College of Resources and Environmental Sciences; National Academy of Agriculture Green Development; Key Laboratory of Plant-Soil Interactions (Ministry of Education), China Agricultural University, Beijing 100193, China
● The contribution of fungal necromass C to SOC increased with aggregate sizes.
● Bacterial necromass had a higher proportion to SOC in silt and clay.
● Cropland management increased microbial necromass in macro- and microaggregates.
● Greater fungal necromass increases were found in macroaggregates under manure input and no or reduced tillage.
● Cover crops increased bacterial necromass in small macroaggregates.
The interactions of soil microorganisms and structure regulate the degradation and stabilization processes of soil organic carbon (SOC). Microbial necromass is a persistent component of SOC, and its magnitude of accumulation dependent on management and aggregate sizes. A meta-analysis of 121 paired measurements was conducted to evaluate the management effects on contributions of microbial necromass to SOC depending on aggregate fractions. Results showed that the contribution of fungal necromass to SOC increased with aggregate sizes, while bacterial necromass had a higher proportion in silt and clay. Cropland management increased total and fungal necromass in large macroaggregates (47.1% and 45.6%), small macroaggregates (44.0% and 44.2%), and microaggregates (38.9% and 37.6%). Cropland management increased bacterial necromass independent of aggregate fraction sizes. Greater fungal necromass was increased in macroaggregates in response to manure (26.6% to 28.5%) and no or reduced tillage (68.0% to 73.5%). Cover crops increased bacterial necromass by 25.1% in small macroaggregates. Stimulation of microbial necromass was proportional to the increases of SOC within soil aggregates, and the correlation was higher in macroaggregates. Increasing microbial necromass accumulation in macroaggregates can, therefore, be considered as a central component of management strategies that aim to accelerate C sequestration in agricultural soils.
J, Lehmann D A, Bossio I, Kögel-Knabner M C Rillig . The concept and future prospects of soil health. Nature Reviews. Earth & Environment, 2020, 1(10): 544–553 https://doi.org/10.1038/s43017-020-0080-8
pmid: 33015639
2
E, Hoffland T W, Kuyper R N J, Comans R E Creamer . Eco-functionality of organic matter in soils. Plant and Soil, 2020, 455(1−2): 1−22
R Lal . Soil carbon sequestration to mitigate climate change. Geoderma, 2004, 123(1−2): 1−22
5
M, Lessmann G H, Ros M D, Young Vries W de . Global variation in soil carbon sequestration potential through improved cropland management. Global Change Biology, 2022, 28(3): 1162–1177 https://doi.org/10.1111/gcb.15954
pmid: 34726814
6
J, Six P, Callewaert S, Lenders Gryze S, De S J, Morris E G, Gregorich E A, Paul K Paustian . Measuring and understanding carbon storage in afforested soils by physical fractionation. Soil Science Society of America Journal, 2002, 66(6): 1981–1987 https://doi.org/10.2136/sssaj2002.1981
7
M E, Schutter R P Dick . Microbial community profiles and activities among aggregates of winter fallow and cover-cropped soil. Soil Science Society of America Journal, 2002, 66(1): 142–153 https://doi.org/10.2136/sssaj2002.1420
8
M C, Rillig L A, Muller A Lehmann . Soil aggregates as massively concurrent evolutionary incubators. ISME Journal, 2017, 11(9): 1943–1948 https://doi.org/10.1038/ismej.2017.56
pmid: 28409772
9
K M, Buckeridge C, Creamer J Whitaker . Deconstructing the microbial necromass continuum to inform soil carbon sequestration. Functional Ecology, 2022, 36(6): 1396–1410 https://doi.org/10.1111/1365-2435.14014
10
X L, Ding C, Liang B, Zhang Y R, Yuan X Z Han . Higher rates of manure application lead to greater accumulation of both fungal and bacterial residues in macroaggregates of a clay soil. Soil Biology & Biochemistry, 2015, 84: 137–146 https://doi.org/10.1016/j.soilbio.2015.02.015
11
C, Liang J P, Schimel J D Jastrow . The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology, 2017, 2(8): 17105 https://doi.org/10.1038/nmicrobiol.2017.105
pmid: 28741607
12
G, Angst K E, Mueller K G J, Nierop M J Simpson . Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter.. Soil Biology & Biochemistry, 2021, 156: 108189 https://doi.org/10.1016/j.soilbio.2021.108189
13
X, Lu E, Hou J, Guo F S, Gilliam J, Li S, Tang Y Kuang . Nitrogen addition stimulates soil aggregation and enhances carbon storage in terrestrial ecosystems of China: a meta-analysis. Global Change Biology, 2021, 27(12): 2780–2792 https://doi.org/10.1111/gcb.15604
pmid: 33742519
14
R, Huang M, Lan J, Liu M Gao . Soil aggregate and organic carbon distribution at dry land soil and paddy soil: the role of different straws returning. Environmental Science and Pollution Research International, 2017, 24(36): 27942–27952 https://doi.org/10.1007/s11356-017-0372-9
pmid: 28988326
15
H, Zheng W, Liu J, Zheng Y, Luo R, Li H, Wang H Qi . Effect of long-term tillage on soil aggregates and aggregate-associated carbon in black soil of Northeast China. PLoS One, 2018, 13(6): e0199523 https://doi.org/10.1371/journal.pone.0199523
pmid: 29953462
16
D, Topps M I U, Khabir H, Abdelmagid T, Jackson J, Iqbal B K, Robertson Z H, Pervaiz M Saleem . Impact of cover crop monocultures and mixtures on organic carbon contents of soil aggregates. Soil Systems, 2021, 5(3): 43 https://doi.org/10.3390/soilsystems5030043
17
R T, Simpson S D, Frey J, Six R K Thiet . Preferential accumulation of microbial carbon in aggregate structures of no-tillage soils. Soil Science Society of America Journal, 2004, 68(4): 1249–1255 https://doi.org/10.2136/sssaj2004.1249
18
L D, Li C B, Wilson H B, He X D, Zhang F, Zhou S M Schaeffer . Physical, biochemical, and microbial controls on amino sugar accumulation in soils under long-term cover cropping and no-tillage farming. Soil Biology & Biochemistry, 2019, 135: 369–378 https://doi.org/10.1016/j.soilbio.2019.05.017
19
J, Tian N, Zong I P, Hartley N, He J, Zhang D, Powlson J, Zhou Y, Kuzyakov F, Zhang G, Yu J A J Dungait . Microbial metabolic response to winter warming stabilizes soil carbon. Global Change Biology, 2021, 27(10): 2011–2028 https://doi.org/10.1111/gcb.15538
pmid: 33528058
20
R G Joergensen . Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils, 2018, 54(5): 559–568 https://doi.org/10.1007/s00374-018-1288-3
21
X B, Chen Y H, Xia Y C, Rui Z, Ning Y J, Hu H M, Tang H B, He H X, Li Y, Kuzyakov T D, Ge J S, Wu Y R Su . Microbial carbon use efficiency, biomass turnover, and necromass accumulation in paddy soil depending on fertilization. Agriculture, Ecosystems & Environment, 2020, 292: 106816 https://doi.org/10.1016/j.agee.2020.106816
22
Y, Luo M L, Xiao H Z, Yuan C, Liang Z K, Zhu J M, Xu Y, Kuzyakov J S, Wu T D, Ge C X Tang . Rice rhizodeposition promotes the build-up of organic carbon in soil via fungal necromass. Soil Biology & Biochemistry, 2021, 160: 108345 https://doi.org/10.1016/j.soilbio.2021.108345
23
Y T, Hu Q, Zheng L, Noll S S, Zhang W Wanek . Direct measurement of the in situ decomposition of microbial-derived soil organic matter. Soil Biology & Biochemistry, 2020, 141: 107660 https://doi.org/10.1016/j.soilbio.2019.107660
24
Y D, Du B J, Cui Q, Zhang Z, Wang J, Sun W Q Niu . Effects of manure fertilizer on crop yield and soil properties in China: a meta-analysis. Catena, 2020, 193: 104617 https://doi.org/10.1016/j.catena.2020.104617
25
C, Liang W, Amelung J, Lehmann M Kästner . Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology, 2019, 25(11): 3578–3590 https://doi.org/10.1111/gcb.14781
pmid: 31365780
M, Egger Smith G, Davey M, Schneider C Minder . Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical Research Edition), 1997, 315(7109): 629–634 https://doi.org/10.1136/bmj.315.7109.629
pmid: 9310563
M H, Chantigny D A, Angers D, Prévost L P, Vézina F P Chalifour . Soil aggregation and fungal and bacterial biomass under annual and perennial cropping systems. Soil Science Society of America Journal, 1997, 61(1): 262–267 https://doi.org/10.2136/sssaj1997.03615995006100010037x
30
J, Six S D, Frey R K, Thiet K M Batten . Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal, 2006, 70(2): 555–569 https://doi.org/10.2136/sssaj2004.0347
31
H M, Throckmorton J A, Bird L, Dane M K, Firestone W R Horwath . The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems. Ecology Letters, 2012, 15(11): 1257–1265 https://doi.org/10.1111/j.1461-0248.2012.01848.x
pmid: 22897121
32
H, Wei B, Guenet S, Vicca N, Nunan H, Asard H, Abdelgawad W, Shen I A Janssens . High clay content accelerates the decomposition of fresh organic matter in artificial soils. Soil Biology & Biochemistry, 2014, 77: 100–108 https://doi.org/10.1016/j.soilbio.2014.06.006
33
K U, Totsche W, Amelung M H, Gerzabek G, Guggenberger E, Klumpp C, Knief E, Lehndorff R, Mikutta S, Peth A, Prechtel N, Ray I Kögel-Knabner . Microaggregates in soils. Journal of Plant Nutrition and Soil Science, 2018, 181(1): 104–136 https://doi.org/10.1002/jpln.201600451
34
J, Six E T, Elliott K Paustian . Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biology & Biochemistry, 2000, 32(14): 2099–2103 https://doi.org/10.1016/S0038-0717(00)00179-6
35
M E, Samson M H, Chantigny A, Vanasse S, Menasseri-Aubry I, Royer D A Angers . Management practices differently affect particulate and mineral-associated organic matter and their precursors in arable soils. Soil Biology & Biochemistry, 2020, 148: 107867 https://doi.org/10.1016/j.soilbio.2020.107867
36
G P, Ye Y X, Lin Y, Kuzyakov D Y, Liu J F, Luo S, Lindsey W J, Wang J B, Fan W X Ding . Manure over crop residues increases soil organic matter but decreases microbial necromass relative contribution in upland Ultisols: results of a 27-year field experiment. Soil Biology & Biochemistry, 2019, 134: 15–24 https://doi.org/10.1016/j.soilbio.2019.03.018
37
R, Zhou Y, Liu J A J, Dungait A, Kumar J, Wang L K, Tiemann F, Zhang Y, Kuzyakov J Tian . Microbial necromass in cropland soils: a global meta-analysis of management effects. Global Change Biology, 2023, 29(7): 1998–2014 https://doi.org/10.1111/gcb.16613
pmid: 36751727
38
M, Griepentrog S, Bodé P, Boeckx F, Hagedorn A, Heim M W I Schmidt . Nitrogen deposition promotes the production of new fungal residues but retards the decomposition of old residues in forest soil fractions. Global Change Biology, 2014, 20(1): 327–340 https://doi.org/10.1111/gcb.12374
pmid: 23996910
Y, Yang H, Xie Z, Mao X, Bao H, He X, Zhang C Liang . Fungi determine increased soil organic carbon more than bacteria through their necromass inputs in conservation tillage croplands. Soil Biology & Biochemistry, 2022, 167: 108587 https://doi.org/10.1016/j.soilbio.2022.108587
J, Clayton K, Lemanski M Bonkowski . Shifts in soil microbial stoichiometry and metabolic quotient provide evidence for a critical tipping point at 1% soil organic carbon in an agricultural post-mining chronosequence. Biology and Fertility of Soils, 2021, 57(3): 435–446 https://doi.org/10.1007/s00374-020-01532-2
43
X, Wan L, Xiao M A, Vadeboncoeur C E, Johnson Z Huang . Response of mineral soil carbon storage to harvest residue retention depends on soil texture: a meta-analysis. Forest Ecology and Management, 2018, 408: 9–15 https://doi.org/10.1016/j.foreco.2017.10.028
