Plant-microorganism combined bioremediation is an efficient tool to decontaminate contaminated soils, and seeking the best matching partners between plants and microorganisms that constitute the key for success in this process. The aims of the present work were to study the effects of inoculating plant growth-promoting bacterial mixtures and different mowing heights on plant development and U-uptake capacity.
Materials and methods
First, a total of 12 mixtures consisting of Bacillus mucitaginosus, Bacillus subtilis, Citrobacter Werkman and Gillen, Bacillus cereus Frankland, and Bacillus thuringiensis in different proportions were analyzed for indole-3-acetic acid (IAA), siderophores, and 1-aminocyclopropane-1-carboxylate (ACC) deaminase produced to screen as the inocula for phytoremediation. Second, three grass species, including Lolium multiflorum Lam., Lolium perenne L., and Dactylis glomerata L., were inoculated with the best bacterial inoculant mixtures that were M4 (10% Bacillus mucitaginosus, 20% Citrobacter Werkman and Gillen, 20% Bacillus thuringiensis), M10 (10% Bacillus mucitaginosus, 20% Bacillus subtilis, and 10% Bacillus cereus Frankland), and M12 (20% Bacillus mucitaginosus, and 10% Bacillus subtilis) selected from the first step experiment. In addition, mowing was adopted to assess the effects of mild mowing height, moderate mowing height, and heavy mowing height on U-uptake and grass growth.
Results and discussion
The results demonstrated that inoculation of M4 and M12 significantly improved the phytoextraction capability of three grass species along with influencing plant health and plant biomass. The extraction efficiency of L. perenne to U is higher than L. multiflorum and D. glomerata in the same concentration of U-contaminated soils. Compared with the two other plants inoculated with M12, the remediation effect of L. perenne was the best. Furthermore, we observed that moderate mowing height greatly influenced the plant growth and achieved a significant biomass harvest, thereby resulting in higher U-uptake compared with other treatments.
The present study demonstrated that inoculation of bacteria in combination with a mowing is an approach that can be exploited to improve the efficiency of phytoextraction.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Abhilash PC, Powell JR, Singh HB, Singh BK (2012) Plant-microbe interactions: novel applications for exploitation in multipurpose remediation technologies. Trends Biotechnol 30:416–420
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881
Amprayn KO, Rose MT, Kecskes M, Pereg L, Nguyen HT, Kennedy IR (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299
Anning AK, Akoto R (2018) Assisted phytoremediation of heavy metal contaminated soil from a mined site with Typha latifolia and Chrysopogon zizanioides. Ecotoxicol Environ Saf 148:97–144
Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. Sci Total Environ 319:13–25
Becerra-Castro C, Prieto-Fernández A, Álvarez-Lopez V, Monterroso C, Cabello-Conejo MI, Acea MJ, Kidd PS (2011) Nickel solubilizing capacity and characterization of rhizobacteria isolated from hyperaccumulating and non-hyperaccumulating subspecies of Alyssum serpyllifolium. Int J Phytoremediat 13:229–244
Bidar G, Garcon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553
Bonnet M, Camares O, Veisseire P (2000) Effects of zinc and influence of Acremonium lolii on growth parameters chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot 51:945–953
Braud A, Jézéquel K, Vieille E, Tritter A, Lebeau T (2006) Changes in extractability of Cr and Pb in a polycontaminated soil after bioaugmentation with microbial producers of biosurfactants, organic acids and siderophores. Water Air Soil Pollut 6:261–279
Bric JM, Bostock RM, Silversone SE (1991) Rapid in situ assay for indole acetic acid production by bacteria immobilization on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Burges A, Epelde L, Blanco F, Becerril JM, Garbisu C (2017) Ecosystem services and plant physiological status during endophyte-assisted phytoremediation of metal contaminated soil. Sci Total Environ 584-585:329–338
Caggiano R, D’Emilio M, Macchiato M, Ragosta M (2005) Heavy metals in ryegrass species versus metal concentrations in atmospheric particulate measured in an industrial area southern Italy. Environ Monit Assess 102:67–84
Carisse O, Bernier J, Benhamou N (2003) Selection of biological agents from composts for control of damping-off of cucumber caused by Pythium ultimum. Can J Plant Pathol 25:258–267
Chandra R, Kumar V (2017) Phytoextraction of heavy metals by potential native plants and their microscopic observation of root growing on stabilised distillery sludge as a prospective tool for in situ phytoremediation of industrial waste. Environ Sci Pollut Res Int 24:2605–2619
Chandra R, Yadav S (2011) Phytoremediation of Cd, Cr, Cu, Mn, Fe, Ni, Pb and Zn from aqueous solution using Phragmites cummunis, Typha angustifolia and Cyperus esculentus. Int J Phytoremediation 13:580–591
Chandra R, Kumar V, Tripathi S, Sharma P (2018) Heavy metal phytoextraction potential of native weeds and grasses from endocrine-disrupting chemicals rich complex distillery sludge and their histological observations during in-situ phytoremediation. Ecol Eng 111:143–156
Chen L, Luo S, Xiao X, Guo H, Chen J, Wan Y (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389
Chen X, Liu X, Zhang X, Cao L, Hu X (2017) Phytoremediation effect of Scirpus triqueter inoculated plant-growth-promoting bacteria (PGPB) on different fractions of pyrene and Ni in co-contaminated soils. J Hazard Mater 325:319–326
Dell'Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84
Gaonkar T, Bhosle S (2013) Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils. Chemosphere 93:1835–1843
Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39
Glick BR, Liu CP, Ghosh S, Dumbroff EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239
Gonzalez A, Loreau M (2009) The causes and consequences of compensatory dynamics in ecological communities. Annu Rev Ecol Evol Syst 40:393–414
Guarino C, Sciarrillo R (2017) Effectiveness of in situ application of an integrated phytoremediation system (IPS) by adding a selected blend of rhizosphere microbes to heavily multi-contaminated soils. Ecol Eng 99:70–82
Hardoim PR, Overbeek LSV, Elsas JDV (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471
Hugoa E, Saayman-Du Toit AEJ, Reinhardt CF (2014) Germination characteristics of the grass weed Digitaria nuda (Schumach.). S Afr J Bot 90:52–58
Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44
Kochar M, Srivastava S (2012) Surface colonization by Azospirillum brasilense SM in the indole-3-acetic acid dependent growth improvement of sorghum. J Basic Microbiol 52:123–131
Liu W, Wang Q, Wang B, Hou J, Luo Y, Tang C, Franks AE (2015) Plant growth-promoting rhizobacteria enhance the growth and Cd uptake of Sedum plumbizincicola in a Cd-contaminated soil. J Soils Sediments 15:1191–1199
Luo SL, Chen L, Chen JL, Xiao X, Xu TY, Wan Y, Rao C, Liu CB, Liu YT, Lai C, Zeng GM (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138
Ma Y, Rajkumar M, Luo Y, Freitas H (2013) Phytoextraction of heavy metal polluted soils using Sedum plumbizincicola inoculated with metal mobilizing Phyllobacterium myrsinacearum RC6b. Chemosphere 93:1386–1392
Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25
Malekzadeh E, Alikhani HA, Savaghebi-Firoozabadi GR, Zarei M (2012) Bioremediation of cadmium-contaminated soil through cultivation of maize inoculated with plant growth-promoting rhizobacteria. Bioremediat J 16:204–211
Meerts P, Grommesch C (2001) Soil seed banks in a heavy-metal polluted grassland at Prayon (Belgium). Plant Ecol 155:35–45
Melo D, Burkart W (2011) Uranium: environmental pollution and health effects. Encyclopedia Environ Health 36:526–533
Michael B, Štěpán J, Jitka K (2011) Effect of mowing and fertilization on biomass and carbohydrate reserves of Molinia caerulea at two organizational levels. Acta Oecol 37:299–306
Nriagu J, Nam DH, Ayanwola TA, Dinh H, Erdenechimeg E, Ochir C, Bolormaa TA (2012) High levels of uranium in groundwater of Ulaanbaatar, Mongolia. Sci Total Environ 414:722–726
Parham JA, Deng SP (2000) Detection, quantification and characterization of β-glucosaminidase activity in soil. Soil Biol Biochem 32:1183–1190
Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801
Rasmussena G, Olsenb RA (2004) Sorption and biological removal of creosote-contaminants from groundwater in soil/sand vegetated with orchard grass (Dactylis glomerata). Adv Environ Res 8:313–327
Robinson BH, Bañuelos G, Conesa HM, Evangelou MWH, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28:240–266
Safronova VI, Stepanok VV, Engqvist GL, Alekseyev YV, Belimov AA (2006) Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol Fertil Soils 42:267–272
Schwyn B, Neilands JB (1987) Universal chemical assay for detection and determination of siderophores. Anal Biochem 160:47–56
Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194
Shakur HR, Rezaee ESK, Abdi MR, Azimi G (2016) Selective removal of uranium ions from contaminated waters using modified-X nanozeolite. Appl Radiat Isot 118:43–55
Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170
Shimoda S (2017) Plant-derived carbon and nitrogen addition due to mowing in the early stages of post-agricultural succession. Ecol Eng 98:24–31
Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280
Tang J, Wang R, Niu X, Zhou Q (2010) Enhancement of soil petroleum remediation by using a combination of ryegrass (Lolium perenne) and different microorganisms. Soil Tillage Res 110:87–93
Vigliotta G, Matrella S, Cicatelli A, Guarino F, Castiglione S (2016) Effects of heavy metals and chelants on phytoremediation capacity and on rhizobacterial communities of maize. J Environ Manag 179:93–102
Wang XM, Liu WJ, Zhang LJ, Liu W, Bo-Wen LI, Yang ZX (2013) Effect of Bacillus megaterium and Bacillus mucilaginosus on soil DTPA extractable Cd. J Soil Water Conserv 27:217–221
Weyens N, VanderLelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
Wood JL, Tang C, Franks AE (2016) Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils. Soil Biol Biochem 103:131–137
Yang R, Li B, Liu W (2013) Effects of Bacillus mucilaginosus on soil pH and Cd accumulation by Brassica juncea. Acta Sci Circumst 33:1648–1654
Zareh MM, Aldaher A, Hussein AEM, Mahfouz MG, Soliman M (2012) Uranium adsorption from a liquid waste using thermally and chemically modified bentonite. J Radioanal Nucl Chem 295:1153–1159
The study was supported by the National Defense Science and Technology Foundation of China (Grant No. 16ZG6101), State Key Laboratory of NBC Protection for Civilian (SKLNBC2015–04), the Major State Development Program of China (973 Program, No.2014CB846003), Natural Science Foundation of Sichuan Province of China (Grant No. 18YYJC0927) .
Springer Nature remains neutral with regard to jurisdictionalclaims in published maps and institutional affiliations.
Responsible editor: Maria Manuela Abreu
About this article
Cite this article
Qi, X., Hao, X., Chen, X. et al. Integrated phytoremediation system for uranium-contaminated soils by adding a plant growth promoting bacterial mixture and mowing grass. J Soils Sediments 19, 1799–1808 (2019). https://doi.org/10.1007/s11368-018-2182-1
- Bacterial mixture
- Plant growth
- Soil contamination