J Ecol 103:1442–1453. doi:10.1111/1365-2745.12484
Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396. doi:10.1051/agro:2003011
Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610. doi:10.1111/j.1469-8137.2006.01931.x
Paterson E. and Sim A (2013) Soil-specific response functions of organic matter mineralization to the availability of labile carbon. Glob Chang Biol 19: 1562-1571. doi:10.1111/gcb.12140
Philips DA, Fox TC, Six J (2006) Root exudation (net efflux of amino acids) may increase rhizodeposition under elevated CO2. Glob Chang Biol 12:561–567. doi:10.1111/j.1365-2486.2006.01100.x
Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29: 1513-1523. doi:10.1093/treephys/tpp083
Phillips RP, Finzi A, Bernhardt E (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. doi:10.1111/j.1461-0248.2010.01570.x
Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggests functional redundancy in carbon mineralisation. Appl Environ Microbiol 75:1589–1596. doi:10.1128/AEM.02775-08
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315. doi:10.1016/s0038-0717(02)00074-3
Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331. doi:10.2307/1934820
Strickland MS, McCulley RL, Nelson JA, Bradford MA (2015) Compositional differences in simulated root exudates elicit a limited functional and compositional response in soil microbial communities Front Microbiol 6. doi:10.3389/fmicb.2015.00817
Wang P, Bi SP, Wang S, Ding QY (2006) Variation of wheat root exudates under aluminum stress. J Agric Food Chem 54:10040–10046. doi:10.1021/jf061249o
Wang XJ, Tang CX, Severi J, Butterly CR, Baldock JA (2016) Rhizosphere priming effect on soil organic carbon decomposition under plant species differing in soil acidification and root exudation. New Phytol 211:864. doi:10.1111/nph.13966
Watt M (2009) The rhizosphere: biochemistry and organic substances at the soil? Plant interface. 2nd edn. Ann Bot 104: ix. doi:10.1093/aob/mcp166
Wu FY, Anna KCC, Nora FYT, Ming HW (2012) Root exudates of wetland plants influenced by nutrient status and types of plant cultivation. Int J Phytoremediat 14:543–553. doi:10.1080/15226514.2011.604691
Xu ZH, Chen CR (2006) Fingerprinting global climate change and forest management within rhizosphere carbon and nutrient cycling processes. Environ Sci Pollut R 13:293–298. doi:10.1065/espr2006.08.340
Xu ZF, Hu R, Xiong P, Wan C, Cao G, Liu Q (2010) Initial soil responses to experimental warming in two contrasting forest ecosystems, eastern Tibetan plateau, China: nutrient availabilities, microbial properties and enzyme activities. Appl Soil Ecol 46:291–299. doi:10.1016/j.apsoil.2010.07.005
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. Glob Chang Biol 19:2158–2167. doi:10.1111/gcb.12161
Yin HJ, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. doi:10.1016/j.soilbio.2014.07.022
Yin HJ, Phillips RP, Liang RB, Xu ZF, Liu Q (2016) Resource stoichiometry mediates soil C loss and nutrient transformations in forest soils. Appl Soil Ecol:248–257. doi:10.1016/j.apsoil.2016.09.001
Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294. doi:10.1016/s0045-6535(97)00155-0
Zelles L (1999) Identification of single cultured micro-organisms based on their whole-community fatty acid profiles, using an extended extraction procedure. Chemosphere 39:665–682. doi:10.1016/s0045-6535(99)00131-9
Acknowledgements
This study was supported jointly by the National Key R&D Program of China (2017YFC0505200), Frontier Science Key Research Programs of CAS (QYZDB-SSW-SMC023), the National Natural Science Foundation of China (31670449, 31500445), the Youth Innovation Promotion Association, CAS (2013242), the CAS “Light of West China” Program (Y6C2051100), Sichuan Youth Science and Technology Foundation (2016JQ0037) and the Key Laboratory of Mountain Surface Processes and Ecological Regulation of CAS. We also thank the staff in the Forestry Bureau of Western Sichuan and the Maoxian Mountain Ecosystem of CERN Research Station for their kind help with field investigations.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible Editor: Martin Weih.
Electronic supplementary material
ESM 1
(DOC 101 kb)
Rights and permissions
About this article
Cite this article
Yuan, Y., Zhao, W., Xiao, J. et al. Exudate components exert different influences on microbially mediated C losses in simulated rhizosphere soils of a spruce plantation. Plant Soil 419, 127–140 (2017). https://doi.org/10.1007/s11104-017-3334-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3334-6