Abstract
Background and aims
It is unclear how atmospheric nitrogen (N) deposition influences CO2 release from grassland by affecting heterotrophic respiration of bulk and rhizosphere soils and how the heterotrophic rhizosphere respiration of different grass species responds to N deposition.
Methods
In this study, we investigated the effects of N addition on heterotrophic respiration of bulk and rhizosphere soils associated with the dominant species (Bothriochloa ischaemum) and subdominant species (Artemisia sacrorum and Stipa capillata) in the grassland treated with N fertilizer (0,3,9 g N m−2 y−1) for eight years.
Results
Low-N addition significantly increased cumulative CO2-C emissions of bulk soil by 22.91% and rhizosphere soil of A. sacrorum by 72.26%, while high-N addition significantly increased that of rhizosphere soil of (A) sacrorum by 37.38% and S. capillata by 13.71%. There was no clear response to N addition for (B) ischaemum. Heterotrophic rhizosphere respiration of B. ischaemum was most strongly related to stable-C-degrading functional genes, whereas that of A. sacrorum and S. capillata was most strongly related to labile-C-degrading functional genes. C-degrading functional genes in rhizosphere soil were significantly related to root morphological characteristics, especially specific root length, specific root surface area, and root average diameter rather than root exudation rates.
Conclusion
The present study revealed that N addition could affect heterotrophic soil respiration by changing labile-C and stable-C degrading functional genes, which in the rhizosphere of different plant species were regulated by their root functional traits.
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Data Availability
Sequence data associated with this project have been deposited into the NCBI Sequence Read Archive database (accession number: PRJNA939903).
References
Ackerman D, Millet DB, Chen X (2019) Global estimates of inorganic nitrogen deposition across four decades. Glob Biogeochem Cycles 33(1):100–107. https://doi.org/10.1029/2018GB005990
Altieri KE, Fawcett SE, Hastings MG (2021) Reactive Nitrogen cycling in the atmosphere and ocean. Annu Rev Earth Planet Sci 49(1):523–550. https://doi.org/10.1146/annurev-earth-083120-052147
Ataka M, Sun L, Nakaji T, Katayama A, Hiura T (2020) Five-year nitrogen addition affects fine root exudation and its correlation with root respiration in a dominant species, Quercus crispula, of a cool temperate forest, Japan. Tree Physiol 40(3):367–376. https://doi.org/10.1093/treephys/tpz143
Babur E, Uslu ÖS, Battaglia ML, Mumtaz MZ, Danish S, Fahad S, Diatta AA, Datta R, Ozlu E (2021) Nitrogen fertilizer effects on microbial respiration, microbial biomass, and carbon sequestration in a mediterranean grassland ecosystem. Int J Environ Res 15(4):655–665. https://doi.org/10.1007/s41742-021-00336-y
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19(2):90–98. https://doi.org/10.1016/j.tplants.2013.11.006
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interations with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bakker JP (2002) Plant strategies, vegetation processes and ecosystem properties. New Phytol 156:6–8
Bao SD (2018) Soil and agricultural chemistry analysis, 3rd edn. Chinese Agriculture Press, Beijing
Cabrera M, Beare M (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57(4):1007–1012. https://doi.org/10.2136/sssaj1993.03615995005700040021x
Chai YN, Schachtman DP (2022) Root exudates impact plant performance under abiotic stress. Trends Plant Sci 27(1):80–91. https://doi.org/10.1016/j.tplants.2021.08.003
Chapin FS, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem Ecology. Springer, New York. https://doi.org/10.1007/b97397
Chen C, Chen X, Chen HYH (2023) Mapping N deposition impacts on soil microbial biomass across global terrestrial ecosystems. Geoderma 433:116429. https://doi.org/10.1016/j.geoderma.2023.116429
Chen Y, Neilson JW, Kushwaha P, Maier RM, Barberan A (2021) Life-history strategies of soil microbial communities in an arid ecosystem. ISME J 15(3):649–657. https://doi.org/10.1038/s41396-020-00803-y
Chen G, Tu L, Peng Y, Hu H, Hu T, Xu Z, Liu L, Tang Y (2017) Effect of nitrogen additions on root morphology and chemistry in a subtropical bamboo forest. Plant Soil 412(1):441–451. https://doi.org/10.1007/s11104-016-3074-z
Ciais P, Yao Y, Gasser T, Baccini A, Wang Y, Lauerwald R, Peng S, Bastos A, Li W, Raymond PA, Canadell JG, Peters GP, Andres RJ, Chang J, Yue C, Dolman AJ, Haverd V, Hartmann J, Laruelle G, Zhu D, Ciais P, Yao Y, Gasser T, Baccini A, Wang Y, Lauerwald R, Peng S, Bastos A, Li W, Raymond PA, Canadell JG, Peters GP, Andres RJ, Chang J, Yue C, Dolman AJ, Haverd V, Hartmann J, Laruelle G, Konings AG, King AW, Liu Yi, Luyssaert S, Maignan F, Patra PK, Peregon A, Regnier P, Pongratz J, Poulter B, Shvidenko A, Valentini R, Wang R, Broquet G, Yin Yi, Zscheischler J, Guenet B, Goll DS, Ballantyne A-P, Yang H, Qiu C, Zhu D (2021) Empirical estimates of regional carbon budgets imply reduced global soil heterotrophic respiration. Natl Sci Rev 8(2):nwaa145. https://doi.org/10.1093/nsr/nwaa145
Devaraju N, Bala G, Caldeira K, Nemani R (2016) A model based investigation of the relative importance of CO2-fertilization, climate warming, nitrogen deposition and land use change on the global terrestrial carbon uptake in the historical period. Clim Dyn 47(1–2):173–190. https://doi.org/10.1007/s00382-015-2830-8
Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. In M. Begon and A. H. Fitter (Eds.), Advances in Ecological Research, vol. 27, pp. 1–60. Academic Press Ltd-Elsevier Science Ltd. https://doi.org/10.1016/S0065-2504(08)60005-7
el Zahar Haichar F, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. https://doi.org/10.1016/j.soilbio.2014.06.017
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892. https://doi.org/10.1126/science.1136674
Geng P, Jin G (2022) Fine root morphology and chemical responses to N addition depend on root function and soil depth in a korean pine plantation in Northeast China. For Ecol Manag 520:120407. https://doi.org/10.1016/j.foreco.2022.120407
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111(982):1169–1194. https://doi.org/10.1086/283244
Han M, Chen Y, Li R, Yu M, Fu L, Li S, Su J, Zhu B (2022) Root phosphatase activity aligns with the collaboration gradient of the root economics space. New Phytol 234(3):837–849. https://doi.org/10.1111/nph.17906
Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48(1):115–146. https://doi.org/10.1023/A:1006244819642
Houghton RA (2007) Balancing the global carbon budget. Annu Rev Earth Planet Sci 35:313–347. https://doi.org/10.1146/annurev.earth.35.031306.140057
Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, van der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2738. https://doi.org/10.1038/s41467-018-05122-7
Jia SX, Hu CQ, Sun Y, Han J, Zhang WL, Chen XW, Liang AZ, Zhang SX (2018) Effects of N fertilization on soil microbial respiration in Larix Gmelinii plantation. Appl Ecol Environ Res 16(5):5921–5932. https://doi.org/10.15666/aeer/1605_59215932
Jing H, Li J, Yan B, Wei F, Wang G, Liu G (2021) The effects of nitrogen addition on soil organic carbon decomposition and microbial C-degradation functional genes abundance in a Pinus tabulaeformis forest. For Ecol Manag 489:119098. https://doi.org/10.1016/j.foreco.2021.119098
Jing H, Zhang P, Li J, Yao X, Liu G, Wang G (2019) Effect of nitrogen addition on the decomposition and release of compounds from fine roots with different diameters: the importance of initial substrate chemistry. Plant Soil 438(1):281–296. https://doi.org/10.1007/s11104-019-04017-w
Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38(5):991–999. https://doi.org/10.1016/j.soilbio.2005.08.012
Lefroy R, Blair G, Strong W (1993) Changes in soil organic-matter with cropping as measured by organic-carbon fractions and C-13 natural isotope abundance. Plant Soil 155:399–402. https://doi.org/10.1007/BF00025067
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528(7580):60–68. https://doi.org/10.1038/nature16069
Li X, Rui J, Xiong J, Li J, He Z, Zhou J, Yannarell AC, Mackie RI (2014) Functional potential of soil microbial communities in the Maize Rhizosphere. PLoS ONE 9(11):e112609. https://doi.org/10.1371/journal.pone.0112609
Liang C, Amelung W, Lehmann J, Kaestner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Change Biol 25(11):3578–3590. https://doi.org/10.1111/gcb.14781
Liu Y, Men M, Peng Z, Chen HYH, Yang Y, Peng Y (2023) Spatially explicit estimate of nitrogen effects on soil respiration across the globe. Glob Change Biol 29(13):3591–3600. https://doi.org/10.1111/gcb.16716
Ma X, Wang T, Shi Z, Chiariello NR, Docherty K, Field CB, Gutknecht J, Gao Q, Gu Y, Guo X, Hungate BA, Lei J, Niboyet A, Le Roux X, Yuan M, Yuan T, Zhou J, Yang Y (2022) Long-term nitrogen deposition enhances microbial capacities in soil carbon stabilization but reduces network complexity. Microbiome 10(1):112. https://doi.org/10.1186/s40168-022-01309-9
Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi Ö, Yu R, Zhou B (eds) (2021) Climate Change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press. https://doi.org/10.1017/9781009157896
Merino-Martín L, Griffiths RI, Gweon HS, Furget-Bretagnon C, Oliver A, Mao Z, Le Bissonnais Y, Stokes A (2020) Rhizosphere bacteria are more strongly related to plant root traits than fungi in temperate montane forests: insights from closed and open forest patches along an elevational gradient. Plant Soil 450(1):183–200. https://doi.org/10.1007/s11104-020-04479-3
Metcalfe DB, Fisher RA, Wardle DA (2011) Plant communities as drivers of soil respiration: pathways, mechanisms, and significance for global change. Biogeosciences 8(8):2047–2061. https://doi.org/10.5194/bg-8-2047-2011
Michalet S, Rohr J, Warshan D, Bardon C, Roggy J-C, Domenach A-M, Czarnes S, Pommier T, Combourieu B, Guillaumaud N, Bellvert F, Comte G, Poly F (2013) Phytochemical analysis of mature tree root exudates in situ and their role in shaping soil microbial communities in relation to tree N-acquisition strategy. Plant Physiol Biochem 72:169–177. https://doi.org/10.1016/j.plaphy.2013.05.003
Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of Soil Analysis, Part 2. Chemical and Microbial Properties. Agronomy Society of America, p 539e552. Agronomy Monograph 9, Madison, Wisconsin
Ning Q, Hättenschwiler S, Lü X, Kardol P, Zhang Y, Wei C, Xu C, Huang J, Li A, Yang J, Wang J, Peng Y, Peñuelas J, Sardans J, He J, Xu Z, Gao Y, Han X (2021) Carbon limitation overrides acidification in mediating soil microbial activity to nitrogen enrichment in a temperate grassland. Glob Change Biol 27(22):5976–5988. https://doi.org/10.1111/gcb.15819
Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22(6):990–999. https://doi.org/10.1111/j.1365-2435.2008.01495.x
Riutta T, Kho LK, Teh YA, Ewers R, Majalap N, Malhi Y (2021) Major and persistent shifts in below-ground carbon dynamics and soil respiration following logging in tropical forests. Glob Change Biol 27(10):2225–2240. https://doi.org/10.1111/gcb.15522
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Koegel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478(7367):49–56. https://doi.org/10.1038/nature10386
Schulte-Uebbing L, de Vries W (2018) Global-scale impacts of nitrogen deposition on tree carbon sequestration in tropical, temperate, and boreal forests: a meta-analysis. Glob Change Biol 24(2):E416–E431. https://doi.org/10.1111/gcb.13862
Song Y, Li X, Yao S, Yang X, Jiang X (2020) Correlations between soil metabolomics and bacterial community structures in the pepper rhizosphere under plastic greenhouse cultivation. Sci Total Environ 728:138439. https://doi.org/10.1016/j.scitotenv.2020.138439
Sun L, Ataka M, Han M, Han Y, Gan D, Xu T, Guo Y, Zhu B (2021) Root exudation as a major competitive fine-root functional trait of 18 coexisting species in a subtropical forest. New Phytol 229(1):259–271. https://doi.org/10.1111/nph.16865
Tilman D (1982) Resource competition and community structure. Monogr Popul Biol 17:1–296
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11(10):1111–1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Vermeulen PJ, Stuefer JF, Anten NPR, During HJ (2009) Carbon gain in the competition for light between genotypes of the clonal herb Potentilla reptans. J Ecol 97(3):508–517. https://doi.org/10.1111/j.1365-2745.2009.01491.x
Wang J-J, Bowden RD, Lajtha K, Washko SE, Wurzbacher SJ, Simpson MJ (2019) Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter. Biogeochemistry 142(2):299–313. https://doi.org/10.1007/s10533-018-00535-4
Wang G, Fahey TJ, Xue S, Liu F (2013) Root morphology and architecture respond to N addition in Pinus tabuliformis, west China. Oecologia 171(2):583–590. https://doi.org/10.1007/s00442-012-2441-6
Wang C, Liu D, Bai E (2018) Decreasing soil microbial diversity is associated with decreasing microbial biomass under nitrogen addition. Soil Biol Biochem 120:126–133. https://doi.org/10.1016/j.soilbio.2018.02.003
Wei X, Shao M, Fu X, Agren GI, Yin X (2011) The effects of land use on soil N mineralization during the growing season on the northern Loess Plateau of China. Geoderma 160(3–4):590–598. https://doi.org/10.1016/j.geoderma.2010.11.007
Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019) Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol 223(2):882–895. https://doi.org/10.1111/nph.15833
Wen Z, White PJ, Shen J, Lambers H (2022) Linking root exudation to belowground economic traits for resource acquisition. New Phytol 233(4):1620–1635. https://doi.org/10.1111/nph.17854
Xu X, Shi Z, Li D, Zhou X, Sherry RA, Luo Y (2015) Plant community structure regulates responses of prairie soil respiration to decadal experimental warming. Glob Change Biol 21(10):3846–3853. https://doi.org/10.1111/gcb.12940
Xu C, Xu X, Ju C, Chen HYH, Wilsey BJ, Luo Y, Fan W (2021) Long-term, amplified responses of soil organic carbon to nitrogen addition worldwide. Glob Change Biol 27(6):1170–1180. https://doi.org/10.1111/gcb.15489
Yang Y, Li T, Pokharel P, Liu L, Qiao J, Wang Y, An S, Chang SX (2022) Global effects on soil respiration and its temperature sensitivity depend on nitrogen addition rate. Soil Biol Biochem 174:108814. https://doi.org/10.1016/j.soilbio.2022.108814
Ye C, Chen D, Hall SJ, Pan S, Yan X, Bai T, Guo H, Zhang Y, Bai Y, Hu S (2018) Reconciling multiple impacts of nitrogen enrichment on soil carbon: plant, microbial and geochemical controls. Ecol Lett 21(8):1162–1173. https://doi.org/10.1111/ele.13083
Zeng J, Liu X, Song L, Lin X, Zhang H, Shen C, Chu H (2016) Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol Biochem 92:41–49. https://doi.org/10.1016/j.soilbio.2015.09.018
Zhang X, Zhao W, Liu Y, Fang X, Feng Q (2016) The relationships between grasslands and soil moisture on the Loess Plateau of China: a review. CATENA 145:56–67. https://doi.org/10.1016/j.catena.2016.05.022
Zhao Z-B, He J-Z, Geisen S, Han L-L, Wang J-T, Shen J-P, Wei W-X, Fang Y-T, Li P-P, Zhang L-M (2019) Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome 7:33. https://doi.org/10.1186/s40168-019-0647-0
Zhu X, Zhang Z, Liu D, Kou Y, Zheng Q, Liu M, Xiao J, Liu Q, Yin H (2020) Differential impacts of nitrogen addition on rhizosphere and bulk-soil carbon sequestration in an alpine shrubland. J Ecol 108(6):2309–2320. https://doi.org/10.1111/1365-2745.13417
Acknowledgements
We would like to thank Dr. Joseph Elliot at the University of Kansas for her assistance with English language and grammatical editing of the manuscript.
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This work was supported by the Special Funds of the National Natural Science Foundation of China (No. 42041005-3B) and the National Natural Science Foundation of China, (No. 42077456).
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Wei, F., Yan, B., Wu, C. et al. N addition affects the heterotrophic respiration of bulk and rhizosphere soils through changes in root traits and C-degrading functional genes in semi-arid grassland. Plant Soil 494, 669–683 (2024). https://doi.org/10.1007/s11104-023-06310-1
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DOI: https://doi.org/10.1007/s11104-023-06310-1