Skip to main content
SpringerLink
Log in

Effect of methyl 3-4-hydroxyphenyl propionate, a Sorghum root exudate, on N dynamic, potential nitrification activity and abundance of ammonia-oxidizing bacteria and archaea

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

It has been reported that root exudates of Sorghum bicolor can inhibit nitrification in a bioassay using Nitrosomonas, and methyl 3-(4-hydroxyphenyl) propionate (MHPP) was identified as one of the nitrification inhibiting compounds. Therefore, we have investigated the effects of this compound on nitrogen dynamic, potential nitrification activity and on soil microorganisms.

Methods

We conducted soil incubation experiments using synthetic MHPP to evaluate its effect on changes in inorganic soil nitrogen pools, on nitrification activity and on abundance of ammonia-oxidizing bacteria and archaea. Addition of MHPP at two concentrations equivalent to 70 and 350 μg C g−1 soil was compared to glucose as a carbon source and to the commercially available nitrification inhibitor dicyandiamide (DCD).

Results

Soil amended with the high dose of MHPP and with DCD showed reduced nitrate content and low nitrification activity after 3 and 7 days of incubation. This was mirrored by a 70 % reduction in potential nitrification activity compared to a nitrogen-only control. None of the incubation treatments affected non-target microbial counts as estimated by 16S rRNA gene copy numbers, however, the high dose of MHPP significantly reduced the abundance of ammonia-oxidizing bacteria and archaea.

Conclusions

These findings suggest that MHPP is capable of suppressing nitrification in soil, possibly by reducing the population size and activity of ammonia-oxidizing microorganisms.

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

Similar content being viewed by others

References

  • Amberger A (1989) Research on dicyandiamide as a nitrification inhibitor and future outlook. Commun Soil Sci Plant Anal 20:1933–1955

    Article  CAS  Google Scholar 

  • Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Appl Environ Microbiol 72:7767–7777

    Article  PubMed  CAS  Google Scholar 

  • Ceccherini MT, Ascher J, Pietramellara G, Mocali S, Viti C, Nannipieri P (2007) The effect of pharmaceutical waste-fungal biomass, treated to degrade DNA, on the composition of eubacterial and ammonia oxidizing populations of soil. Biol Fertil Soils 44:299–306

    Article  CAS  Google Scholar 

  • Einhellig FA, Souza IF (1992) Phytotoxicity of sorgoleone found in grain sorghum root exudates. J Chem Ecol 18:1–11

    Article  CAS  Google Scholar 

  • FAO (1974) Legend of the Soil Map of the World. UNESCO, Paris

  • Felske A, Holger RI, Wokerink A, Stackebrandt E, Akkermans ADL (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143:2983–2989

    Article  PubMed  CAS  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle JS, Bottomley BS (eds) Methods of Soil Analysis. Part 2. Microbiological and Biochemical Properties. Soil Science Society of America, Madison, pp 985–1018

    Google Scholar 

  • Jones DL, Darrah PR (1996) Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere. 3. Characteristics of sugar influx and efflux. Plant Soil 178:153–160

    Article  CAS  Google Scholar 

  • Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L (2004) Grass populations control nitrification in savanna soils. Funct Ecol 18:605–611

    Article  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  • Linn DM, Doran JW (1984) Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and non tilled soils. Soil Sci Soc Am J 48:1264–1272

    Google Scholar 

  • Lueders T, Friedrich MW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69:320–326

    Article  PubMed  CAS  Google Scholar 

  • More DRE, Waid JS (1971) The influence of washing of living roots on nitrification. Soil Biol Biochem 3:69–83

    Article  Google Scholar 

  • Nübel U, Engelen B, Felske A et al (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643

    PubMed  Google Scholar 

  • Pariasca TJ, Nardi P, Wissuwa M (2010) Nitrification inhibition activity, a novel trait in root exudates of rice. AoB Plants. doi: 10.1093/aobpla/plq014

  • Park HD, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647

    Article  PubMed  CAS  Google Scholar 

  • Perry LG, Thelen GC, Ridenour WM, Callaway RM, Paschke MW et al (2007) Concentrations of the allelochemical (±)-catechin in Centaurea maculosa soils. J Chem Ecol 33:2337–2344

    Article  PubMed  CAS  Google Scholar 

  • Prasad R, Power PJ (1995) Nitrification inhibitors for the agriculture health and environment. Adv Agron 54:233–281

    Article  CAS  Google Scholar 

  • Rice E, Pancholy SK (1972) Inhibition of nitrification by climax ecosystems. Am J Bot 59:1033–1040

    Article  Google Scholar 

  • Rice CW, Tiedje JM (1989) Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biol Biochem 21:597–602

    Article  CAS  Google Scholar 

  • Rotthauwe JH, Witzel K-P, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed  CAS  Google Scholar 

  • Schimel JP, Van Cleve K, Cates RG, Clausen TP, Reichardt PB (1996) Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: Implications for changes in N cycling during succession. Can J Bot 74:84–90

    Article  CAS  Google Scholar 

  • Schlesinger WH (2009) On the fate of anthropogenic nitrogen. Proc Natl Acad Sci 106:203–208

    Article  PubMed  CAS  Google Scholar 

  • Shi S, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK, Condron LM (2011) Effects of selected root exudate components on soil bacterial communitiesFEMS. Microbiol Ecol 77:600–610

    Article  CAS  Google Scholar 

  • Smits NAC, Hefting MM, Kamst-van Agterveld MP, Laanbroek HJ, Paalman AJ, Bobbink R (2010) Nitrification along a grassland gradient: Inhibition found in matgrass swards. Soil Biol Biochem 42:635–641

    Article  CAS  Google Scholar 

  • Subbarao GV, Ishikawa T, Ito O, Nakahara K, Wang HY, Berry WL (2006) A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant Soil 288:101–112

    Article  CAS  Google Scholar 

  • Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, Lascano C, Berry WL (2007a) Biological nitrification inhibition (BNI)—Is it a widespread phenomenon? Plant Soil 294:5–18

    Article  CAS  Google Scholar 

  • Subbarao GV, Ban T, Masahiro K, Ito O, Samejima H, Wang HY, Pearse SJ, Gopalakrishnan S, Nakahara K, Hossain AKMZ, Tsujimoto H, Berry WL (2007b). Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming?

  • Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proc Nat Acad Sci U S A 106:17302–17307

    Article  CAS  Google Scholar 

  • Subbarao GV, Nakahara K, Ishikawa T, Ono H, Yoshida M, Yoshihashi T, Zhu Y, Zakir HAKM, Deshpande SP, Hash CT, Sahrawat KL (2012a) Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil. doi 10.1007/s11104-012-1419-9

  • Subbarao GV, Sahrawat KL, Nakahara K, Ishikawa T, Kudo N, Kishii M, Rao IM, Hash CT, George TS, Srinivasa RP, Nardi P, Bonnett D, Berry W, Suenaga K, Ito O, Lata JC (2012b) Biological Nitrification Inhibition (BNI):—A Novel Strategy to Regulate Nitrification in Agricultural Systems. Advances in Agronomy Vol 114

  • Trenkel, M.E. (1997). Controlled-Release and Stabilized Fertilizers in Agriculture. International Fertilizer Industry Association

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schlepler C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  PubMed  CAS  Google Scholar 

  • Vivanco JM, Bais HP, Stermitz FR, Thelen G, Callaway R (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292

    Article  Google Scholar 

  • Watkins AJ, Nicol GW, Shaw LJ (2009) Use of an artificial root to examine the influence of 8-hydroxyquinoline on soil microbial activity and bacterial community structure. Soil Biol Biochem 41:580–585

    Article  CAS  Google Scholar 

  • Wrage N, Velthof GL, Beusichem MLV, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732

    Article  CAS  Google Scholar 

  • Zakir HAKM, Subbarao GV, Pearse SJ, Gopalakrishnan S, Ito O, Ishikawa T, Kawano N, Nakahara K, Yoshihashi T, Ono H, Yoshida M (2008) Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl) propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor). New Phytol 180:442–451

    Article  PubMed  CAS  Google Scholar 

  • Zhang LM, Offre PR, He LZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U S A 107:17240–17245

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

P. Nardi was funded by the Japan Society for Promotion of Science (JSPS) postdoctoral fellowship. We are grateful to Dr. M.T. Ceccherini (University of Firenze) for valuable discussions and critical comments on the manuscript. We also thank to Dr. G. Renella (University of Firenze) for kindly providing the soil used in this research and Taro Matsuda (JIRCAS) for technical support.

Author information

Authors and Affiliations

  1. Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences (JIRCAS), 1-1 Ohwashi, Tsukuba, Ibaraki, Japan, 305-8686

    Pierfrancesco Nardi, Masako Akutsu, Juan Pariasca-Tanaka & Matthias Wissuwa

Authors
  1. Pierfrancesco Nardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masako Akutsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Pariasca-Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthias Wissuwa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthias Wissuwa.

Additional information

Responsible Editor: Liz Shaw.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nardi, P., Akutsu, M., Pariasca-Tanaka, J. et al. Effect of methyl 3-4-hydroxyphenyl propionate, a Sorghum root exudate, on N dynamic, potential nitrification activity and abundance of ammonia-oxidizing bacteria and archaea. Plant Soil 367, 627–637 (2013). https://doi.org/10.1007/s11104-012-1494-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1494-y

Keywords

Search

Navigation