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Grazing exclusion increases soil organic C through microbial necromass of root-derived C as traced by 13C labelling photosynthate

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Abstract

Grasslands store large amounts of C; however, the underlying mechanisms of soil C sequestration after grazing exclusion are not well known. This study aimed to elucidate the drivers of soil organic C (SOC) sequestration from plant and microbial residues in temperate grasslands after long-term (~ 40 years) grazing exclusion. We conducted in situ 13C-CO2 labelling experiments in the field and traced 13C in plant-soil systems paired with biomarkers to assess the C input from plants into soils. Long-term grazing exclusion increased all plant and soil pools including shoots, roots, microbial biomass and necromass. 13C allocation in these pools also increased, whereas 13C was lost via respiration as CO2 from soils decreased. 13C incorporation into the soil and microbial biomass increased with 13C allocation into the roots. Grazing exclusion for over 40 years increased the total SOC content by 190%, largely due to increases in fungal necromass C, and there was a minor contribution of lignin phenols to SOC accrual (0.8%). Consequently, grazing exclusion boosts not only aboveground biomass, but also larger roots and rhizodeposition, leading to microbial biomass and necromass formation. Microbial necromass and lignin phenols contribute to SOC accrual under grazing exclusion, and microbial necromass, especially fungal necromass, makes a larger contribution than lignin phenols.

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References

  • 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

    Article  CAS  Google Scholar 

  • Bai YF, Cotrufo MF (2022) Grassland soil carbon sequestration: current understanding, challenges, and solutions. Science 377:603–608

    Article  CAS  PubMed  Google Scholar 

  • Bai XJ, Yang X, Zhang SM, An SS (2021) Newly assimilated carbon allocation in grassland communities under different grazing enclosure times. Biol Fertil Soils 57:563–574

    Article  CAS  Google Scholar 

  • Bardgett RD, Bullock JM, Lavorel S, Manning P, Schaffner U, Ostle N, Chomel M, Durigan G, Fry EL, Johnson D, Lavallee JM, Le Provost G, Luo S, Png K, Sankaran M, Hou X, Zhou H, Ma L, Ren W, Li X, Ding Y, Li Y, Shi H (2021) Combatting global grassland degradation. Nat Rev Earth Environ 2:720–735

    Article  Google Scholar 

  • Birgander J, Olsson PA (2021) Temporal patterns of carbon flow from grassland vegetation to soil microorganisms measured using 13C-labelling and signature fatty acids. Plant Soil 462:245–255

    Article  CAS  Google Scholar 

  • Blaser M, Conrad R (2016) Stable carbon isotope fractionation as tracer of carbon cycling in anoxic soil ecosystems. Curr Opin Biotechnol 41:122–129

    Article  CAS  PubMed  Google Scholar 

  • Chapin FSI, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. In: Chapin FSI, Matson PA, Mooney HA (eds) Part II mechanisms, 2nd edn. Springer, New York, pp 190–193

    Google Scholar 

  • Conant RT, Cerri CEP, Osborne BB, Paustian K (2017) Grassland management impacts on soil carbon stocks: a new synthesis. Ecol Appl 27:662–668

    Article  PubMed  Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob. Chang Biol 19:988–995

    Article  Google Scholar 

  • Cotrufo MF, Ranalli MG, Haddix ML, Six J, Lugato E (2019) Soil carbon storage informed by particulate and mineral-associated organic matter. Nat Geosci 12:989–994

    Article  CAS  Google Scholar 

  • Deng L, Zhang ZN, Shangguan ZP (2014) Long-term fencing effects on plant diversity and soil properties in China. Soil Tillage Res 137:7–15

    Article  Google Scholar 

  • Deng L, Shangguan ZP, Wu GL, Chang XF (2017) Effects of grazing exclusion on carbon sequestration in China’s grassland. Earth-Sci Rev 173:84–95

    Article  CAS  Google Scholar 

  • Deng SH, Zheng XD, Chen XB, Zheng SM, He XY, Ge TD, Kuzyakov Y, Wu JS, Su YR, Hu YJ (2021) Divergent mineralization of hydrophilic and hydrophobic organic substrates and their priming effect in soils depending on their preferential utilization by bacteria and fungi. Biol Fertil Soils 57:65–76

    Article  CAS  Google Scholar 

  • Deng L, Shangguan ZP, Bell SM, Soromotin AV, Peng CH, An SS, Wu X, Xu XL, Wang KB, Li JP, Tang ZS, Yan WM, Zhang FB, Li JW, Wu JZ, Kuzyakov Y (2023) Carbon in Chinese grasslands: meta-analysis and theory of grazing effects. Carbon Res 1:51

    Google Scholar 

  • Du CJ, Gao YH (2021) Grazing exclusion alters ecological stoichiometry of plant and soil in degraded alpine grassland. Agric Ecosyst Environ 308:107256

    Article  CAS  Google Scholar 

  • Feyisa K, Beyene S, Angassa A, Said MY, de Leeuw J, Abebe A, Megersa B (2017) Effects of enclosure management on carbon sequestration, soil properties and vegetation attributes in East African rangelands. CATENA 159:9–19

    Article  Google Scholar 

  • Frostegard A, Baath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Hafner S, Unteregelsbacher S, Seeber E, Lena B, Xu XL, Li XG, Guggenberger G, Miehe G, Kuzyakov Y (2012) Effect of grazing on carbon stocks and assimilate partitioning in a tibetan montane pasture revealed by 13CO2 pulse labeling. Glob Chang Biol 18:528–538

    Article  Google Scholar 

  • Hall SJ, Huang W, Timokhin VI, Hammel KE (2020) Lignin lags, leads, or limits the decomposition of litter and soil organic carbon. Ecology 101:e03113

    Article  PubMed  Google Scholar 

  • He LY, Rodrigues JLM, Soudzilovskaia NA, Barcelo M, Olsson PA, Song CC, Tedersoo L, Yuan FH, Yuan FM, Lipson DA, Xu XF (2020) Global biogeography of fungal and bacterial biomass carbon in topsoil. Soil Biol Biochem 151:108024

    Article  CAS  Google Scholar 

  • Hu YT, Zheng Q, Noll L, Zhang SS, Wanek W (2020) Direct measurement of the in situ decomposition of microbial-derived soil organic matter. Soil Biol Biochem 141:107660

    Article  CAS  Google Scholar 

  • Huang W, Kuzyakov Y, Niu S, Luo Y, Sun B, Zhang J, Liang Y (2023) Drivers of microbially and plant-derived carbon in topsoil and subsoil. Glob Chang Biol 29:6188–6200

    Article  CAS  PubMed  Google Scholar 

  • ISSS Working Group WRB (1998) World reference bases for soil resources: introduction. In: Deckers JA, Nachtergaele FO, Spaargaren OC (eds) International Society of Soil Science (ISSS), International Soil Reference and Information Centre (ISRIC), and Food and Agriculture Organization of the United Nations, 1st edn. FAO, Acco, Leuven, Belgio, p 165

    Google Scholar 

  • Jex CN, Pate GH, Blyth AJ, Spencer RGM, Hernes PJ, Khan SJ, Baker A (2014) Lignin biogeochemistry: from modern processes to quaternary archives. Quat Sci Rev 87:46–59

    Article  Google Scholar 

  • Joergensen RG (2018) Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fertil Soils 54:559–568

    Article  CAS  Google Scholar 

  • Kopittke PM, Hernandez-Soriano MC, Dalal RC, Finn D, Menzies NW, Hoeschen C, Mueller CW (2018) Nitrogen-rich microbial products provide new organo-mineral associations for the stabilization of soil organic matter. Glob Chang Biol 24:1762–1770

    Article  PubMed  Google Scholar 

  • Kuzyakov Y, Biryukova OV, Kuznetzova TV, Mölter K, Kandeler E, Stahr K (2002) Carbon partitioning in plant and soil, carbon dioxide fluxes and enzyme activities as affected by cutting ryegrass. Biol Fertil Soils 35:348–358

    Article  CAS  Google Scholar 

  • Lavallee JM, Soong JL, Cotrufo MF (2020) Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Glob Chang Biol 26:261–273

    Article  PubMed  Google Scholar 

  • Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Amelung W, Lehmann J, Kaestner M (2019) Quantitative assessment of microbial necromass contribution to soil organic matter. Glob Chang Biol 25:3578–3590

    Article  PubMed  Google Scholar 

  • Liu SB, Zamanian K, Schleuss PM, Zarebanadkouki M, Kuzyakov Y (2018) Degradation of tibetan grasslands: consequences for carbon and nutrient cycles. Agric Ecosyst Environ 252:93–104

    Article  CAS  Google Scholar 

  • Liu M, Ouyang SN, Tian YQ, Wen SH, Zhao Y, Li XB, Baoyin TT, Kuzyakov Y, Xu XL (2021) Effects of rotational and continuous overgrazing on newly assimilated C allocation. Biol Fertil Soils 57:193–202

    Article  CAS  Google Scholar 

  • Lorenz K, Lal R (2018) Carbon Sequestration in Grassland soils. In: Lorenz K, Lal R (eds) Carbon sequestration in agricultural ecosystems. Springer International Publishing, Cham, City, State, pp 175–209

    Chapter  Google Scholar 

  • Ma T, Zhu SS, Wang ZH, Chen DM, Dai GH, Feng BW, Su XY, Hu HF, Li KH, Han WX, Liang C, Bai YF, Feng XJ (2018) Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nat Commun 9:3480

    Article  PubMed  PubMed Central  Google Scholar 

  • Mganga KZ, Sietiö O, Meyer N, Poeplau C, Adamczyk S, Biasi C, Kalu S, Räsänen M, Ambus P, Fritze H, Pellikka PKE, Karhu K (2022) Microbial carbon use efficiency along an altitudinal gradient. Soil Biol Biochem 173:108799

    Article  CAS  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Bruecken B, Kaestner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    Article  CAS  Google Scholar 

  • Moore JAM, Sulman BN, Mayes MA, Patterson CM, Classen AT (2020) Plant roots stimulate the decomposition of complex, but not simple, soil carbon. Funct Ecol 34:899–910

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total Carbon, Organic Carbon, and Organic Matter. In: Nelson DW, Sommers LE (eds) Methods of soil analysis. American Society of Agronomy, Madison, WI, pp 961–1010

    Google Scholar 

  • Neurath RA, Pett-Ridge J, Chu-Jacoby I, Herman D, Whitman T, Nico PS, Lipton AS, Kyle J, Tfaily MM, Thompson A, Firestone MK (2021) Root carbon interaction with soil minerals is dynamic, leaving a legacy of microbially derived residues. Environ Sci Technol 55:13345–13355

    CAS  PubMed  Google Scholar 

  • Otto A, Simpson MJ (2006) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 80:121–142

    Article  CAS  Google Scholar 

  • Panchal P, Preece C, Peñuelas J, Giri J (2022) Soil carbon sequestration by root exudates. Trends Plant Sci 27:749–757

    Article  CAS  PubMed  Google Scholar 

  • Pang R, Xu XL, Tian YQ, Cui XY, Ouyang H, Kuzyakov Y (2021) In-situ 13CO2 labeling to trace carbon fluxes in plant-soil-microorganism systems: review and methodological guideline. Rhizosphere 20:100441

    Article  Google Scholar 

  • Pausch J, Kuzyakov Y (2018) Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scales. Glob Chang Biol 24:1–12

    Article  PubMed  Google Scholar 

  • Qin GM, He WJ, Sanders CJ, Zhang JF, Zhou JE, Wu JT, Lu Z, Yu MX, Li YW, Li YX, Lambers H, Li Z, Wang FM (2024) Contributions of plant- and microbial-derived residuals to mangrove soil carbon stocks: implications for blue carbon sequestration. Funct Ecol 00:1–13

    Google Scholar 

  • Qu Q, Zhang J, Hai X, Wu J, Fan J, Wang D, Li J, Shangguan Z, Deng L (2022) Long-term fencing alters the vertical distribution of soil δ13C and SOC turnover rate: revealed by MBC-δ13C. Agric Ecosyst Environ 339:108119

    Article  CAS  Google Scholar 

  • Qu Q, Deng L, Shangguan ZP, Sun J, He JS, Wang KB, Zhou ZC, Li JW, Peñuelas J (2024) Belowground C sequestrations response to grazing exclusion in global grasslands: dynamics and mechanisms. Agric Ecosyst Environ 360:108771

    Article  CAS  Google Scholar 

  • Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155

    Article  CAS  Google Scholar 

  • Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–1377

    Article  CAS  Google Scholar 

  • Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, (2nd ed) USDA-NRCS, Agricultural Handbook, vol. 436. U.S. Gov. Print. Office, Washington, DC

  • Sokol NW, Sanderman J, Bradford MA (2019) Pathways of mineral-associated soil organic matter formation: integrating the role of plant carbon source, chemistry, and point of entry. Glob Chang Biol 25:12–24

    Article  PubMed  Google Scholar 

  • Tao F, Huang Y, Hungate BA, Manzoni S, Frey SD, Schmidt MWI, Reichstein M, Carvalhais N, Ciais P, Jiang L, Lehmann J, Wang Y, Houlton BZ, Ahrens B, Mishra U, Hugelius G, Hocking TD, Lu X, Shi Z, Viatkin K, Vargas R, Yigini Y, Omuto C, Malik AA, Peralta G, Cuevas-Corona R, Di Paolo LE, Luotto I, Liao C, Liang Y, Saynes VS, Huang X, Luo Y (2023) Microbial carbon use efficiency promotes global soil carbon storage. Nature 618:981–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thevenot M, Dignac M, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42:1200–1211

    Article  CAS  Google Scholar 

  • Thuriès L, Larré-Larrouy MC, Feller C (2000) Influences of organic fertilization and solarization in a greenhouse on particle-size fractions of a Mediterranean sandy soil. Biol Fertil Soils 32:449–457

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Villarino SH, Pinto P, Jackson RB, Pineiro G (2021) Plant rhizodeposition: a key factor for soil organic matter formation in stable fractions. Sci Adv 7:eabd3176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang BR, An SS, Liang C, Liu Y, Kuzyakov Y (2021) Microbial necromass as the source of soil organic carbon in global ecosystems. Soil Biol Biochem 162:108422

    Article  CAS  Google Scholar 

  • Wang QC, Yang LM, Song G, Jin SS, Hu HW, Wu FZ, Zheng Y (2022) The accumulation of microbial residues and plant lignin phenols are more influenced by fertilization in young than mature subtropical forests. Ecol Manage 509:120074

    Article  Google Scholar 

  • Wang XT, Chen RR, Petropoulos E, Yu BQ, Lin XG, Feng YZ (2023) Root–derived C distribution drives N transport and transformation after 13C and 15N labelling on paddy and upland soils. Biol Fertil Soils 59:513–525

    Article  CAS  Google Scholar 

  • Wei L, Razavi BS, Wang WQ, Zhu ZK, Liu SL, Wu JS, Kuzyakov Y, Ge TD (2019) Labile carbon matters more than temperature for enzyme activity in paddy soil. Soil Biol Biochem 135:134–143

    Article  CAS  Google Scholar 

  • White PR, Murray S, Rothweder M (2000) Grassland ecosystems. In: White PR, Murray S, Rothweder M (eds) Pilot analysis of global ecosystems. World Resources Institute, Washington, DC, pp 13–15

    Google Scholar 

  • Wilson CH, Strickland MS, Hutchings JA, Bianchi TS, Flory SL (2018) Grazing enhances belowground carbon allocation, microbial biomass, and soil carbon in a subtropical grassland. Glob Chang Biol 24:2997–3009

    Article  PubMed  Google Scholar 

  • Xia YH, Chen XB, Zheng XD, Deng SH, Hu YJ, Zheng SM, He XY, Wu JS, Kuzyakov Y, Su YR (2020) Preferential uptake of hydrophilic and hydrophobic compounds by bacteria and fungi in upland and paddy soils. Soil Biol Biochem 148:107879

    Article  CAS  Google Scholar 

  • Xia S, Song Z, Wang W, Fan Y, Guo L, Van Zwieten L, Hartley IP, Fang Y, Wang Y, Zhang Z, Liu CQ, Wang H (2023) Patterns and determinants of plant-derived lignin phenols in coastal wetlands: implications for organic C accumulation. Funct Ecol 37:1067–1081

    Article  CAS  Google Scholar 

  • Xu X, Kuzyakov Y, Wanek W, Richter A (2008) Root-derived respiration and non-structural carbon of rice seedlings. Eur J Soil Biol 44:22–29

    Article  CAS  Google Scholar 

  • Yang Y, Dou YX, Wang BR, Wang YQ, Liang C, An SS, Soromotin A, Kuzyakov Y (2022) Increasing contribution of microbial residues to soil organic carbon in grassland restoration chronosequence. Soil Biol Biochem 170:108688

    Article  CAS  Google Scholar 

  • Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi SJ, Cho HJ, Karaoz U, Loque D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480

    Article  CAS  PubMed  Google Scholar 

  • Zhang XD, Amelung W (1996) Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biol Biochem 28:1201–1206

    Article  CAS  Google Scholar 

  • Zhang C, Liu GB, Song ZL, Wang J, Guo L (2018) Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands. Soil Biol Biochem 124:47–58

    Article  CAS  Google Scholar 

  • Zhao JX, Luo TX, Li RC, Li X, Tian LH (2016) Grazing effect on growing season ecosystem respiration and its temperature sensitivity in alpine grasslands along a large altitudinal gradient on the central tibetan Plateau. Agric Meteorol 218:114–121

    Article  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (42277471, U2243225), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23070201), the Scientific and Technological Innovation Project of Shaanxi Forestry Academy of Sciences (SXLK2021-0206), the Fundamental Research Funds for the Central Universities (2023HHZX002), Peoples Friendship University of Russia (RUDN University), the West-Siberian Interregional Science and Education Center’s project No. 89-DON (1), and Project CarboRus (075-15-2021-610).

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Qu, Q., Deng, L., Gunina, A. et al. Grazing exclusion increases soil organic C through microbial necromass of root-derived C as traced by 13C labelling photosynthate. Biol Fertil Soils 60, 407–420 (2024). https://doi.org/10.1007/s00374-024-01807-y

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