Skip to main content

Advertisement

SpringerLink
Log in

Cellulose and lignin regulate partitioning of soil phosphorus fractions and alkaline phosphomonoesterase encoding bacterial community in phosphorus-deficient soils

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Crop straw retention is believed to effectively promote soil phosphorus (P) availability. However, little is known about how specific components of crop straw, such as cellulose and lignin, regulate soil P availability, which depends on several processes, including the reactions catalyzed by phosphomonoesterase activities. Of the genes encoding alkaline phosphomonoesterase, phoD are ubiquitous in soil. Here, we studied the effects of cellulose and lignin on soil P fractions and phoD-harboring bacterial community in P-deficient upland and paddy soils. In the upland soil, cellulose amendment significantly increased microbial P assimilation and decreased soil citrate-P and HCl-P fractions, suggesting that cellulose mediated the conversion of soil P fractions from the non-labile to the labile P pool (e.g., microbial P) via microbial enrichment. Lignin significantly increased soil Olsen-P content, but scarcely influenced P-related microbial parameters after incubation for 60 days. Therefore, lignin directly increased soil available P via competitive P adsorption by lignin functional groups, rather than by altering soil microbial processes. Compared to upland soil, a smaller effect of both cellulose and lignin on phoD gene abundance, alkaline phosphomonoesterase activity, and phoD-harboring bacterial community was observed in paddy soil, suggesting that the carbon inputs may be unable to promote organic P availability under oxygen-deficient conditions. Our results highlight the contrasting mechanisms of soil P availability regulation via cellulose or lignin in P-deficient soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Acuña JJ, Durán P, Lagos LM, Ogram A, de la Luz Mora M, Jorquera MA (2016) Bacterial alkaline phosphomonoesterase in the rhizospheres of plants grown in Chilean extreme environments. Biol Fertil Soils 52:763–773

    Article  Google Scholar 

  • Bååth E, Frostegard A, Pennanen T, Fritze H (1995) Microbial community structure and pH response in relation to soil organic matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol Biochem 27:229–240

    Article  Google Scholar 

  • Béguin P, Aubert J (1994) The biological degradation of cellulose. FEMS Microbiol Rev 13:25–58

    Article  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Creamer CA, Jones DL, Baldock JA, Farrell M (2014) Stoichiometric controls upon low molecular weight carbon decomposition. Soil Biol Biochem 79:50–56

    Article  CAS  Google Scholar 

  • Cui H, Zhou Y, Gu ZH, Zhu HH, Fu SL, Yao Q (2015) The combined effects of cover crops and symbiotic microbes on phosphatase gene and organic phosphorus hydrolysis in subtropical orchard soils. Soil Biol Biochem 82:119–126

    Article  CAS  Google Scholar 

  • Damon PM, Bowden B, Rose T, Rengel Z (2014) Crop residue contributions to phosphorus pools in agricultural soils: a review. Soil Biol Biochem 74:127–137

    Article  CAS  Google Scholar 

  • Deluca TH, Glanville HC, Harris M, Emmett BA, Pingree MRA, Sosa LLD, Cerdá-Moreno C, Jones DL (2015) A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–119

    Article  CAS  Google Scholar 

  • Dinh MV, Guhr A, Spohn M, Matzner E (2017) Release of phosphorus from soil bacterial and fungal biomass following drying/rewetting. Soil Biol Biochem 110(1–7):1–7

    Article  CAS  Google Scholar 

  • Easterwood GW, Sartain JB (1990) Clover residue effectiveness in reducing orthophosphate sorption on ferric hydroxide coated soil. Soil Sci Soc Am J 54:1345–1350

    Article  CAS  Google Scholar 

  • Espinosa D, Sale P, Tang C (2017) Effect of soil phosphorus availability and residue quality on phosphorus transfer from crop residues to the following wheat. Plant Soil 416:361–375

    Article  CAS  Google Scholar 

  • Fraser T, Lynch DH, Entz MH, Dunfield KE (2015) Linking alkaline phosphatase activity with bacterial pho D gene abundance in soil from a long-term management trial. Geoderma 257:115–122

    Article  Google Scholar 

  • Guillon E, Merdy P, Aplincourt M, Dumonceau J, Vezin H (2001) Structural characterization and iron (III) binding ability of dimeric and polymeric lignin models. J Colloid Interface Sci 239:39–48

    Article  CAS  Google Scholar 

  • Guo XY, Zhang SZ, Shan XQ (2008) Adsorption of metal ions on lignin. J Hazard Mater 151:134–142

    Article  CAS  Google Scholar 

  • Haynes RJ (1982) Effects of liming on phosphate availability in acid soils: a critical review. Plant Soil 68:289–308

    Article  CAS  Google Scholar 

  • Herbien SA, Neal JL (1990) Soil pH and phosphatase activity. Commun Soil Sci Plant Anal 21:439–456

    Article  CAS  Google Scholar 

  • Hu HW, Zhang LM, Yuan CL, He JZ (2013) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27

    Article  CAS  Google Scholar 

  • Hu YJ, Xia YH, Sun Q, Liu KP, Chen XB, Ge TD, Zhu BL, Zhu ZK, Zhang ZH, Su YR (2018) Effects of long-term fertilization on phoD-harboring bacterial community in Karst soils. Sci Total Environ 628:53–63

    Article  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    Article  Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron Sustain Dev 27:29–43

    Article  Google Scholar 

  • Krämer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32:179–188

    Article  Google Scholar 

  • Lagos LM, Acuña JJ, Maruyama F, Ogram A, de la Luz Mora M, Jorquera MA (2016) Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fertil Soils 52:1007–1019

    Article  CAS  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  Google Scholar 

  • Leytem AB, Mikkelsen RL, Gilliam JW (2002) Sorption of organic phosphorus compounds in Atlantic coastal plain soils. Soil Sci 167:652–658

    Article  CAS  Google Scholar 

  • Liu EK, Yan CR, Mei XR, He WQ, Bing SH, Ding LP, Liu Q, Liu S, Fan TL (2010) Long-term effect of chemical fertilizer, straw, and manure on soil chemical and biological properties in northwest China. Geoderma 158:173–180

    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 

  • Luo GW, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo SW, Shen QR (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388

    Article  CAS  Google Scholar 

  • Lynd LR, Weimer PJ, Zyl WHV, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    Article  CAS  Google Scholar 

  • Mosin O, Ignatov I (2014) Evolution, metabolism and biotechnological usage of methylotrophic microorganisms. Eur J Mol Biotechnol 5:131–148

    Article  Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 215–243

    Chapter  Google Scholar 

  • Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19

    Article  CAS  Google Scholar 

  • Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895

    Article  CAS  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture Circular 939, US Department of Agriculture, Washington DC

  • Qiu YQ, Gan GJ, Liu W, Liu Y, Hou HB, Peng PQ, Gao TJ (2013) Haracteristics of phosphate adsorption and desorption in soils under different utilization. Chin J Environ Eng 7:2758–2760

    Google Scholar 

  • Ragot SA, Kertesz MA, Bünemann EK (2015) phoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:7281–7289

    Article  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996

    Article  CAS  Google Scholar 

  • Rousk J, Brookes PC, Glanville HC, Jones DL (2011) Lack of correlation between turnover of low-molecular-weight dissolved organic carbon and differences in microbial community composition or growth across a soil pH gradient. Appl Environ Microbiol 77:2791–2795

    Article  CAS  Google Scholar 

  • Rui JP, Peng JJ, Lu YH (2009) Succession of bacterial populations during plant residue decomposition in rice field soil. Appl Environ Microbiol 75:4879–4886

    Article  CAS  Google Scholar 

  • Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71

    Article  CAS  Google Scholar 

  • Schutter M, Dick R (2001) Shifts in substrate utilization potential and structure of soil microbial communities in response to carbon substrates. Soil Biol Biochem 33:1481–1491

    Article  CAS  Google Scholar 

  • Shi Y, Chai LY, Tang CJ, Yang ZH, Zhang H, Chen RH (2013) Characterization and genomic analysis of Kraft lignin biodegradation by the beta-proteobacterium Cupriavidus basilensis B-8. Biotechnol Biofuels 6(1):14

    Article  Google Scholar 

  • Šnajdr J, Steffen KT, Hofrichter M, Baldrian P (2010) Transformation of 14C-labelled lignin and humic substances in forest soil by the saprobic basidiomycetes Gymnopus erythropus and Hypholoma fasciculare. Soil Biol Biochem 42:1541–1548

    Article  Google Scholar 

  • Spees JL, Olson SD, Whitney MJ, Prockop DJ (2006) Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci U S A 103:1283–1288

    Article  CAS  Google Scholar 

  • Sun RB, Zhang XX, Guo XS, Wang DZ, Chu HY (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18

    Article  CAS  Google Scholar 

  • Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O’Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Torres IF, Bastida F, Hernández T, Bombach P, Richnow HH, Garcia C (2014) The role of lignin and cellulose in the carbon-cycling of degraded soils under semiarid climate and their relation to microbial biomass. Soil Biol Biochem 75:152–160

    Article  CAS  Google Scholar 

  • Turner BL, Driessen JP, Haygarth PM, Mckelvie ID (2003) Potential contribution of lysed bacterial cells to phosphorus solubilisation in two rewetted Australian pasture soils. Soil Biol Biochem 35:187–189

    Article  CAS  Google Scholar 

  • Van de Graaf AA, De Bruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142:2187–2196

    Article  Google Scholar 

  • Wetzel RG (1991) Extracellular enzymatic interactions: storage, redistribution, and interspecific communication. Microbial enzymes in aquatic environments. Springer, New York, pp 6–28

    Google Scholar 

  • Wu JS, 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 JS, Huang M, Xiao HA, Su YR, Tong CL, Huang DY, Syers JK (2007) Dynamics in microbial immobilization and transformations of phosphorus in highly weathered subtropical soil following organic amendments. Plant Soil 290:333–342

    Article  CAS  Google Scholar 

  • Xie XH, Mackenzie AF, Xie RJ, Fyles JW, O’Halloran IP (1995) Effects of ammonium lignosulphonate and diammonium phosphate on soil organic carbon, soil phosphorus fractions and phosphorus uptake by corn. Can J Soil Sci 75:233–238

    Article  CAS  Google Scholar 

  • Ye D, Li T, Zhang X, Zheng Z, Dai W (2017) Rhizosphere P composition, phosphatase and phytase activities of Polygonum hydropiper grown in excess P soils. Biol Fertil Soils 53:823–836

    Article  CAS  Google Scholar 

  • Zhu J, Li M, Whelan M (2018) Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ 612:522–537

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by grants from the National key Research Program (2017YFC0505503); National Science Foundation (41601260; 41471199); and The Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020401).

Author information

Author notes

  1. Qi Sun and Husen Qiu contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha City, Hunan Province, 410125, People’s Republic of China

    Qi Sun, Husen Qiu, Yajun Hu, Xiaomeng Wei, Xiangbi Chen, Tida Ge, Jinshui Wu & Yirong Su

  2. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Qi Sun, Husen Qiu & Xiaomeng Wei

Authors
  1. Qi Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Husen Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yajun Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaomeng Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiangbi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tida Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jinshui Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yirong Su
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yajun Hu.

Electronic supplementary material

ESM 1

(DOC 2731 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, Q., Qiu, H., Hu, Y. et al. Cellulose and lignin regulate partitioning of soil phosphorus fractions and alkaline phosphomonoesterase encoding bacterial community in phosphorus-deficient soils. Biol Fertil Soils 55, 31–42 (2019). https://doi.org/10.1007/s00374-018-1325-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-018-1325-2

Keywords

Search

Navigation