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Synergism between urea and urease-positive bacteria in controlling root-knot nematodes

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Abstract

Synergistic effects between urea and urease-positive bacteria against root-knot nematodes were assayed in laboratory and greenhouse trials. We isolated 85 urease-positive bacterial strains from soil, compost, sludge, and animal faeces; they belonged to four clades and sixteen genera of Eubacteria based on 16S rRNA BLAST. Twenty-five representative strains were assessed for nematicidal and urease activities. The urease-positive bacteria were nematicidal. A cubic relationship with a critical threshold was found between a strain’s nematicidal and urease activities. Sixteen strains with urease activity above this threshold had a 100 % nematicidal activity level. These 16 strains and urea alone were assessed for urease activity in pot experiments with tomato, which found that high-dose urea was nematicidal to root-knot nematodes (400–800 mg per kg soil) and phytotoxic (1,600 mg), while low-dose urea (≤200 mg) was non-nematicidal. However, nematodes could be controlled at 200 mg urea per kg soil in combination with urease-positive bacteria from seven different strains, and the nematode control efficacy of urea was always non-linearly positively correlated with soil urease activity. To test bacterial persistence, soils were recycled for another experiment, in which nine strains were significantly nematicidal, with a stronger relationship between nematode control efficacy and soil urease activity. These results suggest ways to manipulate soil bacteria to improve soil urease activity for the management of plant-parasitic nematodes. While urease-positive bacteria may have practical applications in controlling nematodes, their use will require careful field investigation and appropriate environmental safety evaluation.

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References

  • Achal, V., & Pan, X. L. (2011). Characterization of urease and carbonic anhydrase producing bacteria and their role in calcite precipitation. Current Microbiology, 62, 894–902.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, S., Al-Hazmi, & Ahmed, A. M. D. (2014). Effect of urea and certain NPK fertilizers on the cereal cyst nematode (Heterodera avenae) on wheat. Saudi Journal of Biological Sciences, 21, 191–196.

    Article  Google Scholar 

  • Akhtar, M. (1999). Plant growth and nematode dynamics in response to soil amendments with neem products, urea and compost. Bioresource Technology, 69, 181–183.

    Article  CAS  Google Scholar 

  • Anuradha, B., & Karthe, P. (2010). Crystal structure of the first plant urease from jack bean: 83 years of journey from its first crystal to molecular structure. Journal of Molecular Biology, 400, 274–283.

    Article  Google Scholar 

  • Blaxter, M. L. (2003). Nematoda: genes, genomes and the evolution of parasitism. Advances in Parasitology, 54, 101–195.

    Article  PubMed  Google Scholar 

  • Briar, S. S., Grewal, P. S., Somasekhar, N., Stinner, D., & Miller, S. A. (2007). Soil nematode community, organic matter, microbial biomass and nitrogen dynamics in field plots transitioning from conventional to organic management. Applied Soil Ecology, 37, 256–266.

    Article  Google Scholar 

  • Britto, D. T., Siddiqi, M. Y., Glass, A. D. M., & Kronzucker, H. J. (2001). Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences USA, 98, 4255–4258.

    Article  CAS  Google Scholar 

  • Chakravarthula, M., & Krishna, G. M. (2006). Rhizosphere biology-an overview. Soil Biology, 7, 1–15.

    Article  Google Scholar 

  • Ciurli, S., Marzadori, C., Benini, S., Deiana, S., & Gessa, C. (1996). Urease from the soil bacterium Bacillus pasteurii: immobilization on Ca-polygalacturonate. Soil Biology Biochemistry, 28(6), 811–817.

    Article  CAS  Google Scholar 

  • Cover, T. L., Puryear, W., Perez-Perez, G. I., & Blaser, M. J. (1991). Effect of urease on HeLa cell vacuolation induced by Helicobacter pylori cytotoxin. Infection and Immunity, 59(4), 1264–1270.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crow, W. T., Guertal, E. A., & Rodríguez-kábana, R. (1996). Responses of Meloidogyne arenaria and M. incognita to green manures and supplemental urea in glasshouse culture. Journal of Nematology, 28(4), 648–654.

    CAS  PubMed Central  PubMed  Google Scholar 

  • D’Addabbo, T., & Sasanelli, N. (1997). Suppression of Meloidogyne incognita by combinations of olive pomace of wheat straw with urea. Nematology Meditations, 25, 159–164.

    Google Scholar 

  • Díaz, A., Vàzquez, L., Ventura, F., & Galceran, M. T. (2004). Estimation of measurement uncertainty for the determination of nonylphenol in water using solid-phase extraction and solid-phase microextraction procedures. Analytica Chimica Acta, 506, 71–80.

    Article  Google Scholar 

  • Docherty, P. A., & Snider, M. D. (1991). Effect of hypertonic and sodium-free medium on transport of a membrane glycoprotein along the secretory pathway in cultured mammalian cells. Journal of Cell Physiology, 146, 34–42.

    Article  CAS  Google Scholar 

  • Dong, L. Q., & Zhang, K. Q. (2006). Microbial control of plant-parasitic nematodes: a five-party interaction. Plant and Soil, 288, 31–45.

    Article  CAS  Google Scholar 

  • Erwin, A., Simona, P., Anna, M., & Paula, P. (2012). Assessment of rhizobacteria from grapevine for their suppressive effect on the parasitic nematode Xiphinema index. Crop Protection, 42, 36–41.

    Article  Google Scholar 

  • Farshid, N., & Carlos, M. M. (2004). Effects of soil properties and trace metals on urease activities of calcareous soils. Biology and Fertility of Soils, 40, 359–362.

    Article  Google Scholar 

  • Gerhard, H., Ulrich, S., Giuseppe, V., Matthias, H., Stefan, B., Heike, C., & Ulrich, V. (2003). Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiology, 149, 67–75.

    Article  Google Scholar 

  • Gilbert, P. M., Harrison, J., Heil, C., & Seitzinger, S. (2006). Escalating worldwide use of urea-a global change contributing to coastal eutrophication. Biogeochemistry, 77, 441–463.

    Article  Google Scholar 

  • Glazer, I., & Orion, D. (1984). Influence of urea, hydroxyurea, and thiourea on Meloidogyne javanica infected excised tomato roots in culture. Journal of Nematology, 16, 125–130.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gu, Y. Q., Mo, M. H., Zhou, J. P., Zou, C. S., & Zhang, K. Q. (2007). Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biology and Biochemistry, 39, 2567–2575.

    Article  CAS  Google Scholar 

  • Huang, Y., Xu, C. K., Ma, L., Zhang, K. Q., Duan, C. Q., & Mo, M. H. (2010). Characterisation of volatiles produced from Bacillus megaterium YEM3.25 and their nematicidal activity against Meloidogyne incognita. Europe Journal of Plant Pathology, 126, 417–422.

    Article  CAS  Google Scholar 

  • Huang, X. Q., Zhang, N., Yong, X. Y., Yang, X. M., & Shen, Q. R. (2011). Biocontrol of Rhizoctonia solani damping-off disease in cucumber with Bacillus pumilus SQR-N43. Microbiological Research, 3, 1–9.

    CAS  Google Scholar 

  • Javier, A. C. N., Flor, N. R. O., Leonardo, P. Z., Anton, V. S., Jose, C., Bram, G., & Luc, G. (2010). Phylogenetic and multivariate analyses to determine the effects of different tillage and residue management practices on soil bacterial communities. Applied and Environmental Microbiology, 76(11), 3685–3691.

    Article  Google Scholar 

  • Jiao, X. G., Liang, W. J., Chen, L. J., Zhang, H. J., Li, Q., Wang, P., & Wen, D. Z. (2005). Effects of slow-release urea fertilizers on urease activity, microbial biomass, and nematode communities in an aquic brown soil. Science in China Series C-Life Sciences, 48(1), 26–32.

    Article  CAS  Google Scholar 

  • Kandeler, E., & Gerber, H. (1988). Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils, 6, 68–72.

    Article  CAS  Google Scholar 

  • Lane, D.J. (1991). 16S/23S rRNA sequencing. Stackbrandt, E. and Goodfellow, M., (eds.), Nucleic acid techniques in bacterial systematics, New York, pp. 115–175.

  • Liang, W. J., Li, Q., Jiang, Y., & Neher, D. A. (2005). Nematode faunal analysis in an aquic brown soil fertilized with slow-release urea, Northeast China. Applied Soil Ecology, 29, 185–192.

    Article  Google Scholar 

  • Ma, L., Fu, W., Huang, Y., Mo, M. H., Xi, J. Q., Duan, Y. Q., & Yang, S. H. (2012). A strategy to discover potential nematicidal fumigants based on toxic volatiles from nematicidal bacteria. African Journal of Microbiology, 6(31), 6106–6113.

    CAS  Google Scholar 

  • Mobley, H. L. T., Island, M. D., & Hausinger, R. P. (1995). Molecular biology of microbial ureases. Microbiology Review, 59(3), 451–480.

    CAS  Google Scholar 

  • Niu, Q. H., Huang, X. W., & Tian, B. Y. (2006). Bacillus sp. B16 kill nematodes with a serine protease identified as a pathogenic factor. Applied Microbiology Biotechnology, 69, 722–730.

    Article  CAS  Google Scholar 

  • Oka, Y. (2010). Mechanisms of nematode suppression by organic soil amendments-a review. Applied Soil Ecology, 44, 101–115.

    Article  Google Scholar 

  • Oka, Y., Chet, I., & Spiegel, I. (1993). Control of the root-knot nematode Meloidogyne javanica by Bacillus cereus. Biocontrol Science and Technology, 3, 115–126.

    Article  Google Scholar 

  • Oka, Y., Koltai, H., Bar-Eyal, M., Mor, M., Sharon, E., Chet, I., & Spiegel, Y. (2000). New strategies for the control of plant-parasitic nematodes. Pest Management Science, 56, 983–988.

    Article  CAS  Google Scholar 

  • Oka, Y., Shapira, N., & Fine, P. (2007). Control of root-knot nematodes in organic farming systems by organic amendments and soil solarization. Crop Protection, 26, 1556–1565.

    Article  Google Scholar 

  • Pierre, A., Jérǒme, G., Jean-Marc, A., et al. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology, 26(8), 909–915.

    Article  Google Scholar 

  • Plessis, M. C. F. D., & Kroontje, W. (1964). The relationship between pH and ammonia equilibria in soil. Soil Science Society of America Journal, 28(6), 751–754.

    Article  Google Scholar 

  • Rush, C. M., & Lyda, S. D. (1982). Effects of anhydrous ammonia on mycelium and sclerotia of Phymatotrichum omnivorum. Phytopathology, 72, 1085–1089.

    Article  CAS  Google Scholar 

  • Saroj, K. M., James, E. K., James, R. M., Rod, M. H., & Muraleedharan, G. N. (1987). Insecticidal and nematicidal properties of microbial metabolites. Journal of Industrial Microbiology, 2, 267–276.

    Article  Google Scholar 

  • Siddiqui, Z. A., & Mahmood, I. (1999). Role of bacteria in the management of plant parasitic nematodes: a review. Bioresource Technology, 69, 167–179.

    Article  CAS  Google Scholar 

  • Timper, P. (2011). Utilization of biological control for managing plant-parasitic nematodes. Progress of Biological Control, 11, 259–289.

    Google Scholar 

  • Trudgill, D. L., & Blok, V. C. (2001). Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annual Review of Phytopathology, 39, 53–77.

    Article  CAS  PubMed  Google Scholar 

  • Verschoor, B. C., Goede, R. G. M., & Brussaard, L. (2002). Do plant parasitic nematodes have differential effects on the productivity of a fast- and a slow -growing grass species? Plant and Soil, 243, 81–90.

    Article  CAS  Google Scholar 

  • Wani, A. H., & Yaqub Bhat, M. (2012). Control of root-knot nematode, Meloidogyne incognita by urea coated with Nimin or other natural oils on mung, Vigna radiata (L.) R. Wilczek. Journal Biopest, 5, 255–258.

    Google Scholar 

  • Wei, C. Z., Zhen, H. F., Li, Q., Lü, X. T., Yu, Q., Zhang, H. Y., Chen, Q. S., He, N. P., Paul, K., Liang, W. J., & Han, X. G. (2012). Nitrogen addition regulates soil nematode community composition through ammonium suppression. Plos One, 7(8), 1–9.

    Google Scholar 

  • Westerdahl, B. B., Carlson, H. L., Grant, J., Radewald, J. D., Welch, N., Anderson, C. A., Darso, J., Kirby, D., & Shibuya, F. (1992). Management of plant-parasitic nematodes with a chitin-urea soil amendment and other materials. Journal of Nematology, 24(4), 669–680.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Widmer, T. L., Mitkowski, N. A., & Abawi, G. S. (2002). Soil organic matter and management of plant-parasitic nematodes. Journal of Nematology, 34(4), 289–295.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu, C. K., Mo, M. H., Zhang, L. M., & Zhang, K. Q. (2004). Soil volatile fungistasis and volatile fungistatic compounds. Soil Biology Biochemistry, 36, 1997–2004.

    Article  CAS  Google Scholar 

  • Yeasmin, S., Mominul Islam, A. K. M., & Aminul Islam, A. K. M. (2012). Nitrogen fractionation and its mineralization in paddy soils: a review. Journal of Agricultural Science and Technology, 8, 775–793.

    CAS  Google Scholar 

  • Younis, M. E., Hasaneen, M. N. A., Ahmed, A. R., & EI-Bialy, D. M. (2008). Plant growth, metabolism and adaptation in relation to stress conditions. XXI. reversal of harmful NaCl-effects in lettuce plants by foliar application with urea. Australian Journal of Crop Science, 2(2), 83–85.

    CAS  Google Scholar 

  • Zaki, A. S., & Irshad, M. (1996). Biological control of plant parasitic nematodes by fungi: a review. Bioresource Technology, 58, 229–239.

    Article  Google Scholar 

  • Zeng, D., Chen, B., Yao, S. Z., & Ying, J. Y. (2006). Determination of tetramethylenedisulfotetramine in human urine with gas chromatograph-flame thermionic detection coupling with direct immersed solid-phase micro-extraction. Forensic Science International, 159, 168–174.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, Q. F., Huang, H. Q., Zhu, J., Fang, Z., Sun, Q. G., & Bao, S. X. (2013). A new nematicidal compound produced by Streptomyces albogriseolus HA10002. Antonie van Leeuwenhoek, 103, 1107–1111.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank Louis and Jianrong Wu for their assistance with our English expression. This work was financially supported by grants from the “National Key Sciences and Technology Program for Water Solutions” (2012ZX07102-003), NSFC (30970100, 31160376), China.

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Authors and Affiliations

  1. Key Laboratory of Plant Pathology of the Ministry of Education, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Fu Wen & Yueqiu He

  2. Laboratory for Conservation and Utilization of Bio-Resources and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming, 650091, People’s Republic of China

    Zhixiao Zhang, Ma Li & Minghe Mo

  3. School of Life Sciences, Yunnan University, Kunming, 650091, Yunnan, People’s Republic of China

    Zhen Chen

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  1. Fu Wen
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  2. Zhixiao Zhang
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  3. Yueqiu He
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Correspondence to Minghe Mo.

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Wen, F., Zhang, Z., He, Y. et al. Synergism between urea and urease-positive bacteria in controlling root-knot nematodes. Eur J Plant Pathol 141, 179–191 (2015). https://doi.org/10.1007/s10658-014-0536-0

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