Soil microbial carbon pump: Mechanism and appraisal

Abstract

The soil microbial carbon pump (MCP) conceptualizes a sequestration mechanism based on the process of microbial production of a set of new organic compounds, which carry the carbon from plant, through microbial anabolism, and enter into soil where it can be stabilized by the entombing effect. Understanding soil MCP and its related entombing effect is essential to the stewardship of ecosystem services, provided by microbial necromass in the formation and stabilization of soil organic matter as well as its resilience and vulnerability to global change. The mechanism and appraisal of soil MCP, however, remain to be elucidated. This lack of knowledge hampers the improvement of climate models and the development of land use policies. Here, I overview available knowledge to provide insights on the nature of the soil MCP in the context of two main aspects, i.e., internal features and external constraints that mechanistically influence the soil MCP operation and ultimately influence microbial necromass dynamics. The approach of biomarker amino sugars for investigation of microbial necromass and the methodological limitations are discussed. Finally, I am eager to call new investigations to obtain empirical data in soil microbial necromass research area, which urgently awaits synthesized quantitative and modeling studies to relate to soil carbon cycling and climate change.

Keywords

Microbial carbon pump / Microbial necromass / Biomarker / Soil carbon stabilization / Soil organic matter / Global change

References

[1] Amelung, W., 2001. Methods using amino sugars as markers for microbial residues in soil, In: Lal, R., Kimble, J.M., Follett, R.F., Stewart B.A., eds. Assessment Methods for Soil Carbon. CRC/Lewis Publishers, Boca Raton, FL, pp. 233–270.

[2] Amelung, W., Kimble, J.M., Samson-Liebig, S., Follett, R.F., 2001. Restoration of microbial residues in soils of the conservation reserve program. Soil Science Society of America Journal 65, 1704–1709

[3] Anderson, T.H., Joergensen, R.G., 1997. Relationship between SIR and FE estimates of microbial biomass C in deciduous forest soils at different pH. Soil Biology & Biochemistry 29, 1033–1042

[4] Anthony, M.A., Crowther, T.W., Maynard, D.S., van den Hoogen, J., Averill, C., 2020. Distinct assembly processes and microbial communities constrain soil organic carbon formation. One Earth 2, 349–360

[5] Appuhn, A., Joergensen, R., 2006. Microbial colonisation of roots as a function of plant species. Soil Biology & Biochemistry 38, 1040–1051

[6] Bai, Z., Bodé, S., Huygens, D., Zhang, X., Boeckx, P., 2013. Kinetics of amino sugar formation from organic residues of different quality. Soil Biology & Biochemistry 57, 814–821

[7] Baldock, J.A., Skjemstad, J.O., 2000. Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Organic Geochemistry 31, 697–710

[8] Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511

[9] Bodé, S., Denef, K., Boeckx, P., 2009. Development and evaluation of a high-performance liquid chromatography/isotope ratio mass spectrometry methodology for d¹³C analyses of amino sugars in soil. Rapid Communications in Mass Spectrometry 23, 2519–2526

[10] Böllmann, J., Elmer, M., Wöllecke, J., Raidl, S., Hüttl, R.F., 2010. Defensive strategies of soil fungi to prevent grazing by Folsomia candida (Collembola). Pedobiologia 53, 107–114

[11] Boschker, H.T.S., Middelburg, J.J., 2002. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiology Ecology 40, 85–95

[12] Bradford, M.A., Wieder, W.R., Bonan, G.B., Fierer, N., Raymond, P.A., Crowther, T.W., 2016. Managing uncertainty in soil carbon feedbacks to climate change. Nature Climate Change 6, 751–758

[13] Chantigny, M.H., Angers, D.A., Prevost, D., Vezina, L.P., Chalifour, F.P., 1997. Soil aggregation and fungal and cacterial biomass under annual and perennial cropping systems. Soil Science Society of America Journal 61, 262–267

[14] Cotrufo, M.F., Wallenstein, M.D., Boot, C.M., 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? Global Change Biology 19, 988–995

[15] Craig, M.E., Turner, B.L., Liang, C., Clay, K., Johnson, D.J., Phillips, R.P., 2018. Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Global Change Biology 24, 3317–3330

[16] Creamer, C.A., Foster, A.L., Lawrence, C., McFarland, J., Schulz, M., Waldrop, M.P., 2019. Mineralogy dictates the initial mechanism of microbial necromass association. Geochimica et Cosmochimica Acta 260, 161–176

[17] Crowther, T.W., Boddy, L., Hefin Jones, T., 2012. Functional and ecological consequences of saprotrophic fungus-grazer interactions. ISME Journal 6, 1992–2001

[18] Crowther, T.W., Thomas, S.M., Maynard, D.S., Baldrian, P., Covey, K., Frey, S.D., van Diepen, L.T., Bradford, M.A., 2015. Biotic interactions mediate soil microbial feedbacks to climate change. Proceedings of the National Academy of Sciences of the United States of America 112, 7033–7038

[19] Dalal, R.C., 1998. Soil microbial biomass: What do the numbers really mean? Australian Journal of Experimental Agriculture 38, 649–665

[20] Decock, C., Denef, K., Bod, S., Six, J., Boeckx, P., 2009. Critical assessment of the applicability of gas chromatography-combustion-isotope ratio mass spectrometry to determine amino sugar dynamics in soil. Rapid Communications in Mass Spectrometry 23, 1201–1211

[21] Ding, X., Chen, S., Zhang, B., Liang, C., He, H., Horwath, W.R., 2019. Warming increases microbial residue contribution to soil organic carbon in an alpine meadow. Soil Biology & Biochemistry 135, 13–19

[22] Ding, X., Han, X., Zhang, X., Qiao, Y., 2013. Effects of contrasting agricultural management on microbial residues in a Mollisol in China. Soil & Tillage Research 130, 13–17

[23] Ding, X., Liang, C., Zhang, B., Yuan, Y., Han, X., 2015. Higher rates of manure application lead to greater accumulation of both fungal and bacterial residues in macroaggregates of a clay soil. Soil Biology & Biochemistry 84, 137–146

[24] Ding, X., Zhang, B., Lü, X., Wang, J., Horwath, W.R., 2017. Parent material and conifer biome influence microbial residue accumulation in forest soils. Soil Biology & Biochemistry 107, 1–9

[25] Dippold, M.A., Boesel, S., Gunina, A., Kuzyakov, Y., Glaser, B., 2014. Improved d¹³C analysis of amino sugars in soil by ion chromatography-oxidation-isotope ratio mass spectrometry. Rapid Communications in Mass Spectrometry 28, 569–576

[26] Dungait, J.A.J., Hopkins, D.W., Gregory, A.S., Whitmore, A.P., 2012. Soil organic matter turnover is governed by accessibility not recalcitrance. Global Change Biology 18, 1781–1796

[27] Eisenhauer, N., Schlaghamerský, J., Reich, P.B., Frelich, L.E., 2011. The wave towards a new steady state: Effects of earthworm invasion on soil microbial functions. Biological Invasions 13, 2191–2196

[28] Eswaran, H., Van Den Berg, E., Reich, P., 1993. Organic carbon in soils of the world. Soil Science Society of America Journal 57, 192–194

[29] Fan, Z., Liang, C., 2015. Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs. Scientific Reports 5, 9575

[30] Fine, P.V.A., Miller, Z.J., Italo, M., Sebastian, I., Appel, H.M., Stevens, M.H.H., Ilari, S.K.R., Schultz, J.C., Coley, P.D., 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87, 150–162

[31] Foley, J.A., DeFries, R., Asner, G.P., Barford, C., Bonan, G., Carpenter, S.R., Chapin, F.S., Coe, M.T., Daily, G.C., Gibbs, H.K., Helkowski, J.H., Holloway, T., Howard, E.A., Kucharik, C.J., Monfreda, C., Patz, J.A., Prentice, I.C., Ramankutty, N., Snyder, P.K., 2005. Global consequences of land use. Science 309, 570–574

[32] Frey, S.D., Drijber, R., Smith, H., Melillo, J., 2008. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biology & Biochemistry 40, 2904–2907

[33] Fu, S., Ferris, H., Plant, R., Brown, D., 2005. Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biology & Biochemistry 37, 1979–1987

[34] Gan, H., Liang, C., Wickings, K., 2018. Root herbivores accelerate carbon inputs to soil and drive changes in biogeochemical processes. Rhizosphere 6, 112–115

[35] Geyer, K.M., Kyker-Snowman, E., Grandy, A.S., Frey, S.D., 2016. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127, 173–188

[36] Glaser, B., 2005. Compound-specific stable-isotope (d¹³C) analysis in soil science. Journal of Plant Nutrition and Soil Science 168, 633–648

[37] Glaser, B., Gross, S., 2005. Compound-specific δ¹³C analysis of individual amino sugars– a tool to quantify timing and amount of soil microbial residue stabilization. Rapid Communications in Mass Spectrometry 19, 1409–1416.

[38] Glaser, B., Millar, N., Blum, H., 2006. Sequestration and turnover of bacterial- and fungal-derived carbon in a temperate grassland soil under long-term elevated atmospheric p CO₂. Global Change Biology 12, 1521–1531

[39] Glaser, B., Turrion, M.B., Alef, K., 2004. Amino sugars and muramic acid - biomarkers for soil microbial community structure analysis. Soil Biology & Biochemistry 36, 399–407

[40] Grandy, A.S., Wieder, W.R., Wickings, K., Kyker-Snowman, E., 2016. Beyond microbes: Are fauna the next frontier in soil biogeochemical models? Soil Biology & Biochemistry 102, 40–44

[41] Guerrant, G.O., Moss, C.W., 1984. Determination of monosaccharides as aldononitrile, O-methyloxime, alditol, and cyclitol acetate derivatives by gas chromatography. Analytical Chemistry 56, 633–638

[42] Guggenberger, G., Christensen, B.T., Zech, W., 1994. Land-use effects on the composition of organic matter in particle-size separates of soil: I. Lignin and carbohydrate signature. European Journal of Soil Science 45, 449–458

[43] Guggenberger, G., Frey, S.D., Six, J., Paustian, K., Elliott, E.T., 1999. Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Science Society of America Journal 63, 1188–1198

[44] Hanlon, R.D.G., 1981. Influence of grazing by collembola on the activity of senescent fungal colonies grown on media of different nutrient concentration. Oikos 36, 362–367

[45] He, H., Xie, H., Zhang, X., 2006. A novel GC/MS technique to assess ¹⁵N and ¹³C incorporation into soil amino sugars. Soil Biology & Biochemistry 38, 1083–1091

[46] He, H., Xie, H., Zhang, X., Wang, Y., Wu, Y., 2005. A gas chromatographic/mass spectrometric method for tracing the microbial conversion of glucose into amino sugars in soil. Rapid Communications in Mass Spectrometry 19, 1993–1998

[47] Hunter, M.D., 2001. Insect population dynamics meets ecosystem ecology: Effects of herbivory on soil nutrient dynamics. Agricultural & Forest Entomology 3, 77–84.

[48] Jastrow, J.D., Amonette, J.E., Bailey, V.L., 2007. Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Climatic Change 80, 5–23

[49] Jastrow, J.D., Miller, R.M., Matamala, R., Norby, R.J., Boutton, T.W., Rice, C.W., Owensby, C.E., 2005. Elevated atmospheric carbon dioxide increases soil carbon. Global Change Biology 11, 2057–2064

[50] Jia, J., Feng, X., He, J.S., He, H., Lin, L., Liu, Z., 2017. Comparing microbial carbon sequestration and priming in the subsoil versus topsoil of a Qinghai-Tibetan alpine grassland. Soil Biology & Biochemistry 104, 141–151

[51] Jiao, N., Herndl, G.J., Hansell, D.A., Benner, R., Kattner, G., Wilhelm, S.W., Kirchman, D.L., Weinbauer, M.G., Luo, T., Chen, F., Azam, F., 2010. Microbial production of recalcitrant dissolved organic matter: Long-term carbon storage in the global ocean. Nature Reviews. Microbiology 8, 593–599

[52] Jiao, N., Wang, H., Xu, G., Aricò, S., 2018. Blue carbon on the rise: Challenges and opportunities. National Science Review 5, 464–468.

[53] Joergensen, R.G., 2018. Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils 54, 559–568

[54] Joergensen, R.G., Emmerling, C., 2006. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. Journal of Plant Nutrition and Soil Science 169, 295–309

[55] Joergensen, R.G., Mäder, P., Fließbach, A., 2010. Long-term effects of organic farming on fungal and bacterial residues in relation to microbial energy metabolism. Biology and Fertility of Soils 46, 303–307

[56] Jouquet, P., Dauber, J., Lagerlöf, J., Lavelle, P., Lepage, M., 2006. Soil invertebrates as ecosystem engineers: Intended and accidental effects on soil and feedback loops. Applied Soil Ecology 32, 153–164

[57] Kallenbach, C.M., Frey, S.D., Grandy, A.S., 2016. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nature Communications 7, 13630

[58] Kallenbach, C.M., Grandy, A.S., Frey, S.D., Diefendorf, A.F., 2015. Microbial physiology and necromass regulate agricultural soil carbon accumulation. Soil Biology & Biochemistry 91, 279–290

[59] Khan, K.S., Mack, R., Castillo, X., Kaiser, M., Joergensen, R.G., 2016. Microbial biomass, fungal and bacterial residues, and their relationships to the soil organic matter C/N/P/S ratios. Geoderma 271, 115–123

[60] Kiem, R., Kogel-Knabner, I., 2003. Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biology & Biochemistry 35, 101–118

[61] Kivlin, S.N., Waring, B.G., Averill, C., Hawkes, C.V., 2013. Tradeoffs in microbial carbon allocation may mediate soil carbon storage in future climates. Frontiers in Microbiology 4, 4

[62] Knicker, H., 2000. Nature of organic nitrogen in fine particle size separates of sandy soils of highly industrialized areas as revealed by NMR spectroscopy. Soil Biology & Biochemistry 32, 241–252

[63] Knicker, H., 2004. Stabilization of N-compounds in soil and organic-matter-rich sediments– what is the difference? Marine Chemistry 92, 167–195

[64] Kögel-Knabner, I., 2002. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biology & Biochemistry 34, 139–162

[65] Kögel-Knabner, I., Guggenberger, G., Kleber, M., Kandeler, E., Kalbitz, K., Scheu, S., Eusterhues, K., Leinweber, P., 2008. Organo-mineral associations in temperate soils: Integrating biology, mineralogy, and organic matter chemistry. Journal of Plant Nutrition and Soil Science 171, 61–82

[66] Kubicki, J.D., Schroeter, L.M., Itoh, M.J., Nguyen, B.N., Apitz, S.E., 1999. Attenuated total reflectance Fourier-transform infrared spectroscopy of carboxylic acids adsorbed onto mineral surfaces. Geochimica et Cosmochimica Acta 63, 2709–2725

[67] Lauer, F., Kösters, R., Preez, C.C.D., Amelung, W., 2011. Microbial residues as indicators of soil restoration in South African secondary pastures. Soil Biology & Biochemistry 43, 787–794

[68] Lavelle, P., 1997. Faunal Activities and Soil Processes: Adaptive Strategies That Determine Ecosystem Function, In: Fitter, M.B.a.A.H., ed. Advances in Ecological Research. Academic Press, pp. 93–132.

[69] Lechtenfeld, O.J., Hertkorn, N., Shen, Y., Witt, M., Benner, R., 2015. Marine sequestration of carbon in bacterial metabolites. Nature Communications 6, 6711

[70] Lee, Z.M., Schmidt, T.M., 2014. Bacterial growth efficiency varies in soils under different land management practices. Soil Biology & Biochemistry 69, 282–290

[71] Lehmann, J., Kinyangi, J., Solomon, D., 2007. Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms. Biogeochemistry 85, 45–57

[72] Lehmann, J., Kleber, M., 2015. The contentious nature of soil organic matter. Nature 528, 60–68

[73] Li, X., Fisk, M.C., Fahey, T.J., Bohlen, P.J., 2002. Influence of earthworm invasion on soil microbial biomass and activity in a northern hardwood forest. Soil Biology & Biochemistry 34, 1929–1937

[74] Liang, C., Amelung, W., Lehmann, J., Kästner, M., 2019. Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology 25, 3578–3590

[75] Liang, C., Balser, T.C., 2008. Preferential sequestration of microbial carbon in subsoils of a glacial-landscape toposequence, Dane County, WI, USA. Geoderma 148, 113–119

[76] Liang, C., Balser, T.C., 2010. Mass spectrometric characterization of amino sugar aldononitrile acetate derivatives used for isotope enrichment assessment of microbial residues. Soil Biology & Biochemistry 42, 904–909

[77] Liang, C., Balser, T.C., 2011. Microbial production of recalcitrant organic matter in global soils: Implications for productivity and climate policy. Nature Reviews. Microbiology 9, 75

[78] Liang, C., Balser, T.C., 2012. Warming and nitrogen deposition lessen microbial residue contribution to soil carbon pool. Nature Communications 3, 1222

[79] Liang, C., Cheng, G., Wixon, D., Balser, T., 2011. An Absorbing Markov Chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106, 303–309

[80] Liang, C., Duncan, D.S., Balser, T.C., Tiedje, J.M., Jackson, R.D., 2013. Soil microbial residue storage linked to soil legacy under biofuel cropping systems in southern Wisconsin, USA. Soil Biology & Biochemistry 57, 939–942

[81] Liang, C., Gutknecht, J.L.M., Balser, T.C., 2015. Microbial lipid and amino sugar responses to long-term simulated global environmental changes in a California annual grassland. Frontiers in Microbiology 6, 385

[82] Liang, C., Pedersen, J.A., Balser, T.C., 2009a. Aminoglycoside antibiotics may interfere with microbial amino sugar analysis. Journal of Chromatography. A 1216, 5296–5301

[83] Liang, C., Read, H., Balser, T., 2009b. Reliability of muramic acid as a bacterial biomarker is influenced by methodological artifacts from streptomycin. Microbial Ecology 57, 494–500

[84] Liang, C., Read, H.W., Balser, T.C., 2012. GC-based detection of aldonitrile acetate derivatized glucosamine and muramic acid for microbial residue determination in soil samples: analytical protocol and derivative validation. Journal of Visualization Experiment 63, 3767.

[85] Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology 2, 17105

[86] Liang, C., Zhang, X., Balser, T.C., 2007. Net microbial amino sugar accumulation process in soil as influenced by different plant material inputs. Biology and Fertility of Soils 44, 1–7

[87] Ludwig, M., Achtenhagen, J., Miltner, A., Eckhardt, K.U., Leinweber, P., Emmerling, C., Thiele-Bruhn, S., 2015. Microbial contribution to SOM quantity and quality in density fractions of temperate arable soils. Soil Biology & Biochemistry 81, 311–322

[88] Ma, T., Zhu, S., Wang, Z., Chen, D., Dai, G., Feng, B., Su, X., Hu, H., Li, K., Han, W., Liang, C., Bai, Y., Feng, X., 2018. Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nature Communications 9, 3480

[89] Malik, A.A., Martiny, J.B.H., Brodie, E.L., Martiny, A.C., Treseder, K.K., Allison, S.D., 2020. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME Journal 14, 1–9

[90] Malik, A.A., Roth, V.N., Hébert, M., Tremblay, L., Dittmar, T., Gleixner, G., 2016. Linking molecular size, composition and carbon turnover of extractable soil microbial compounds. Soil Biology & Biochemistry 100, 66–73

[91] Martins, M.R., Angers, D.A., Corá, J.E., 2012. Co-accumulation of microbial residues and particulate organic matter in the surface layer of a no-till Oxisol under different crops. Soil Biology & Biochemistry 50, 208–213

[92] McCarthy, J.F., Ilavsky, J., Jastrow, J.D., Mayer, L.M., Perfect, E., Zhuang, J., 2008. Protection of organic carbon in soil microaggregates via restructuring of aggregate porosity and filling of pores with accumulating organic matter. Geochimica et Cosmochimica Acta 72, 4725–4744

[93] Mikutta, R., Kleber, M., Torn, M., Jahn, R., 2006. Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77, 25–56

[94] Miltner, A., Bombach, P., Schmidt-Brücken, B., Kästner, M., 2012. SOM genesis: Microbial biomass as a significant source. Biogeochemistry 111, 41–55

[95] Monreal, C.M., Sultan, Y., Schnitzer, M., 2010. Soil organic matter in nano-scale structures of a cultivated Black Chernozem. Geoderma 159, 237–242

[96] Mooney, H.A., Canadell, J., Chapin, F.S. III, Ehleringer, J.H., Korner, C., McMurtrie, R.E., Parton, W.J., Pitelka, L.F., Schulze, E.D., 1999. Ecosystem physiology responses to global change, In: Walker, B., ed. The Terrestrial Biosphere and Global Change. Cambridge University Press, pp. 141–189.

[97] Moritz, L.K., Liang, C., Wagai, R., Kitayama, K., Balser, T.C., 2009. Vertical distribution and pools of microbial residues in tropical forest soils formed from distinct parent materials. Biogeochemistry 92, 83–94

[98] Morrissey, E.M., Mchugh, T.A., Preteska, L., Hayer, M., Dijkstra, P., Hungate, B.A., Schwartz, E., 2015. Dynamics of extracellular DNA decomposition and bacterial community composition in soil. Soil Biology & Biochemistry 86, 42–49

[99] Nannipieri, P., Pedrazzini, F., Arcara, P.G., Piovanelli, C., 1979. Changes in amino-acids, enzyme-activities, and biomasses during soil microbial-growth. Soil Science 127, 26–34

[100] Niggemann, J., Schubert, C.J., 2006. Sources and fate of amino sugars in coastal Peruvian sediments. Geochimica et Cosmochimica Acta 70, 2229–2237

[101] Poeplau, C., Helfrich, M., Dechow, R., Szoboszlay, M., Tebbe, C.C., Don, A., Greiner, B., Zopf, D., Thumm, U., Korevaar, H., Geerts, R., 2019. Increased microbial anabolism contributes to soil carbon sequestration by mineral fertilization in temperate grasslands. Soil Biology & Biochemistry 130, 167–176

[102] Potthoff, M., Dyckmans, J., Flessa, H., Beese, F., Joergensen, R., 2008. Decomposition of maize residues after manipulation of colonization and its contribution to the soil microbial biomass. Biology and Fertility of Soils 44, 891–895

[103] Pronk, G.J., Heister, K., Kögel-Knabner, I., 2015. Amino sugars reflect microbial residues as affected by clay mineral composition of artificial soils. Organic Geochemistry 83–84, 109–113

[104] Rillig, M.C., Wright, S.F., Nichols, K.A., Schmidt, W.F., Torn, M.S., 2001. Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant & Soil 233, 167–177.

[105] Roller, B.R.K., Stoddard, S.F., Schmidt, T.M., 2016. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nature Microbiology 1, 16160

[106] Rumpel, C., Eusterhues, K., Kögel-Knabner, I., 2010. Non-cellulosic neutral sugar contribution to mineral associated organic matter in top- and subsoil horizons of two acid forest soils. Soil Biology & Biochemistry 42, 379–382

[107] Schimel, J., Schaeffer, S.M., 2012. Microbial control over carbon cycling in soil. Frontiers in Microbiology 3, 1–11

[108] Schlautman, M.A., Morgan, J.J., 1994. Adsorption of aquatic humic substances on colloidal-size aluminum oxide particles: Influence of solution chemistry. Geochimica et Cosmochimica Acta 58, 4293–4303

[109] Schmidt, M.W.I., Torn, M.S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I.A., Kleber, M., Kogel-Knabner, I., Lehmann, J., Manning, D.A.C., Nannipieri, P., Rasse, D.P., Weiner, S., Trumbore, S.E., 2011. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56

[110] Shao, P., Liang, C., Lynch, L., Xie, H., Bao, X., 2019. Reforestation accelerates soil organic carbon accumulation: Evidence from microbial biomarkers. Soil Biology & Biochemistry 131, 182–190

[111] Simpson, A.J., Simpson, M.J., Smith, E., Kelleher, B.P., 2007. Microbially derived inputs to soil organic matter: Are current estimates too low? Environmental Science & Technology 41, 8070–8076

[112] Sokol, N.W., Bradford, M.A., 2019. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nature Geoscience 12, 46–53

[113] Sokol, N.W., Sanderman, J., Bradford, M.A., 2019. Pathways of mineral-associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry. Global Change Biology 25, 12–24

[114] Sollins, P., Homann, P., Caldwell, B.A., 1996. Stabilization and destabilization of soil organic matter: Mechanisms and controls. Geoderma 74, 65–105

[115] Solomon, D., Lehmann, J., Zech, W., 2001. Land use effects on amino sugar signature of chromic Luvisol in the semi-arid part of northern Tanzania. Biology and Fertility of Soils 33, 33–40

[116] Soong, J.L., Vandegehuchte, M.L., Horton, A.J., Nielsen, U.N., Denef, K., Shaw, E.A., Tomasel, C.M.D., Parton, W., Wall, D.H., Cotrufo, M.F., 2016. Soil microarthropods support ecosystem productivity and soil C accrual: Evidence from a litter decomposition study in the tallgrass prairie. Soil Biology & Biochemistry 92, 230–238

[117] Stevenson, F., 1994. Humus Chemistry: Genesis, Composition, Reactions. 2nd ed. John Wiley & Sons, New York.

[118] Stockmann, U., Adams, M.A., Crawford, J.W., Field, D.J., Henakaarchchi, N., Jenkins, M., Minasny, B., McBratney, A.B., Courcelles, V.R., Singh, K., Wheeler, I., Abbott, L., Angers, D.A., Baldock, J., Bird, M., Brookes, P.C., Chenu, C., Jastrow, J.D., Lal, R., Lehmann, J., O’Donnell, A.G., Parton, W.J., Whitehead, D., Zimmermann, M., 2013. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agriculture, Ecosystems & Environment 164, 80–99

[119] Swift, R.G., 2001. Sequestration of carbon by soil. Soil Science 166, 858–871

[120] Tao, W., Zhaomo, T., Per, B., Anders, T., Per, P., 2017. Mineral surface-reactive metabolites secreted during fungal decomposition contribute to the formation of soil organic matter. Environmental Microbiology 19, 5117–5129

[121] van Groenigen, K.J., Six, J., Harris, D., Van Kessel, C., 2007. Elevated CO₂ does not favor a fungal decomposition pathway. Soil Biology & Biochemistry 39, 2168–2172

[122] van Groenigen, K.J., Six, J., Hungate, B.A., de Graaff, M.A., van Breemen, N., van Kessel, C., 2006. Element interactions limit soil carbon storage. Proceedings of the National Academy of Sciences of the United States of America 103, 6571–6574

[123] von Lützow, M., Kögel-Knabner, I., Ekschmitt, K., Matzner, E., Guggenberger, G., Marschner, B., Flessa, H., 2006. Stabilization of organic matter in temperate soils: Mechanisms and their relevance under different soil conditions-a review. European Journal of Soil Science 57, 426–445

[124] Wardle, D.A., 1992. A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biological Reviews of the Cambridge Philosophical Society 67, 321–358

[125] Whitman, W.B., Coleman, D.C., Wiebe, W.J., 1998. Prokaryotes: The unseen majority. Proceedings of the National Academy of Sciences of the United States of America 95, 6578–6583

[126] Wilkinson, M.T., Richards, P.J., Humphreys, G.S., 2009. Breaking ground: Pedological, geological, and ecological implications of soil bioturbation. Earth-Science Reviews 97, 257–272

[127] Wolters, V., 2000. Invertebrate control of soil organic matter stability. Biology and Fertility of Soils 31, 1–19

[128] Xu, X., Thornton, P.E., Post, W.M., 2013. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecology and Biogeography 22, 737–749

[129] Zhang, B., Drury, C.F., Yang, X., Reynolds, W.D., Zhang, X., 2014. Effects of long-term and recently imposed tillage on the concentration and composition of amino sugars in a clay loam soil in Ontario, Canada. Soil & Tillage Research 135, 9–17

[130] 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

[131] Zhang, W., Liang, C., Kao-Kniffin, J., He, H., Xie, H., Zhang, H., Zhang, X., 2015. Differentiating the mineralization dynamics of the originally present and newly synthesized amino acids in soil amended with available carbon and nitrogen substrates. Soil Biology & Biochemistry 85, 162–169

[132] Zhang, X., Amelung, W., 1996. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology & Biochemistry 28, 1201–1206

[133] Zhang, X., Amelung, W., Yuan, Y., Samson-Liebig, S., Brown, L., Zech, W., 1999. Land-use effects on amino sugars in particle size fractions of an Argiudoll. Applied Soil Ecology 11, 271–275

[134] Zhu, X., Liang, C., Masters, M.D., Kantola, I.B., DeLucia, E.H., 2018. The impacts of four potential bioenergy crops on soil carbon dynamics as shown by biomarker analyses and DRIFT spectroscopy. Global Change Biology. Bioenergy 10, 489–500

[135] Zhu, X., Xie, H., Masters, M.D., Luo, Y., Zhang, X., Liang, C., 2020. Microbial trade-off in soil organic carbon storage in a no-till continuous corn agroecosystem. European Journal of Soil Biology 96, 103146

Acknowledgments

I would like to thank Drs. X. Zhang, T. Balser, J. Tiedje, J. Jastrow, E. DeLucia and M. Kästner for their supports along with the idea evolution and career development of C. Liang. I would like to thank Drs. H. Gan and K. Wickings for discussions on soil fauna, Dr. M. Zhu for discussions biomarker chemistry, Drs. J. Schimel and J. Lehmann for offering general insightful comments, and Dr. X. Zhu for improving visual quality of the figures. This work was supported by the National Natural Science Foundation of China (No. 31930070, 41977051). The grants or other support to C. Liang from the K. C. Wong Education Foundation of China (No. GJTD-2019-10) and the Alexander von Humboldt Foundation of Germany are also acknowledged with gratitude.

Competing financial interests

The author declares no competing financial interests.

RIGHTS & PERMISSIONS

2020 Higher Education Press