Abstract
This study analyzed the application of three microorganism inoculums, including Bacillus subtilis, Bacillus cereus, and commercial effective microorganism (EM) solution in order to determine cadmium (Cd) reduction in rice (Oryza sativa L.) and rice growth promotion. Rice was grown in Cd-contaminated soil (120 mg/kg) and selected microorganisms were inoculated. Cd concentration and rice weight were measured at 45 and 120 days of the experiment. The result showed that B. subtilis inoculation into rice can highly reduce Cd accumulation in every part of rice roots and shoots (45 days), and grains (120 days). This species can effectively absorb Cd compared to other inoculums, which might be the main mechanism to reduce Cd transportation in rice plants. Interestingly, plants that were inoculated with bacterial species individually harbored higher calcium (Ca) and magnesium (Mg) accumulation; B. subtilis-inoculated plants had the highest levels of Ca and Mg compared to other inoculated ones. Moreover, inoculating rice plants with these microorganisms could increase the dry weight of the plant and protect them from Cd stress because all the inoculums presented the ability to solubilize phosphate, produce indole-3-acetic acid (IAA), and control ethylene levels by 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity. After 120 days, quantification of each inoculum by quantitative polymerase chain reaction (qPCR) confirmed the root colonization of bacterial species, with B. subtilis showing higher 16S rRNA gene copy numbers than the other species. B. subtilis was classified as a non-human pathogenic strain, reassuring the safe application of this plant growth-promoting bacterium as a crop inoculum.
Similar content being viewed by others
References
Ahemad M (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. 3 Biotech 5:111–121
Boparai HK, Joseph M, O’Carroll DM (2011) Kinetics and thermodynamics of cadmium ions removal by adsorption onto nano zerovalent iron particles. J Hazard Mater 186:458–465
Byers HK, Stackebrandt E, Hayward C, Blackall LL (1998) Molecular investigation of a microbial mat associated with the great artesian basin. FEMS Microbiol Ecol 25:391–403
Carter MR (1994) Soil sampling and method of analysis. Lewis Publishers, Boca Raton
Chakraborty U, Chakraborty BN, Chakraborty AP (2012) Induction of plant growth promotion in Camellia sinensis by Bacillus megaterium and its bioformulations. World Journal of Agricultural Sciences 8(1):104–112
Chaturvedi I (2004) Phytotoxicity of cadmium and its effect on two genotypes of Brassica juncea L. Emirates journal of agricultural sciences 16(2):01–08
Cho SC, Cho YY, Kao CH (2012) Calcium deficiency increase Cd to toxicity and Ca is required for heat-shock induced Cd tolerance in rice seedlings. J Plant Physiol 169:892–898
Chou TS, Cho YY, Huang WD, Hong CY, Kao CH (2011) Effect of magnesium deficiency on antioxidant status and cadmium toxicity. J Plant Physiol 168:1021–1030
Deng ZJ, Zhang RD, Shi Y, Hu LA, Tan HM, Cao LX (2014) Characterization of Cd-, Pb-, Zn-resistant endophytic sp. MXSF31 from metal accumulating and its potential in promoting the growth of rape in metal-contaminated soils. Environ Sci Pollut Res 21:2346–2357
Duan YQ, He ST, Li QQ, Wang MF, Wang WY, Zhe W, Cao YH, Mo MH, Zhai YL, Li WJ (2013) Lysinibacillus sp., Avicennia marina, a novel endophytic bacterium isolated from Nicotiana tabacum leaves. J Microbiol 51(3):289–294
Esringu A, Güneş A, Turan M, Karaman MR (2014) Roles of Bacillus megaterium in remediation of boron, lead, and cadmium from contaminated soil. Communication in soil science and plant analysis 45:1741–1759
Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400
Garg N, Bhandari P (2014) Cadmium toxicity in crop plants and its alleviation by Arbuscular mycorrhizal (AM) fungi: an overview. Plant Biosystems 148:609–621
Gordon SA, Weber RP (1951) Colorimetric estimation of indolacetic acid. Plant Physiol 26:192–195
Gutierrez-Segura S-RM, Colin-Cruz A, Fall C (2012) Adsorption of cadmium by Na and Fe modified zeolitic tuffs and carbonaceous material from pyrolyzed sewage sludge. The Journal of Environmental Management 97:6–13
Harmon M. E., Lajtha K., 1999. Analysis of detritus and organic horizons for minerals and organic constitutes. In: Robertson G. P., Coleman D. C., Bledsoe C. S., Sollins P. (eds) Standard soil method
Hilda R, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–359
Kashem MDA, Kawal S (2007) Alleviation of cadmium phyto toxicity by magnesium in Japanese mustard spinach. Soil Science and Plant Nutrition 53:246–251
Kathiresan K, Saravanakumar K, Sahu SK, Sivasankaran M (2014) Adenosine deaminase production by an endophytic bacterium (Lysinibacillus sp.) from Avicennia marina. 3 Biotech 4(3):235–239
Khaksar G, Siswanto D, Treesubsuntorn C, Thiravetyan P (2016a) Euphorbia milii-endophytic bacteria interactions affect hormonal levels of the native host differently under various airborne pollutants. Mol Plant-Microbe Interact 29:663–673
Khaksar G, Treesubsuntorn C, Thiravetyan P (2016b) Endophytic Bacillus cereus ERBP-Clitoria ternatea interactions: potentials for the enhancement of gaseous formaldehyde removal. Environ Exp Bot 126:10–20
Khaksar G, Treesubsuntorn C, Thiravetyan P (2016c) Effect of endophytic Bacillus cereus ERBP inoculation into non-native host: potentials and challenges for airborne formaldehyde removal. Plant Physiol Biochem 107:326–336
Khaksar G, Treesubsuntorn C, Thiravetyan P (2017a) Euphorbia milii-native bacteria interactions under airborne formaldehyde stress: effect of epiphyte and endophyte inoculation in relation to IAA, ethylene and ROS levels. Plant Physiol Biochem 111:284–294
Khaksar G, Treesubsuntorn C, Thiravetyan P (2017b) Impact of endophytic colonization patterns on Zamioculcas zamiifolia stress response and in regulating ROS, tryptophan and IAA levels under airborne formaldehyde and formaldehyde-contaminated soil conditions. Plant Physiol Biochem 114:1–9
Khaksar G, Treesubsuntorn C, Thiravetyan P (2017c) Effect of exogenous methyl jasmonate on airborne benzene removal by Zamioculcas zamiifolia: the role of cytochrome P450 expression, salicylic acid, IAA, ROS and antioxidant activity. Environ Exp Bot 138:130–138
Li T, Liu MJ, Zhang XT, Zhang HB, Sha T, Zhao ZW (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074
Lopez-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, Macías-Rodríguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant-Microbe Interact 20:207–217
Ma Y, Rajkumar M, Luo YM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237
Mastretta C, Taghavi S, Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2010) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. International iournal of phytoremediation. 11(3):251–267
McGrath SP, Cunliffe CH (1985) A simplified method for the extraction of the metals Fe, Zn, Cu, Ni, Cd, Pb, Cr, Co, Mn from soil and sewage sludges. J Sci Food Agric 36:794–798
Mehta P, Walia A, Kulshrestha S, Chauhan A, Shirkot CK (2015) Efficiency of plant growth-promoting P-solubilizing Bacillus circulans CB7 for enhancement of tomato growth under net house conditions. J Basic Microbiol 55:33–44
Meng X, Yan D, Long X, Wang C, Liu Z, Rengel Z (2014) Colonization by endophytic Ochrobactrum anthropic Mn1 promotes growth of Jerusalem artichoke. Microb Biotechnol 7:601–610
Mesa J, Mateos-Naranjo E, Caviedes MA, Redondo-Gómez S, Pajuelo E, Rodríguez-Llorente ID (2015) Endophytic cultivable bacteria of the metal bioaccumulator Spartina maritima improve plant growth but not metal uptake in polluted marshes soils. Front Microbiol 6:1450
Mohamed HM, Almaroai YA (2017) Effect of phosphate solubilizing bacteria on the uptake of heavy metals by corn plants in a long-term sewage wastewater treated soil. International journal of environmental science and development 8(5):366–371
Nazar R, Iqbal N, Masood A, Iqbal M, Khan R, Syeed S, Khan NA (2012) Cadmium toxicity in plants and role of mineral nutrients in its alleviation. Am J Plant Sci 3:1476–1489
Ortiz-Castro R, Martínez-Trujillo M, López-Bucio J (2008) N-acyl-L homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509
Ozturk L, Eker S, Ozkutlu F (2003) Effect of cadmium on growth and concentrations of cadmium, ascorbic acid and sulphydryl groups in durum wheat cultivars. Turk J Agric For 27:161–168
Phaenark C, Pokethitiyook P, Kruatrachue M, Ngernsansaruay C (2009) Cd and Zn accumulation in plant from the Padaeng zinc mine. International journal of phytoremediation 11:479–495
Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370
Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879
Rhoades JK (1982) Cation exchange capacity. In: Page AL (ed) Methods of soil analysis, part 2. Chemical and microbiological properties, 2nd edn. Agronomy Monograph 9, Madison (WI)
Sao V, Nakbanpote W, Thiravetyan P (2006) Cadmium accumulation by Axonopus compressus (Sw.) P. Beauv and Cyperus rotundas Linn growing in cadmium solution and cadmium-zinc contaminated soil. Songklanakarin journal of science and technology 29:881–892
Schmitz-Eiberger M, Haefs R, Noga G (2002) Calcium deficiency influence on the antioxidative defense system in tomato plants. J Plant Physiol 159:733–742
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
Simmons RW, Pongsakul D, Saiyasitpanich D, Klinphoklap S (2005) Elevated levels of cadmium and zinc in paddy soil and elevated of cadmium in rice grain downstream of a zinc mineralized area in Thailand: implications for public health. Environ Geochem Health 27:501–511
Siripornadulsil S, Siripornadulsil W (2013) Cadmium-tolerant bacteria reduce the uptake of cadmium in rice: potential for microbial bioremediation. Ecotoxicol Environ Saf 94:94–103
Suksabye P, Pimthong A, Dhurakit P, Mekvichitsaeng P, Thiravetyan P (2015) Effect of biochars and microorganisms on cadmium accumulation in rice grains grown in Cd-contaminated soil. Environ Sci Pollut Res 23(2):962–973
Swaddiwudhipong W, Limpatanachote P, Mahasakpan P, Krintratun S, Padungtod C (2007) Cadmium-exposed population in Mae Sot District, Tak Province: 1 prevalence of high urinary cadmium levels in the adults. J Med Assoc Thail 90:143–148
Tian S, Lu L, Zhang J, Wang K, Brown P, He Z, Liang J, Yang X (2011) Calcium protects roots of Sedum alfredii H. against cadmium induced oxidative stress. Chemosphere 84:63–69
Walkley A, Black CA (1934) An examination of degradation method for determining soil organic matter: a proposed modification of the chromic acid titration method. Soil Sci 37:29–35
Wang J, Li T, Liu G, Smith J, Zhao MZ (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Scientific Report 6:22–28
Wu J, Dumat C, Lu H, Li Y, Li H, Xiao Y, Zhuang P, Li Z (2015) Synergistic improvement of crop physiological status by combination of cadmium immobilization and micronutrient fertilization. Environ Sci Pollut Res 23:6661–6670
Yilmaz EI, Ensari NY (2005) Cadmium biosorption by Bacillus circulans strain EB1. World J Microbiol Biotechnol 21:777
Acknowledgements
The authors would like to thank the financial support provided by King Mongkut’s University of Technology Thonburi through the “Kmutt 55th Anniversary Commemorative fund” and National Research University Project of Thailand, Office of the higher Education Commission.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Robert Duran
Rights and permissions
About this article
Cite this article
Treesubsuntorn, C., Dhurakit, P., Khaksar, G. et al. Effect of microorganisms on reducing cadmium uptake and toxicity in rice (Oryza sativa L.). Environ Sci Pollut Res 25, 25690–25701 (2018). https://doi.org/10.1007/s11356-017-9058-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-9058-6