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Fate of rice shoot and root residues, rhizodeposits, and microbial assimilated carbon in paddy soil - part 2: turnover and microbial utilization

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Abstract

Background and aims

The turnover of plant- and microbial- derived carbon (C) plays a significant role in the soil organic C (SOC) cycle. However, there is limited information about the turnover of the recently photosynthesized plant- and soil microbe-derived C in paddy soil.

Methods

We conducted an incubation study with four different 13C–labeled substrates: rice shoots (Shoot-C), rice roots (Root-C), rice rhizodeposits (Rhizo-C), and microbe-assimilated C (Micro-C).

Results

Shoot- and Root-C were initially rapidly transformed into the dissolved organic C (DOC) pool, while their recovery in microbial biomass C (MBC) and SOC increased with incubation time. There were 0.05%, 9.8% and 10.0% of shoot-C, and 0.06%, 15.9% and 16.5% of root-C recovered in DOC, MBC and SOC pools, respectively at the end of incubation. The percentages of Rhizo- and Micro-C recovered in DOC, MBC, and SOC pools slowly decreased over time. Less than 0.1% of the Rhizo- and Micro-C recovered in DOC pools at the end of experiment; while 45.2% and 33.8% of Rhizo- and Micro-C recovered in SOC pools. Shoot- and Root-C greatly increased the amount of 13C–PLFA in the initial 50 d incubation, which concerned PLFA being indicative for fungi and actinomycetes while those assigning gram-positive bacteria decreased. The dynamic of soil microbes utilizing Rhizo- and Micro-C showed an inverse pattern than those using Shoot- and Root-C. Principal component analysis of 13C–PLFA showed that microbial community composition shifted obviously in the Shoot-C and Root-C treatments over time, but that composition changed little in the Rhizo-C and Micro-C treatments.

Conclusions

The input C substrates drive soil microbial community structure and function with respect to carbon stabilization. Rhizodeposited and microbial assimilated C have lower input rates, however, they are better stabilized than shoot- and root-derived C, and thus are preferentially involved in the formation of stable SOC in paddy soils.

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References

  • Alberti G, Vicca S, Inglima I, Belelli-Marchesini L, Genesio L, Miglietta F, Marjanovic H, Martinez C, Matteucci G, Andrea E, Peressotti A, Petrella F, Rodeghiero M, and Cotrufo M (2015) Soil C:N stoichiometry controls carbon sink partitioning between above-ground tree biomass and soil organic matter in high fertility forests. iForest 8:195–206

  • Bastida F, Torres IF, Hernández T, Bombach P, Richnow HH, García C (2013) Can the labile carbon contribute to carbon immobilization in semiarid soils? Priming effects and microbial community dynamics. Soil Biol Biochem 57:892–902

    Article  CAS  Google Scholar 

  • Baumann K, Marschner P, Smernik RJ, Baldock JA (2009) Residue chemistry and microbial community structure during decomposition of eucalypt, wheat and vetch residues. Soil Biol Biochem 41:1966–1975

    Article  CAS  Google Scholar 

  • Berg B (1986) Nutrient release from litter and humus in coniferous forest soils—a mini review. Scand J Forest Res 1:359–369

    Article  Google Scholar 

  • Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835

    Article  CAS  Google Scholar 

  • Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  Google Scholar 

  • Bol R, Poirier N, Balesdent J, Gleixner G (2009) Molecular turnover time of soil organic matter in particle-size fractions of an arable soil. Rapid Commun Mass Sp 23:2551–2558

    Article  CAS  Google Scholar 

  • Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232

    Article  CAS  Google Scholar 

  • Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841

    Article  CAS  Google Scholar 

  • Chen R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Lin X, Blagodatskaya E, Kuzyakov Y (2014) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Chang Biol 20:2356–2367

    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  PubMed  Google Scholar 

  • Derrien D, Plain C, Courty PE et al (2014) Does the addition of labile substrate destabilise old soil organic matter. Soil Biol Biochem 76:149–160

    Article  CAS  Google Scholar 

  • Devêvre OC, Horwáth WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol Biochem 32:1773–1785

    Article  Google Scholar 

  • Dilly O, Bloem J, Vos A, Munch JC (2004) Bacterial diversity in agricultural soils during litter decomposition. Appl Environ Microb 70:468–474

    Article  CAS  Google Scholar 

  • Dungait JAJ, Kemmitt SJ, Michallon L, Guo S, Wen Q, Brookes PC, Evershed RP (2011) Variable responses of the soil microbial biomass to trace concentrations of 13C-labelled glucose, using 13C-PLFA analysis. Eur J Soil Sci 62:117–126

    Article  CAS  Google Scholar 

  • Falkowski PG, Godfrey LV (2008) Electrons, life and the evolution of Earth's oxygen cycle. Philos T R Soc B Biol Sci 363:2705–2716

    Article  CAS  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Gale WJ, Cambardella CA, Bailey TB (2000) Root-derived carbon and the formation and stabilization of aggregates. Soil Sci Soc Am J 64:201–207

    Article  CAS  Google Scholar 

  • Ge T, Yuan H, Zhu H, Wu X, Nie S, Liu C, Tong C, Wu J, Brookes P (2012) Biological carbon assimilation and dynamics in a flooded rice – soil system. Soil Biol Biochem 48:39–46

    Article  CAS  Google Scholar 

  • Ge T, Wu X, Chen H, Yuan HZ, Li B, Zhou P, Liu C, Tong C, Brookes P, Wu J (2013) Microbial phototrophic fixation of atmospheric CO2 in China subtropical upland and paddy soils. Geochim Cosmochim Ac 113:70–78

    Article  CAS  Google Scholar 

  • Glanville H, Rousk J, Golyshin P, Jones DL (2012) Mineralization of low molecular weight carbon substrates in soil solution under laboratory and field conditions. Soil Biol Biochem 48:88–95

    Article  CAS  Google Scholar 

  • Gunina A, Dippold MA, Glaser B, Kuzyakov Y (2014) Fate of low molecular weight organic substances in an arable soil: from microbial uptake to utilisation and stabilisation. Soil Biol Biochem 77:304–313

    Article  CAS  Google Scholar 

  • Jingguo W, Bakken LR (1997) Competition for nitrogen during mineralization of plant residues in soil: microbial response to C and N availability. Soil Biol Biochem 29:163–170

    Article  CAS  Google Scholar 

  • Johnson JMF, Allmaras RR, Reicosky DC (2006) Estimating source carbon from crop residues, roots and rhizodeposits using the National Grain-Yield Database. Agron J 98:622–636

    Article  CAS  Google Scholar 

  • Jones DL, Kemmitt SJ, Wright D, Cuttle SP, Bol R, Edwards AC (2005) Rapid intrinsic rates of amino acid biodegradation in soils are unaffected by agricultural management strategy. Soil Biol Biochem 37:1267–1275

    Article  CAS  Google Scholar 

  • Kirkby CA, Richardson AE, Wade LJ, Batten GD, Blanchard C, Kirkegaard JA (2013) Carbon-nutrient stoichiometry to increase soil carbon sequestration. Soil Biol Biochem 60:77–86

    Article  CAS  Google Scholar 

  • Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14

    Article  Google Scholar 

  • Kramer S, Marhan S, Ruess L, Armbruster W, Butenschoen O, Haslwimmer H, Kuzyakov Y, Pausch J, Scheunemann N, Schoene J, Schmalwasser A, Totsche KU, Walker F, Scheu S, Kandeler E (2012) Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 55:111–119

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Larionova AA (2005) Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. J Plant Nut Soil Sci 168:503–520

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li J, Li Y, Yang X, Zhang J, Lin Z, Zhao B (2015) Microbial community structure and functional metabolic diversity are associated with organic carbon availability in an agricultural soil. J Integr Agr 14:2500–2511

    Article  CAS  Google Scholar 

  • Liang C, Balser TC (2008) Preferential sequestration of microbial carbon in subsoils of a glacial-landscape toposequence, Dane County, WI, USA. Geoderma 148:113–119

    Article  CAS  Google Scholar 

  • Loeppmann S, Blagodatskaya E, Pausch J, Kuzyakov Y (2016) Substrate quality affects kinetics and catalytic efficiency of exo-enzymes in rhizosphere and detritusphere. Soil Biol Biochem 92:111–118

    Article  CAS  Google Scholar 

  • Lu Y, Watanabe A, Kimura M (2002) Contribution of plant-derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biol Fert Soil 36:136–142

    Article  CAS  Google Scholar 

  • Lu Y, Watanabe A, Kimura M (2003) Carbon dynamics of rhizodeposits, root- and shoot-residues in a rice soil. Soil Biol Biochem 35:1223–1230

    Article  CAS  Google Scholar 

  • Marschner P, Umar S, Baumann K (2011) The microbial community composition changes rapidly in the early stages of decomposition of wheat residue. Soil Biol Biochem 43:445–451

    Article  CAS  Google Scholar 

  • Mikutta R, Kaiser K (2011) Organic matter bound to mineral surfaces: resistance to chemical and biological oxidation. Soil Biol Biochem 43:1738–1741

    Article  CAS  Google Scholar 

  • Müller K, Kramer S, Haslwimmer H, Marhan S, Scheunemann N, Butenschön O, Scheu S, Kandeler E (2016) Carbon transfer from maize roots and litter into bacteria and fungi depends on soil depth and time. Soil Biol Biochem 93:79–89

    Article  Google Scholar 

  • Nikolausz M, Kappelmeyer U, Székely A, Rusznyák A, Márialigeti K (2008) Diurnal redox fluctuation and microbial activity in the rhizosphere of wetland plants. Eur J Soil Biol 44:324–333

    Article  CAS  Google Scholar 

  • Pan G, Li L, Wu L, Zhang X (2004) Storage and sequestration potential of topsoil organic carbon in China's paddy soils. Glob Chang Biol 10:79–92

    Article  Google Scholar 

  • Paterson E, Sim A, Osborne SM, Murray PJ (2011) Long-term exclusion of plant-inputs to soil reduces the functional capacity of microbial communities to mineralise recalcitrant root-derived carbon sources. Soil Biol Biochem 43:1873–1880

    Article  CAS  Google Scholar 

  • Rubino M, Dungait JAJ, Evershed RP, Bertolini T, Angelis PD, D’Onofrio A, Lagomarsino A, Lubritto C, Merola A, Terrasi F, Cotrufo MF (2010) Carbon input belowground is the major C flux contributing to leaf litter mass loss: evidences from a 13C labelled-leaf litter experiment. Soil Biol Biochem 42:1009–1016

    Article  CAS  Google Scholar 

  • Ruf A, Kuzyakov Y, Lopatovskaya O (2006) Carbon fluxes in soil food webs of increasing complexity revealed by 14C labelling and 13C natural abundance. Soil Biol Biochem 38:2390–2400

    Article  CAS  Google Scholar 

  • Schurig C, Smittenberg RH, Berger J, Kraft F, Woche SK, Goebel MO, Heipieper HJ, Miltner A, Kaestner M (2013) Microbial cell-envelope fragments and the formation of soil organic matter: a case study from a glacier forefield. Biogeochemistry 113:595–612

    Article  CAS  Google Scholar 

  • Seth EC, Taga ME (2014) Nutrient cross-feeding in the microbial world. Front Microbiol 5:1–6

    Article  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 

  • Singh S, Ghoshal N, Singh KP (2007) Variations in soil microbial biomass and crop roots due to differing resource quality inputs in a tropical dryland agroecosystem. Soil Biol Biochem 39:76–86

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939

    Article  PubMed  Google Scholar 

  • Spohn M, Pötsch EM, Eichorst SA, Woebken D, Wanek W, Richter A (2016) Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem 97:168–175

    Article  CAS  Google Scholar 

  • Tian J, Dippold M, Pausch J, Blagodatskaya E, Fan M, Li X, Kuzyakov Y (2013) Microbial response to rhizodeposition depending on water regimes in paddy soils. Soil Biol Biochem 65:195–203

    Article  CAS  Google Scholar 

  • Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284

    Article  PubMed  Google Scholar 

  • Waldrop MP, Harden JW, Turetsky MR, Petersen DG, McGuire AD, Briones MJI, Churchill AC, Doctor DH, Pruett LE (2012) Bacterial and enchytraeid abundance accelerate soil carbon turnover along a lowland vegetation gradient in interior Alaska. Soil Biol Biochem 50:188–198

    Article  CAS  Google Scholar 

  • Wang Q, Wang S, He T, Liu L, Wu J (2014a) Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol Biochem 71:13–20

    Article  CAS  Google Scholar 

  • Wang Q, Wang Y, Wang S, He T, Liu L (2014b) Fresh carbon and nitrogen inputs alter organic carbon mineralization and microbial community in forest deep soil layers. Soil Biol Biochem 72:145–151

    Article  CAS  Google Scholar 

  • Weintraub M, Scott-Denton L, Schmidt S, Monson R (2007) The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia 154:327–338

    Article  PubMed  Google Scholar 

  • Williams MA, Myrold DD, Bottomley PJ (2006) Carbon flow from 13C-labeled straw and root residues into the phospholipid fatty acids of a soil microbial community under field conditions. Soil Biol Biochem 38:759–768

    Article  CAS  Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

  • Wu J, Zhou P, Li L, Su Y, Yuan H, Syers JK (2012) Restricted mineralization of fresh organic materials incorporated into a subtropical paddy soil. J Sci Food Agr 92:1031–1037

    Article  CAS  Google Scholar 

  • Xiao J, Wen Y, Li H, Hao J, Shen Q, Ran W, Mei X, He X, Yu G (2015) In situ visualisation and characterisation of the capacity of highly reactive minerals to preserve soil organic matter (SOM) in colloids at submicron scale. Chemosphere 138:225–232

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Ge T, Wu X, Liu S, Tong C, Qin H, Wu M, Wei W, Wu J (2012) Long-term field fertilization alters the diversity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl Microbiol Biot 95:1061–1071

    Article  CAS  Google Scholar 

  • Yuan H, Zhu Z, Liu S, Ge T, Jing H, Li B, Liu Q, Lynn TM, Wu J, Kuzyakov Y (2016) Microbial utilization of rice root exudates: 13C labeling and PLFA composition. Biol Fert Soil 52:615–627

    Article  CAS  Google Scholar 

  • Zelles L (1997) Experimental and theoretical approaches in environmental chemistry phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294

    Article  CAS  PubMed  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fert Soil 29:111–129

    Article  CAS  Google Scholar 

  • Zhu Z, Zeng G, Ge T, Hu Y, Tong C, Shibistova O, He X, Wang J, Guggenberger G, Wu J (2016) Fate of rice shoot and root residues, rhizodeposits, and microbe-assimilated carbon in paddy soil – part 1: decomposition and priming effect. Biogeosciences 13:4481–4489

    Article  Google Scholar 

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Acknowledgments

The present study was supported by the National Natural Science Foundation of China (41522107; 41501321), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020401), and the Recruitment Program of High-End Foreign Experts of the State Administration of Foreign Experts Affairs, awarded to Prof. Georg Guggenberger (GDT20164300013). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance.

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Zhu, Z., Ge, T., Hu, Y. et al. Fate of rice shoot and root residues, rhizodeposits, and microbial assimilated carbon in paddy soil - part 2: turnover and microbial utilization. Plant Soil 416, 243–257 (2017). https://doi.org/10.1007/s11104-017-3210-4

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