Skip to main content

Advertisement

Log in

Rhizobacterial Pseudomonas spp. Strains Harbouring acdS Gene Could Enhance Metallicolous Legume Nodulation in Zn/Pb/Cd Mine Tailings

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Phytostabilisation can benefit from phytostimulatory rhizobacteria. Forty-three bacterial strains were isolated from the roots of the metallicolous legume Anthyllis vulneraria ssp. carpatica grown in a highly contaminated mine tailing (total Cd, Pb and Zn were up to 1200; 34,000; and 170,000 mg kg−1, respectively). We aimed at evaluating their phytostimulatory effects on the development of leguminous metallophytes. Strains were screened for fluorescent siderophores and auxin synthesis, inorganic P solubilisation and 1-amino-cyclopropane-1-carboxylate deaminase (ACCd) activity to define a subset of 11 strains that were inoculated on the leguminous metallophytes A. vulneraria and Lotus corniculatus grown in diluted mine spoil (Zn 34,653; Pb 6842; and Cd 242, all in mg kg−1). All strains were affiliated to Pseudomonas spp. (except two), synthetised auxins and siderophores and solubilised P (except three), and seven of them were ACCd positive. The inoculation effects (shoot-root-nodule biomass, chlorophyll content) depended on legume species and bacterial strain genotype. Phytostimulation scores were unrelated to siderophore/auxin synthesis and P solubilisation rates. Inoculations of the strain nos. 17–43 triggered a 1.2-fold significant increase in the chlorophyll content of A. vulneraria. Chlorophyll content and root biomass of L. corniculatus were significantly increased following the inoculations of the strain nos. 17–22 (1.5–1.4-fold, respectively). The strongest positive effects were related to increases in the nodule biomass of L. corniculatus in the presence of three ACCd-positive strains (1.8-fold), one of which was the highest auxin producer. These data suggest to focus on interactions between ACCd activity and auxin synthesis to enhance nodulation of metallicolous legumes.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Ahmad, E., Khan, M. S., & Zaidi, A. (2013). ACC deaminase producing Pseudomonas putida strain PSE3 and Rhizobium leguminosarum strain RP2 in synergism improves growth, nodulation and yield of pea grown in alluvial soils. Symbiosis, 61, 93–104.

    Article  CAS  Google Scholar 

  • Alexander, D. B., & Zuberer, D. A. (1991). Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biology Fertility of Soils, 12, 39–45.

    Article  CAS  Google Scholar 

  • Becerra-Castro, C., Monterroso, C., Prieto-Fernández, A., Rodríguez-Lamas, L., Loureiro-Viñas, M., Acea, M. J., & Kidd, P. S. (2012). Pseudometallophytes colonising Pb/Zn mine tailings: a description of the plant–microorganism–rhizosphere soil system and isolation of metal-tolerant bacteria. Journal of Hazardous Materials, 217–218, 350–359.

    Article  Google Scholar 

  • Belimov, A. A., Dodd, I. C., Hontzeas, N., Theobald, J. C., Safronova, V. I., & Davies, W. J. (2009). Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytologist, 181, 413–423.

    Article  CAS  Google Scholar 

  • Belimov, A. A., Dodd, I. C., Safronova, V. I., Hontzeas, N., & Davies, W. J. (2007). Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. Journal of Experimental Botany, 58, 1485–1495.

    Article  CAS  Google Scholar 

  • Braud, A., Geoffroy, V., Hoegy, F., Mislin, G. L. A., & Schalk, I. J. (2010). Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environmental Microbiology Reports, 2, 419–425.

    Article  CAS  Google Scholar 

  • Braud, A. M., Hubert, M., Gaudin, P., & Lebeau, T. (2015). A quick rhizobacterial selection tests for the remediation of copper contaminated soils. Journal of Applied Microbiology, 119, 435–445.

    Article  CAS  Google Scholar 

  • Burd, G. I., Dixon, D. G., & Glick, B. R. (1998). A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Applied Environmental Microbiology, 64, 3663–3668.

    CAS  Google Scholar 

  • Cardinale, M., Ratering, S., Suarez, C., Montoya, A. M. Z., Geissler-Plaum, R., & Schnell, S. (2015). Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiological Research, 181, 22–32.

    Article  CAS  Google Scholar 

  • Cassán, F., Vanderleyden, J., & Spaepen, S. (2014). Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. Journal of Plant Growth Regulation, 33, 440–459.

    Article  Google Scholar 

  • Cattelan, A. J., Hartel, P. G., & Fuhrmann, J. J. (1999). Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Science Society of America Journal, 63, 1670–1680.

    Article  CAS  Google Scholar 

  • Cornu, J. Y., Elhabiri, M., Ferret, C., Geoffroy, V. A., Jezequel, K., Leva, Y., Lollier, M., Schalk, I. J., & Lebeau, T. (2014). Contrasting effects of pyoverdine on the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere, 103, 212–219.

    Article  CAS  Google Scholar 

  • DeKock, P. C. (1956). Heavy metal toxicity and iron chlorosis. Annals of Botany-London, 20, 133–141.

    Article  CAS  Google Scholar 

  • Dell’Amico, E., Cavalca, L., & Andreoni, V. (2005). Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiology Ecology, 52, 153–162.

    Article  Google Scholar 

  • Dey, R., Pal, K. K., Bhatt, D. M., & Chauhan, S. M. (2004). Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth- promoting rhizobacteria. Microbiological Research, 159, 371–394.

    Article  CAS  Google Scholar 

  • Dimkpa, C. O., Merten, D., Svatoš, A., Büchel, G., & Kothe, E. (2009). Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biology and Biochemistry, 41, 154–162.

    Article  CAS  Google Scholar 

  • Dimkpa, C. O., Svatoš, A., Dabrowska, P., Schmidt, A., Boland, W., & Kothe, E. (2008). Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere, 74, 19–25.

    Article  CAS  Google Scholar 

  • Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Broek, A., & Vanderleyden, J. (1999). Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant and Soil, 212, 155–164.

    Article  CAS  Google Scholar 

  • Frérot, H., Lefèbvre, C., Gruber, W., Collin, C., Dos Santos, A., & Escarré, J. (2006). Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant and Soil, 282, 53–65.

    Article  Google Scholar 

  • Gaby, J.C., & Buckley, D.H. (2012). A comprehensive evaluation of PCR primers to amplify the nifH gene of nitrogenase. PLoS ONE, 7. doi:10.1371/journal.pone.0042149.

  • Gaur, A., & Adholeya, A. (2004). Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Current Science, 86, 528–534.

    CAS  Google Scholar 

  • Glick, B. R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research, 169, 30–39.

    Article  CAS  Google Scholar 

  • Glick, B. R., Todorovic, B., Czarny, J., Cheng, Z., Duan, J., & McConkey, B. (2007). Promotion of plant growth by bacterial ACC deaminase. Critical Reviews in Plant Sciences, 26, 227–242.

    Article  CAS  Google Scholar 

  • Göhre, V., & Paszkowski, U. (2006). Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta, 223, 1115–1122.

    Article  Google Scholar 

  • Grandlic, C. J., Mendez, M. O., Chorover, J., Machado, B., & Maier, R. M. (2008). Plant growth-promoting bacteria for phytostabilization of mine tailings. Environmental Science and Technology, 42, 2079–2084.

    Article  CAS  Google Scholar 

  • Grandlic, C. J., Palmer, M. W., & Maier, R. M. (2009). Optimization of plant growth-promoting bacteria-assisted phytostabilization of mine tailings. Soil Biology and Biochemistry, 41, 1734–1740.

    Article  CAS  Google Scholar 

  • Hol, W.H.G., Bezemer, T.M., & Biere, A. (2013). Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens. Frontiers in Plant Science, doi: org/10.3389/fpls.2013.00081

  • Honma, M., & Shimomura, T. (1978). Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agricultural and Biological Chemistry, 42, 1825–1831.

    CAS  Google Scholar 

  • Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W., & Sessitsch, A. (2004). Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Applied Environmental Microbiology, 70, 2667–2677.

    Article  CAS  Google Scholar 

  • Kuffner, M., De Maria, S., Puschenreiter, M., Fallmann, K., Wieshammer, G., Gorfer, M., Strauss, J., Rivelli, A. R., & Sessitsch, A. (2010). Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. Journal of Applied Microbiology, 108, 1471–1484.

    Article  CAS  Google Scholar 

  • Liu, W., Yang, C., Shi, S., & Shu, W. (2014). Effects of plant growth-promoting bacteria isolated from copper tailings on plants in sterilized and non-sterilized tailings. Chemosphere, 97, 47–53.

    Article  CAS  Google Scholar 

  • Ma, Y., Prasad, M. N. V., Rajkumar, M., & Freitas, H. (2011). Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Advances, 29, 248–258.

    Article  CAS  Google Scholar 

  • Magnucka, E. G., & Pietr, S. J. (2015). Various effects of fluorescent bacteria of the genus Pseudomonas containing ACC deaminase on wheat seedling growth. Microbiological Research, 181, 112–119.

    Article  CAS  Google Scholar 

  • Mahieu, S., Escarré, J., Brunel, B., Méjamolle, A., Soussou, S., Galiana, A., & Cleyet-Marel, J. C. (2014). Soil nitrogen balance resulting from N fixation and rhizodeposition by the symbiotic association Anthyllis vulneraria/Mesorhizobium metallidurans grown in highly polluted Zn, Pb and Cd mine tailings. Plant and Soil, 375, 175–188.

    Article  CAS  Google Scholar 

  • Mahieu, S., Frérot, H., Vidal, C., Galiana, A., Heulin, K., Maure, L., Brunel, B., Lefèbvre, C., Escarré, J., & Cleyet-Marel, J. C. (2011). Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn, Pb and Cd. Plant and Soil, 342, 405–417.

    Article  CAS  Google Scholar 

  • Maynaud, G., Brunel, B., Mornico, D., Durot, M., Severac, D., Dubois, E., Navarro, E., Cleyet-Marel, J. C., & Le-Quéré, A. (2013). Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to zinc and cadmium exposure. BMC Genomics, 14, 292. doi:10.1186/1471-2164-14-292.

    Article  CAS  Google Scholar 

  • Maynaud, G., Willems, A., Soussou, S., Vidal, C., Maure, L., Moulin, L., Cleyet-Marel, J. C., & Brunel, B. (2012). Molecular and phenotypic characterization of strains nodulating Anthyllis vulneraria in mine tailings, and proposal of Aminobacter anthyllidis sp. nov., the first definition of Aminobacter as legume-nodulating bacteria. Systematic and Applied Microbiology, 35, 65–72.

    Article  CAS  Google Scholar 

  • Meyer, J. M., & Abdallah, M. A. (1978). The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Journal of General Microbiology, 107, 319–328.

    Article  CAS  Google Scholar 

  • Moreira, H., Marques, A. P. G. C., Franco, A. R., Rangel, A. O. S. S., & Castro, P. M. L. (2014). Phytomanagement of Cd-contaminated soils using maize (Zea mays L.) assisted by plant growth-promoting rhizobacteria. Environmental Science and Pollution Research, 21, 9742–9753.

    Article  CAS  Google Scholar 

  • Nascimento, F.X., Rossi, M.J., Soares, C.R.F.S., McConkey, B.J., & Glick, B.R. (2014). New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS ONE, 9. doi:10.1371/journal.pone.0099168.

  • Nautiyal, C. S. (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters, 170, 265–270.

    Article  CAS  Google Scholar 

  • Navarro-Noya, Y. E., Hernández-Mendozaa, E., Morales-Jiméneza, J., Jan-Robleroa, J., Martínez-Romerob, E., & Hernández-Rodríguez, C. (2012). Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Applied Soil Ecology, 62, 52–60.

    Article  Google Scholar 

  • Penrose, D. M., & Glick, B. R. (2003). Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiologia Plantarum, 118, 10–15.

    Article  CAS  Google Scholar 

  • Poly, F., Monrozier, L. J., & Bally, R. (2001). Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Research in Microbiology, 152, 95–103.

    Article  CAS  Google Scholar 

  • Rodríguez, H., & Fraga, R. (1999). Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances, 17, 319–339.

    Article  Google Scholar 

  • Römheld, V., & Marschner, H. (1986). Mobilization of iron in the rhizosphere of different plant species. Advances in Plant Nutrition, 2, 155–204.

    Google Scholar 

  • Salt, D. E., Smith, R. D., & Raskin, I. (1998). Phytoremediation. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 643–668.

    Article  CAS  Google Scholar 

  • Sessitsch, A., Kuffner, M., Kidd, P., Vangronsveld, J., Wenzel, W. W., Fallmann, K., & Puschenreiter, M. (2013). The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biology and Biochemistry, 60, 182–194.

    Article  CAS  Google Scholar 

  • Shaharoona, B., Arshad, M., & Zahir, Z. A. (2006). Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Letters in Applied Microbiology, 42, 155–159.

    Article  CAS  Google Scholar 

  • Shahzad, S. M., Khalid, A., Arshad, M., Tahir, J., & Mahmood, T. (2010). Improving nodulation, growth and yield of Cicer arietinum L. through bacterial ACC-deaminase induced changes in root architecture. European Journal of Soil Biology, 46, 342–347.

    Article  CAS  Google Scholar 

  • Soussou, S., Mahieu, S., Brunel, B., Escarré, J., Lebrun, M., Banni, M., Boussetta, H., & Cleyet-Marel, J. C. (2013). Zinc accumulation patterns in four Anthyllis vulneraria subspecies supplemented with mineral nitrogen or grown in the presence of their symbiotic bacteria. Plant and Soil, 371, 423–434.

    Article  CAS  Google Scholar 

  • Teixeira, C., Almeida, C. M. R., da Silva, M. N., Bordalo, A. A., & Mucha, A. P. (2014). Development of autochthonous microbial consortia for enhanced phytoremediation of salt-marsh sediments contaminated with cadmium. Science of the Total Environment, 493, 757–765.

    Article  CAS  Google Scholar 

  • Timmusk, S., Paalme, V., Pavlicek, T., Bergquist, J., Vangala, A., Danilas, T., & Nevo, E. (2011). Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS ONE, 6. doi:10.1371/journal.pone.0017968.

  • Valls, M., & de Lorenzo, V. (2002). Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiology Reviews, 26, 327–338.

    Article  CAS  Google Scholar 

  • van der Heijden, M. G. A., Bardgett, R. D., & van Straalen, N. M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters, 11, 296–310.

    Article  Google Scholar 

  • van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., & Sanders, I. R. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69–72.

    Article  Google Scholar 

  • Vidal, C., Chaintreuil, C., Berge, O., Maure, L., Escarre, J., Bena, G., Brunel, B., & Cleyet-Marel, J. C. (2009). Mesorhizobium metallidurans sp. nov., a metal-resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France. International Journal of Systematic and Evolutionary Microbiology, 59, 850–855.

    Article  CAS  Google Scholar 

  • Wardle, D. A., Bardgett, R. D., Klironomos, J. N., Setälä, H., van der Putten, W. H., & Wall, D. H. (2004). Ecological linkages between aboveground and belowground biota. Science, 304, 1629–1633.

    Article  CAS  Google Scholar 

  • Wawrik, B., Kerkhof, L., Zylstra, G. J., & Kukor, J. J. (2005). Identification of unique type II polyketide synthase genes in soil. Applied Environmental Microbiology, 71, 2232–2238.

    Article  CAS  Google Scholar 

  • Whiting, S. N., Reeves, R. D., Richards, D., Johnson, M. S., Cooke, J. A., Malaisse, F., Paton, A., Smith, J. A. C., Angle, J. S., Chaney, R. L., Ginocchio, R., Jaffré, T., Johns, R., McIntyre, T., Purvis, O. W., Salt, D. E., Schat, H., Zhao, F. J., & Baker, A. J. M. (2004). Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restoration Ecology, 12, 106–116.

    Article  Google Scholar 

  • Yu, X., Li, Y., Zhang, C., Liu, H., Liu, J., Zheng, W., Kang, X., Leng, X., Zhao, K., Gu, Y., Zhang, X., Xiang, Q., & Chen, Q. (2014). Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China. PLoS ONE, 9. doi:10.1371/journal.pone.0106618.

  • Zahir, Z. A., Zafar-ul-Hye, M., Sajjad, S., & Naveed, M. (2011). Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biology Fertility of Soils, 47, 457–465.

    Article  CAS  Google Scholar 

  • Zhang, W. H., Huang, Z., He, L. Y., & Sheng, X. F. (2012). Assessment of bacterial communities and characterization of lead-resistant bacteria in the rhizosphere soils of metal-tolerant Chenopodium ambrosioides grown on lead-zinc mine tailings. Chemosphere, 87, 1171–1178.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Financial support was provided by the ANR project SyMetal (grant number ANR-10-CESA-0006). The authors wish to thank M. Guy Delmot for his technical assistance on the experimental site without which the implementation of the phytostabilisation assays would not have been feasible.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ezékiel Baudoin.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 83 kb)

ESM 2

(PDF 64 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soussou, S., Brunel, B., Pervent, M. et al. Rhizobacterial Pseudomonas spp. Strains Harbouring acdS Gene Could Enhance Metallicolous Legume Nodulation in Zn/Pb/Cd Mine Tailings. Water Air Soil Pollut 228, 142 (2017). https://doi.org/10.1007/s11270-017-3309-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-017-3309-5

Keywords