Abstract
Background and Aims
Plant and microbial-derived carbon (C) constitute the soil C pool and determine its response to N deposition. However, the response of plant and microbial-derived C to exogenous N input in forest soils, accounting for 70% of the global soil C, remains unclear.
Methods
We conducted a global meta-analysis to assess the response of microbial-derived C (indicated by amino sugars) and plant-derived C (indicated by lignin phenols) in forest soils to the increasing N deposition.
Results
Results revealed significant increases in both total amino sugar and lignin phenols, with a more pronounced increase in temperate forest soils experiencing low-level N addition. Glucosamine (GluN) exhibited no significant change, but muramic acid (MurN) was increased following N addition. Positive correlations were observed between total amino sugars and SOC and total phospholipid fatty acid (PLFA), as well as between MurN and bacterial PLFA. Lignin phenols were positively correlated with litterfall but unrelated to root biomass.
Conclusion
N deposition enhanced the accumulation of microbial and plant-derived C in soils, particularly in N-deficient temperate forest soils. The accumulation of microbial-derived C is primarily attribute to the increased microbial biomass and bacterial-derived C, while the accrual plant-derived C is mainly associated with the increase in aboveground C input caused by N addition. These findings collectively uncover the general patterns and mechanisms of microbial and plant-derived C in forest soils in response to N deposition, providing new insights into interpreting soil C dynamics and predicting soil C pools in forest ecosystems facing future climate changes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
References
Angst G, Heinrich L, Kögel-Knabner I, Mueller CW (2016) The fate of cutin and suberin of decaying leaves, needles and roots – Inferences from the initial decomposition of bound fatty acids. Org Geochem 95:81–92. https://doi.org/10.1016/j.orggeochem.2016.02.006
Angst G, Mueller KE, Nierop KGJ, Simpson MJ (2021) Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter. Soil Biol Biochem 156:108189. https://doi.org/10.1016/j.soilbio.2021.108189
Argiroff WA, Zak DR, Upchurch RA et al (2019) Anthropogenic N deposition alters soil organic matter biochemistry and microbial communities on decaying fine roots. Glob Chang Biol 25:4369–4382. https://doi.org/10.1111/gcb.14770
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Soft 67:. https://doi.org/10.18637/jss.v067.i01
Cao Y, Ding J, Li J et al (2023) Necromass-derived soil organic carbon and its drivers at the global scale. Soil Biol Biochem 181:109025. https://doi.org/10.1016/j.soilbio.2023.109025
Chen J, Luo Y, Van Groenigen KJ et al (2018) A keystone microbial enzyme for nitrogen control of soil carbon storage. Sci Adv 4:eaaq1689. https://doi.org/10.1126/sciadv.aaq1689
Chen L, Fang K, Wei B et al (2021) Soil carbon persistence governed by plant input and mineral protection at regional and global scales. Ecol Lett 24:1018–1028. https://doi.org/10.1111/ele.13723
Crow SE, Lajtha K, Filley TR et al (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–2019. https://doi.org/10.1111/j.1365-2486.2009.01850.x
Crowther TW, Riggs C, Lind EM et al (2019) Sensitivity of global soil carbon stocks to combined nutrient enrichment. Ecol Lett 22:936–945. https://doi.org/10.1111/ele.13258
Dai G, Zhu S, Cai Y et al (2022) Plant-derived lipids play a crucial role in forest soil carbon accumulation. Soil Biol Biochem 168:108645. https://doi.org/10.1016/j.soilbio.2022.108645
Du E, Terrer C, Pellegrini AFA et al (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13:221–226. https://doi.org/10.1038/s41561-019-0530-4
Eastman BA, Adams MB, Brzostek ER et al (2021) Altered plant carbon partitioning enhanced forest ecosystem carbon storage after 25 years of nitrogen additions. New Phytol 230:1435–1448. https://doi.org/10.1111/nph.17256
Entwistle EM, Zak DR, Argiroff WA (2018) Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi. Ecol Monogr 88:225–244. https://doi.org/10.1002/ecm.1288
Fan Y, Yang L, Zhong X et al (2020) N addition increased microbial residual carbon by altering soil P availability and microbial composition in a subtropical Castanopsis forest. Geoderma 375:114470. https://doi.org/10.1016/j.geoderma.2020.114470
Feng X, Simpson AJ, Schlesinger WH et al (2010) Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the duke forest: om composition under face and fertilization. Glob Chang Biol 16:2104–2116. https://doi.org/10.1111/j.1365-2486.2009.02080.x
Feng X, Qin S, Zhang D et al (2022) Nitrogen input enhances microbial carbon use efficiency by altering plant–microbe–mineral interactions. Glob Chang Biol 28:4845–4860. https://doi.org/10.1111/gcb.16229
Feng H, Guo J, Peng C et al (2023) Nitrogen addition promotes terrestrial plants to allocate more biomass to aboveground organs: a global meta-analysis. Glob Chang Biol 29:3970–3989. https://doi.org/10.1111/gcb.16731
Frey SD, Knorr M, Parrent JL et al (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171. https://doi.org/10.1016/j.foreco.2004.03.018
Frey SD, Ollinger S, Nadelhoffer K et al (2014) Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121:305–316. https://doi.org/10.1007/s10533-014-0004-0
Galloway JN, Dentener FJ, Capone DG et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Gillespie AW, Diochon A, Ma BL et al (2014) Nitrogen input quality changes the biochemical composition of soil organic matter stabilized in the fine fraction: a long-term study. Biogeochemistry 117:337–350. https://doi.org/10.1007/s10533-013-9871-z
Grandy AS, Sinsabaugh RL, Neff JC et al (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49. https://doi.org/10.1007/s10533-008-9257-9
Griepentrog M, Bodé S, Boeckx P et al (2014) Nitrogen deposition promotes the production of new fungal residues but retards the decomposition of old residues in forest soil fractions. Glob Chang Biol 20:327–340. https://doi.org/10.1111/gcb.12374
He H, Zhang W, Zhang X et al (2011) Temporal responses of soil microorganisms to substrate addition as indicated by amino sugar differentiation. Soil Biol Biochem 43:1155–1161. https://doi.org/10.1016/j.soilbio.2011.02.002
Hu J, Huang C, Zhou S et al (2022a) Nitrogen addition increases microbial necromass in croplands and bacterial necromass in forests: A global meta-analysis. Soil Biol Biochem 165:108500. https://doi.org/10.1016/j.soilbio.2021.108500
Hu J, Huang C, Zhou S, Kuzyakov Y (2022b) Nitrogen addition to soil affects microbial carbon use efficiency: Meta-analysis of similarities and differences in 13C and 18O approaches. Glob Chang Biol 28:4977–4988. https://doi.org/10.1111/gcb.16226
Hu Y, Deng Q, Kätterer T et al (2024) Depth-dependent responses of soil organic carbon under nitrogen deposition. Glob Chang Biol 30:e17247. https://doi.org/10.1111/gcb.17247
Huang W, Kuzyakov Y, Niu S et al (2023a) Drivers of microbially and plant-derived carbon in topsoil and subsoil. Glob Chang Biol 29:6188–6200. https://doi.org/10.1111/gcb.16951
Huang W, Yu W, Yi B et al (2023b) Contrasting geochemical and fungal controls on decomposition of lignin and soil carbon at continental scale. Nat Commun 14:2227. https://doi.org/10.1038/s41467-023-37862-6
Hyvönen R, Persson T, Andersson S et al (2008) Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe. Biogeochemistry 89:121–137. https://doi.org/10.1007/s10533-007-9121-3
Joergensen RG (2018) Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fertil Soils 54:559–568. https://doi.org/10.1007/s00374-018-1288-3
Knorr M, Frey SD, Curtis PS (2005) Nirogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257. https://doi.org/10.1890/05-0150
Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162. https://doi.org/10.1016/S0038-0717(01)00158-4
Koricheva J, Gurevitch J, Mengersen K (2013) Handbook of Meta-analysis in Ecology and Evolution. Princeton University Press, Princeton. https://doi.org/10.1515/9781400846184
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. https://doi.org/10.1038/nature16069
Li Y, Li Q, Yang J et al (2017) Home-field advantages of litter decomposition increase with increasing N deposition rates: a litter and soil perspective. Funct Ecol 31:1792–1801. https://doi.org/10.1111/1365-2435.12863
Liang C, Balser TC (2012) Warming and nitrogen deposition lessen microbial residue contribution to soil carbon pool. Nat Commun 3:1222. https://doi.org/10.1038/ncomms2224
Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105. https://doi.org/10.1038/nmicrobiol.2017.105
Liang C, Amelung W, Lehmann J, Kästner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol 25:3578–3590. https://doi.org/10.1111/gcb.14781
Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828. https://doi.org/10.1111/j.1461-0248.2010.01482.x
Liu J, Wu N, Wang H et al (2016) Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology 97:1796–1806. https://doi.org/10.1890/15-1683.1
Liu J, Fang L, Qiu T et al (2023) Disconnection between plant–microbial nutrient limitation across forest biomes. Funct Ecol 37:2271–2281. https://doi.org/10.1111/1365-2435.14361
Lu X, Vitousek PM, Mao Q et al (2021) Nitrogen deposition accelerates soil carbon sequestration in tropical forests. Proc Natl Acad Sci U S A 118:e2020790118. https://doi.org/10.1073/pnas.2020790118
Ma T, Zhu S, Wang Z et al (2018) Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nat Commun 9:3480. https://doi.org/10.1038/s41467-018-05891-1
Ma S, Chen G, Tian D et al (2020) Effects of seven-year nitrogen and phosphorus additions on soil microbial community structures and residues in a tropical forest in Hainan Island. China Geoderma 361:114034. https://doi.org/10.1016/j.geoderma.2019.114034
Ma S, Chen G, Du E et al (2021) Effects of nitrogen addition on microbial residues and their contribution to soil organic carbon in China’s forests from tropical to boreal zone. Environ Pollut 268:115941. https://doi.org/10.1016/j.envpol.2020.115941
Meng X, Zhang X, Li Y et al (2024) Nitrogen fertilizer builds soil organic carbon under straw return mainly via microbial necromass formation. Soil Biol Biochem 188:109223. https://doi.org/10.1016/j.soilbio.2023.109223
Nadelhoffer KJ, Emmett BA, Gundersen P et al (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148. https://doi.org/10.1038/18205
Nave LE, Vance ED, Swanston CW, Curtis PS (2009) Impacts of elevated N inputs on north temperate forest soil C storage, C/N, and net N-mineralization. Geoderma 153:231–240. https://doi.org/10.1016/j.geoderma.2009.08.012
Neff JC, Townsend AR, Gleixner G et al (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917. https://doi.org/10.1038/nature01136
Ni X, Liao S, Tan S et al (2020) The vertical distribution and control of microbial necromass carbon in forest soils. Global Ecol Biol 29:1829–1839. https://doi.org/10.1111/geb.13159
Otto A, Simpson MJ (2006) Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org Geochem 37:385–407. https://doi.org/10.1016/j.orggeochem.2005.12.011
Pisani O, Frey SD, Simpson AJ, Simpson MJ (2015) Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry 123:391–409. https://doi.org/10.1007/s10533-015-0073-8
Quinn-Thomas R, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geosci 3:13–17. https://doi.org/10.1038/ngeo721
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Shao P, Liang C, Lynch L et al (2019) Reforestation accelerates soil organic carbon accumulation: Evidence from microbial biomarkers. Soil Biol Biochem 131:182–190. https://doi.org/10.1016/j.soilbio.2019.01.012
Shen Y, Tian D, Hou J et al (2021) Forest soil acidification consistently reduces litter decomposition irrespective of nutrient availability and litter type. Funct Ecol 35:2753–2762. https://doi.org/10.1111/1365-2435.13925
Simpson AJ, Simpson MJ, Smith E, Kelleher BP (2007) Microbially derived inputs to soil organic matter: are current estimates too low? Environ Sci Technol 41:8070–8076. https://doi.org/10.1021/es071217x
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. https://doi.org/10.2136/sssaj2004.0347
Thevenot M, Dignac M-F, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42:1200–1211. https://doi.org/10.1016/j.soilbio.2010.03.017
Thomas DC, Zak DR, Filley TR (2012) Chronic N deposition does not apparently alter the biochemical composition of forest floor and soil organic matter. Soil Biol Biochem 54:7–13. https://doi.org/10.1016/j.soilbio.2012.05.010
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x
Wang C, Han S, Zhou Y et al (2012) Responses of fine roots and soil N availability to short-term nitrogen fertilization in a broad-leaved korean pine mixed forest in Northeastern China. PLoS One 7:e31042. https://doi.org/10.1371/journal.pone.0031042
Wang R, Goll D, Balkanski Y et al (2017) Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100. Glob Chang Biol 23:4854–4872. https://doi.org/10.1111/gcb.13766
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
Wang JJ, Bowden RD, Lajtha K et al (2019) Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter. Biogeochemistry 142:299–313. https://doi.org/10.1007/s10533-018-00535-4
Wu N, Filley TR, Bai E et al (2015) Incipient changes of lignin and substituted fatty acids under N addition in a Chinese forest soil. Org Geochem 79:14–20. https://doi.org/10.1016/j.orggeochem.2014.12.001
Wu J, Zhang H, Cheng X, Liu G (2023) Nitrogen addition stimulates litter decomposition rate: From the perspective of the combined effect of soil environment and litter quality. Soil Biol Biochem 179:108992. https://doi.org/10.1016/j.soilbio.2023.108992
Xia Z, Yang J, Sang C et al (2020) Phosphorus reduces negative effects of nitrogen addition on soil microbial communities and functions. Microorganisms 8:1828. https://doi.org/10.3390/microorganisms8111828
Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32. https://doi.org/10.1016/j.soilbio.2018.05.001
Xie D, Zhao B, Wang S, Duan L (2020) Benefit of China’s reduction in nitrogen oxides emission to natural ecosystems in East Asia with respect to critical load exceedance. Environ Int 136:105468. https://doi.org/10.1016/j.envint.2020.105468
Xu C, Xu X, Ju C et al (2021) Long-term, amplified responses of soil organic carbon to nitrogen addition worldwide. Glob Chang Biol 27:1170–1180. https://doi.org/10.1111/gcb.15489
Xu A, Li L, Xie J et al (2022) Bacterial diversity and potential functions in response to long-term nitrogen fertilizer on the semiarid loess plateau. Microorganisms 10:1579. https://doi.org/10.3390/microorganisms10081579
Ye C, Chen D, Hall SJ et al (2018) Reconciling multiple impacts of nitrogen enrichment on soil carbon: plant, microbial and geochemical controls. Ecol Lett 21:1162–1173. https://doi.org/10.1111/ele.13083
Yue K, Fornara DA, Heděnec P et al (2023) No tillage decreases GHG emissions with no crop yield tradeoff at the global scale. Soil Tillage Res 228:105643. https://doi.org/10.1016/j.still.2023.105643
Zak DR, Holmes WE, Burton AJ et al (2008) Simulated atmospheric NO3- deposition increases soil organic matter by slowing decomposition. Ecol Appl 18:2016–2027. https://doi.org/10.1890/07-1743.1
Zhang B, Liang C, He H, Zhang X (2013) Variations in soil microbial communities and residues along an altitude gradient on the Northern Slope of Changbai Mountain. China Plos One 8:e66184. https://doi.org/10.1371/journal.pone.0066184
Zhang W, Cui Y, Lu X et al (2016) High nitrogen deposition decreases the contribution of fungal residues to soil carbon pools in a tropical forest ecosystem. Soil Biol Biochem 97:211–214. https://doi.org/10.1016/j.soilbio.2016.03.019
Zhang T, Chen HYH, Ruan H (2018a) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825. https://doi.org/10.1038/s41396-018-0096-y
Zhang X, Xie J, Yang F et al (2018b) Specific responses of soil microbial residue carbon to long-term mineral fertilizer applications to reddish paddy soils. Pedosphere 28:488–496. https://doi.org/10.1016/S1002-0160(17)60335-7
Zhang Y, Tang Z, You Y et al (2023a) Differential effects of forest-floor litter and roots on soil organic carbon formation in a temperate oak forest. Soil Biol Biochem 180:109017. https://doi.org/10.1016/j.soilbio.2023.109017
Zhang Y, Xiong S, You C et al (2023b) Nitrogen addition promotes foliar litterfall and element return in a subtropical forest, southwestern China. J Res 34:939–948. https://doi.org/10.1007/s11676-022-01543-9
Zhao XC, Tian P, Zhang W, Wang QG, Guo P, Wang QK (2024) Nitrogen deposition caused higher increases in plant-derived organic carbon than microbial-derived organic carbon in forest soils. Sci Total Environ 925:171752. https://doi.org/10.1016/j.scitotenv.2024.171752
Zhou Z, Wang C, Zheng M et al (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441. https://doi.org/10.1016/j.soilbio.2017.09.015
Zhu X, Jackson RD, DeLucia EH et al (2020) The soil microbial carbon pump: from conceptual insights to empirical assessments. Glob Chang Biol 26:6032–6039. https://doi.org/10.1111/gcb.15319
Acknowledgements
This research was supported by the National Natural Science Foundation of China (Nos. 32371674, 32192433, 32271633, and 32171587).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare no conflict of interest.
Additional information
Responsible Editor: Guiyao Zhou.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wang, C., Li, X., Zhang, M. et al. Nitrogen deposition enhances accumulation of microbial and plant-derived carbon in forest soils: a global meta-analysis. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06687-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06687-7