Microbial resource-use strategies mediate soil carbon turnover across forest succession

Wenya Du , Shuxian Jia , Miriam Muñoz-Rojas , Yanghui He , Lingyan Zhou , Guiyao Zhou , Kaiyan Zhai , Minhuang Wang , Zhenghu Zhou , Ruiqiang Liu , Pete Smith , Xuhui Zhou

Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) : 155

PDF
Journal of Forestry Research ›› 2026, Vol. 37 ›› Issue (1) :155 DOI: 10.1007/s11676-026-02094-z
Original Paper
research-article
Microbial resource-use strategies mediate soil carbon turnover across forest succession
Author information +
History +
PDF

Abstract

Forest development is known to increase soil organic carbon (C) storage, yet the understanding of the stability of this accumulated C remains elusive. To address this gap, the study examined how soil C turnover-a key indicator of stability-changes with forest development, by combining a global meta-analysis with two long-term forest chronosequences spanning subtropical and temperate regions. Global data analysis revealed that soil C stability increased with forests development, showing decreasing soil C turnover rates that were primarily driven by increasing fungi: bacteria ratio. Across two long-term forest chronosequences at Changbai Mountain and Dinghu Mountain, soil C turnover declined with forest succession and was positively associated with fungal K/r-strategies, whereas bacterial community attributes exhibited weak relationships. Notably, conventional indicators of physical C protection, such as the mineral-associated to particulate organic C ratio, along with microbial indicators (microbial biomass, extracellular enzyme activities, and respiration rates), explained only a limited proportion of the variation in soil C turnover. These findings highlight that microbial resource-use strategies are more critical predictors of forest soil C stability than traditional physical or microbial indicators.

Keywords

Carbon cycling / Ecological strategy / Microbial community / Fungi: bacteria interactions / Soil organic matter

Cite this article

Download citation ▾
Wenya Du, Shuxian Jia, Miriam Muñoz-Rojas, Yanghui He, Lingyan Zhou, Guiyao Zhou, Kaiyan Zhai, Minhuang Wang, Zhenghu Zhou, Ruiqiang Liu, Pete Smith, Xuhui Zhou. Microbial resource-use strategies mediate soil carbon turnover across forest succession. Journal of Forestry Research, 2026, 37 (1) : 155 DOI:10.1007/s11676-026-02094-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Bossio DA, Cook-Patton SC, Ellis PW, Fargione J, Sanderman J, Smith P, Wood S, Zomer RJ, von Unger M, Emmer IM, Griscom BW. The role of soil carbon in natural climate solutions. Nat Sustain, 2020, 3(5): 391-398.

[2]

Bradford MA, Wieder WR, Bonan GB, Fierer N, Raymond PA, Crowther TW. Managing uncertainty in soil carbon feedbacks to climate change. Nat Clim Change, 2016, 6(8): 751-758.

[3]

Brookes PC, Landman A, Pruden G, Jenkinson DS. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem, 1985, 17(6): 837-842.

[4]

Cao TT, Fang Y, Chen YR, Kong XS, Yang JB, Alharbi H, Kuzyakov Y, Tian XJ. Synergy of saprotrophs with mycorrhiza for litter decomposition and hotspot formation depends on nutrient availability in the rhizosphere. Geoderma, 2022, 410: 115662.

[5]

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA, 2011, 108(supplement_1): 4516-4522.

[6]

Chen HY, Jing QF, Liu X, Zhou XH, Fang CM, Li B, Zhou SR, Nie M. Microbial respiratory thermal adaptation is regulated by r-/K-strategy dominance. Ecol Lett, 2022, 25(11): 2489-2499.

[7]

Chen C, Delgado-Baquerizo M, Zhou GY, Rillig MC, Li B, Fang CM, Li JQ, Nie M. Multiple global change stressors boost soil greenhouse gas emissions worldwide. Glob Change Biol, 2026, 32: e70633.

[8]

Curtis PS, Gough CM. Forest aging, disturbance and the carbon cycle. New Phytol, 2018, 219(4): 1188-1193.

[9]

Davidson EA, Janssens IA. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, 2006, 440(7081): 165-173.

[10]

Don A, Schumacher J, Freibauer A. Impact of tropical land-use change on soil organic carbon stocks–a meta-analysis. Glob Change Biol, 2011, 17(4): 1658-1670.

[11]

Fabian J, Zlatanovic S, Mutz M, Premke K. Fungal–bacterial dynamics and their contribution to terrigenous carbon turnover in relation to organic matter quality. ISME J, 2017, 11(2): 415-425.

[12]

Fernandez CW, See CR, Kennedy PG. Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition. New Phytol, 2020, 226(2): 569-582.

[13]

Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology, 2007, 88(6): 1354-1364.

[14]

Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature, 2007, 450(7167): 277-280.

[15]

Friedlingstein P, O’Sullivan M, Jones MW, Andrew RM, Hauck J, Landschützer P, Le Quéré C, Li HM, Luijkx IT, Olsen A, Peters GP, Peters W, Pongratz J, Schwingshackl C, Sitch S, Canadell JG, Ciais P, Jackson RB, Alin SR, Arneth A, Arora V, Bates NR, Becker M, Bellouin N, Berghoff CF, Bittig HC, Bopp L, Cadule P, Campbell K, Chamberlain MA, Chandra N, Chevallier F, Chini LP, Colligan T, Decayeux J, Djeutchouang LM, Dou XY, Duran Rojas C, Enyo K, Evans W, Fay AR, Feely RA, Ford DJ, Foster A, Gasser T, Gehlen M, Gkritzalis T, Grassi G, Gregor L, Gruber N, Gürses Ö, Harris I, Hefner M, Heinke J, Hurtt GC, Iida Y, Ilyina T, Jacobson AR, Jain AK, Jarníková T, Jersild A, Jiang F, Jin Z, Kato E, Keeling RF, Klein Goldewijk K, Knauer J, Korsbakken JI, Lan X, Lauvset SK, Lefèvre N, Liu Z, Liu JJ, Ma L, Maksyutov S, Marland G, Mayot N, McGuire PC, Metzl N, Monacci NM, Morgan EJ, Nakaoka SI, Neill C, Niwa Y, Nützel T, Olivier L, Ono T, Palmer PI, Pierrot D, Qin ZC, Resplandy L, Roobaert A, Rosan TM, Rödenbeck C, Schwinger J, Smallman TL, Smith SM, Sospedra-Alfonso R, Steinhoff T, Sun Q, Sutton AJ, Séférian R, Takao S, Tatebe H, Tian HQ, Tilbrook B, Torres O, Tourigny E, Tsujino H, Tubiello F, van der Werf G, Wanninkhof R, Wang XH, Yang DX, Yang XJ, Yu Z, Yuan WP, Yue X, Zaehle S, Zeng N, Zeng JY. Global carbon budget 2024. Earth Syst Sci Data, 2025, 17(3): 965-1039.

[16]

Hamdi S, Chevallier T, Ben Aïssa N, Ben Hammouda M, Gallali T, Chotte JL, Bernoux M. Short-term temperature dependence of heterotrophic soil respiration after one-month of pre-incubation at different temperatures. Soil Biol Biochem, 2011, 43(9): 1752-1758.

[17]

He YH, Zhou XH, Jia Z, Zhou LY, Chen HY, Liu RQ, Du ZG, Zhou GY, Shao JJ, Ding JX, Chen KL, Hartley IP. Apparent thermal acclimation of soil heterotrophic respiration mainly mediated by substrate availability. Glob Change Biol, 2023, 29(4): 1178-1187.

[18]

Huang WJ, Han TF, Liu JX, Wang GS, Zhou GY. Changes in soil respiration components and their specific respiration along three successional forests in the subtropics. Funct Ecol, 2016, 30(8): 1466-1474.

[19]

Jastrow J, Six J. Organic matter turnover. Encyclopedia of soil science, 2005, 2CRC Press

[20]

Jia SX, Zhou XH, Fu YL, Zhou GY, Zhou LY, Wang XX, Jiang Z, Sardans J, Penuelas J. Microbial life history mediates the drought-induced decrease in wood decomposition in subtropical forests. Ecol Lett, 2025, 28(5): e70133.

[21]

Lal R. Soil carbon sequestration impacts on global climate change and food security. Science, 2004, 304(5677): 1623-1627.

[22]

Lehmann J, Kleber M. The contentious nature of soil organic matter. Nature, 2015, 528(7580): 60-68.

[23]

Li H, Yang S, Semenov MV, Yao F, Ye J, Bu RC, Ma RA, Lin JJ, Kurganova I, Wang XG, Deng Y, Kravchenko I, Jiang Y, Kuzyakov Y. Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Glob Change Biol, 2021, 27(12): 2763-2779.

[24]

Li C, Shi LN, Wang KC, Liu BR, Liao JJ, An ZF, Chang SX. Crop rotation differentially increases soil bacterial and fungal diversities in global croplands: a meta-analysis. Nat Commun, 2025, 16: 11686.

[25]

Liang GP. Global pattern of warming effects on microbial respiration is explained by soil microbial biomass carbon and nitrogen. CATENA, 2025, 250: 108728.

[26]

Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol, 2007, 173(3): 611-620.

[27]

Liu RQ, Zhou XH, Wang JW, Shao JJ, Fu YL, Liang C, Yan ER, Chen XY, Wang XH, Bai SH. Differential magnitude of rhizosphere effects on soil aggregation at three stages of subtropical secondary forest successions. Plant Soil, 2019, 436(1): 365-380.

[28]

Liu L, Zhu K, Krause SMB, Li SP, Wang X, Zhang ZC, Shen MW, Yang QS, Lian JY, Wang XH, Ye WH, Zhang J. Changes in assembly processes of soil microbial communities during secondary succession in two subtropical forests. Soil Biol Biochem, 2021, 154: 108144.

[29]

Liu RQ, He YH, Zhou GY, Shao JJ, Zhou LY, Zhou HM, Li N, Song BQ, Liang C, Yan ER, Chen XY, Wang XH, Wang MH, Bai SH, Zhou XH, Phillips RP. Mycorrhizal effects on decomposition and soil CO2 flux depend on changes in nitrogen availability during forest succession. J Ecol, 2021, 109(11): 3929-3943.

[30]

Liu RQ, He YH, Du ZG, Zhou GY, Zhou LY, Wang XX, Li N, Yan ER, Feng XJ, Liang C, Zhou XH. Root production and microbe-derived carbon inputs jointly drive rapid soil carbon accumulation at the early stages of forest succession. Forests, 2022, 13(12): 2130.

[31]

Liu SG, Sun ZL, Tian P, Zhao XC, Zhou GY, Dietrich P, Wang QK, Delgado-Baquerizo M. Temperature legacies predict microbial metabolic quotient across forest biomes. Glob Ecol Biogeogr, 2023, 32(1): 107-119.

[32]

Liu RQ, Zhou XH, He YH, Du ZG, Chen HY, Fu YL, Guo LQ, Zhou GY, Zhou LY, Li J, Chai H, Huang CJ, Delgado-Baquerizo M. A transition from arbuscular to ectomycorrhizal forests halts soil carbon sequestration during subtropical forest rewilding. Sci Total Environ, 2024, 946: 174330.

[33]

Malik AA, Martiny JBH, Brodie EL, Martiny AC, Treseder KK, Allison SD. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J, 2020, 14(1): 1-9.

[34]

McGuire KL, Treseder KK. Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem, 2010, 42(4): 529-535.

[35]

Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res, 2019, 47(D1): D259-D264.

[36]

Novick KA, Katul GG. The duality of reforestation impacts on surface and air temperature. J Geophys Res Biogeosci, 2020, 125(4): e2019JG005543.

[37]

Odum EP. The strategy of ecosystem development. Science, 1969, 164: 262-270.

[38]

Olsen SR, Sommers LE (1982) Phosphorus. In: Methods of soil analysis, pp 403–430

[39]

Piton G, Allison SD, Bahram M, Hildebrand F, Martiny JBH, Treseder KK, Martiny AC. Life history strategies of soil bacterial communities across global terrestrial biomes. Nat Microbiol, 2023, 8(11): 2093-2102.

[40]

R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

[41]

Saiya-Cork KR, Sinsabaugh RL, Zak DR. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem, 2002, 34(9): 1309-1315.

[42]

Schimel JP, Schaeffer SM. Microbial control over carbon cycling in soil. Front Microbiol, 2012, 3: 348.

[43]

Schimel JP, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem, 2003, 35(4): 549-563.

[44]

Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J, 2012, 6(9): 1749-1762.

[45]

Su XL, Su X, Zhou GY, Du ZG, Yang SC, Ni MY, Qin H, Huang ZQ, Zhou XH, Deng J. Drought accelerated recalcitrant carbon loss by changing soil aggregation and microbial communities in a subtropical forest. Soil Biol Biochem, 2020, 148: 107898.

[46]

Tong D, Xiao HB, Li ZW, Nie XD, Huang JQ. Stand ages adjust fluctuating patterns of soil respiration and decrease temperature sensitivity after revegetation. Soil Sci Soc Am J, 2020, 84(3): 760-774.

[47]

Tripathi BM, Piñeiro J, Dang C, Brzostek E, Morrissey EM. Mycorrhiza—saprotroph interactions and carbon cycling in the rhizosphere. Glob Change Biol, 2025, 31(4): e70173.

[48]

Wang MH, Xu ZH, Huang ZQ, Zhang YL. Soil carbon accrual under harvest residue retention modulated by the copiotroph-oligotroph spectrum in bacterial community. J Soils Sediments, 2022, 22(9): 2459-2474.

[49]

Wang MM, Yu BB, Shen ZF, Zhao LN, Zhang J, Cui Y, Fan ZJ, Zu WZ, Dai GH, Zhang WX, Fu SL, Shao YH. Changes in soil and litter properties differentially influence soil nematode communities across three successional stages in two contrasting forests. Land Degrad Dev, 2023, 34(11): 3196-3207.

[50]

Wang HC, Wang H, Crowther TW, Isobe K, Reich PB, Tateno R, Shi WY. Metagenomic insights into inhibition of soil microbial carbon metabolism by phosphorus limitation during vegetation succession. ISME Commun, 2024, 4: ycae128.

[51]

Whalen ED, Grandy AS, Geyer KM, Morrison EW, Frey SD. Microbial trait multifunctionality drives soil organic matter formation potential. Nat Commun, 2024, 15: 10209.

[52]

Xiang HM, Luo XZ, Zhang LL, Hou EQ, Li J, Zhu QD, Wen DZ. Forest succession accelerates soil carbon accumulation by increasing recalcitrant carbon stock in subtropical forest topsoils. CATENA, 2022, 212: 106030.

[53]

Yan ER, Wang XH, Guo M, Zhong Q, Zhou W, Li YF. Temporal patterns of net soil N mineralization and nitrification through secondary succession in the subtropical forests of Eastern China. Plant Soil, 2009, 320(1): 181-194.

[54]

Yan XL, Zhou LY, Chen YM, Liu RQ, Guo LQ, Li N, Kang A, Zhai KY, Zhou GY, Zhou XH. Ectomycorrhizal fungi explain more variation in rhizosphere nutrient availability than root traits in temperate forests. Appl Soil Ecol, 2025, 207: 105923.

[55]

Yu WJ, Huang WJ, Weintraub-Leff SR, Hall SJ. Where and why do particulate organic matter (POM) and mineral-associated organic matter (MAOM) differ among diverse soils?. Soil Biol Biochem, 2022, 172: 108756.

[56]

Yu XS, Wang LL, Wang Q, Zhou GY, Sun H, Guggenberger G, Li YF, Yakov K, Luo Y, Fu YY. Faster soil organic carbon turnover in MAOM versus POM: straw input causes larger microbial driven soil organic carbon decomposition but higher straw accumulation in MAOM. Soil Tillage Res, 2025, 251: 106549.

[57]

Zeng XM, Feng J, Yu DL, Wen SH, Zhang QG, Huang QY, Delgado-Baquerizo M, Liu YR. Local temperature increases reduce soil microbial residues and carbon stocks. Glob Change Biol, 2022, 28(21): 6433-6445.

[58]

Zhao YQ, Xu YL, Cha XY, Zhang P, Li YF, Cai AD, Zhou ZH, Yang GH, Han XH, Ren CJ. A global meta-analysis of land use change on soil mineral-associated and particulate organic carbon. Glob Change Biol, 2025, 31(3): e70111.

[59]

Zheng HF, Vesterdal L, Schmidt IK, Rousk J. Ecoenzymatic stoichiometry can reflect microbial resource limitation, substrate quality, or both in forest soils. Soil Biol Biochem, 2022, 167: 108613.

[60]

Zhou GY, Liu SG, Li ZA, Zhang DQ, Tang XL, Zhou CY, Yan JH, Mo JM. Old-growth forests can accumulate carbon in soils. Science, 2006, 314(5804): 1417.

[61]

Zhou T, Shi PJ, Jia GS, Dai YJ, Zhao X, Shangguan W, Du L, Wu H, Luo YQ. Age-dependent forest carbon sink: estimation via inverse modeling. JGR Biogeosci, 2015, 120(12): 2473-2492.

[62]

Zhou ZH, Wang CK, Zheng MH, Jiang LF, Luo YQ. Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem, 2017, 115: 433-441.

[63]

Zhou ZH, Wang CK, Luo YQ. Effects of forest degradation on microbial communities and soil carbon cycling: a global meta-analysis. Glob Ecol Biogeogr, 2018, 27(1): 110-124.

[64]

Zhou GY, Zhou XH, Liu RQ, Du ZG, Zhou LY, Li SS, Liu HY, Shao JJ, Wang JW, Nie YY, Gao J, Wang MH, Zhang MY, Wang XH, Bai SH (2020) Soil fungi and fine root biomass mediate drought-induced reductions in soil respiration. Funct Ecol 34(12):2634–2643. https://doi.org/10.1111/fec.v34.1210.1111/1365-2435.13677

[65]

Zhu XY, Fang X, Wang LF, Xiang WH, Alharbi HA, Lei PF, Kuzyakov Y. Regulation of soil phosphorus availability and composition during forest succession in subtropics. For Ecol Manag, 2021, 502: 119706.

RIGHTS & PERMISSIONS

Northeast Forestry University

PDF

0

Accesses

0

Citation

Detail

Sections
Recommended

/